Diaphragmatic and lung ultrasound application as new predictive indices for the weaning process in ICU patients

Diaphragmatic and lung ultrasound application as new predictive indices for the weaning process in ICU patients The Egyptian Journal of Radiology and Nuclear Medicine xxx (2017) xxx–xxx Contents lists[.]

Original Article

Diaphragmatic and lung ultrasound application as new predictive

indices for the weaning process in ICU patients

Radiology Department – Anesthesia, ICU and Pain Management Department, Faculty of Medicine, Ain Shams University, Cairo, Egypt

a r t i c l e i n f o

Article history:

Received 16 November 2016

Accepted 13 January 2017

Available online xxxx

Keywords:

Diaphragmatic ultrasound (US)

Diaphragmatic excursion (E)

Diaphragmatic thickening fraction (DTF)

Weaning process

Intensive care unit (ICU)

a b s t r a c t

Objective: To assess whether the diaphragmatic and lung ultrasound (US) can be used as additive new parameters for the weaning process in intensive care units (ICU) patients in comparison to the traditional weaning parameters

Patients and methods: 68 patients were included in our study All patients admitted inside different ICU units-Ain Shams University for different causes mainly post major surgeries All patients met the tradi-tional criteria for weaning, had diaphragmatic and lung ultrasound after extubation We measured the diaphragmatic excursion (E), diaphragmatic thickening fraction (DTF) as well as the degree of lung aer-ation All US results were collected and compared with some of usual weaning parameters namely the arterial blood gases as well as respiratory mechanics The results were statistically analyzed

Results: 50 patients showed successful weaning process Diaphragmatic E and TF showed high sensitivity and specificity in correlation with the other parameters The cut off value was 10 mm for the E and 28% for the DTF and 12 for the lung US A score was put to predict the outcome of weaning process Conclusion: For the patients undergoing weaning process, diaphragmatic and lung ultrasound can be used as additive new parameters for prediction of weaning process outcome

Ó 2017 The Egyptian Society of Radiology and Nuclear Medicine Production and hosting by Elsevier This

is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/

4.0/)

1 Introduction

The mechanical ventilation using pressure-supported technique

is widely used in critically ill-patients inside the intensive care

units (ICU)[1] 20% of the patients inside the ICU show difficulties

in weaning process while 40% of them experiences much time in

ICU during weaning trials[2,3]

Multiple indices were built up to assess the patients’ ability to

regain spontaneous breathing such as[4,5]:

– Minute ventilation (Ve)

– Maximum inspiratory pressure (MiP)

– Breathing frequency

– Rapid shallow breathing index (RSBI) = respiratory frequency/

tidal volume which is one of the most accurate index

– Tracheal air way occlusion pressure

– Compliance, rate, oxygen pressure index (CROP)

– Esophageal and gastric pressure

The diaphragm is the main respiratory muscle with prolonged mechanical ventilation can lead to impaired diaphragmatic func-tion secondary to atrophy and prolonged dysfuncfunc-tion with subse-quent difficult weaning process[1,6]

Preserved diaphragmatic function is very important during weaning process to regain spontaneous breathing process with the usual methods for diaphragmatic assessment like fluoroscopy, phrenic nerve conduction, and trans-diaphragmatic pressure mea-surements show a lot of limitations and disadvantages especially inside the ICU due to ionizing radiation exposure, not widely avail-able methods and the need for patient transportation[7]

US is a well established bedside radiological tool with multiple trials were done to assess the useful of its use in estimation of the diaphragmatic function[8,9] Two different parameters have been described for diaphragmatic US namely the diaphragmatic excur-sion (E) during inspiration and diaphragmatic muscle thickening fraction (DTF)

Also, lung US can be used in assessment of lung aeration which can be useful and helpful during the weaning process as it reflect the aeration loss and subsequently predict the post extubation dis-tress[10]

The aim of this work is to assess the ability to use diaphrag-matic and lung US as new additive parameters to predict the

http://dx.doi.org/10.1016/j.ejrnm.2017.01.005

0378-603X/Ó 2017 The Egyptian Society of Radiology and Nuclear Medicine Production and hosting by Elsevier.

This is an open access article under the CC BY-NC-ND license ( http://creativecommons.org/licenses/by-nc-nd/4.0/ ).

Peer review under responsibility of The Egyptian Society of Radiology and Nuclear

Medicine.

⇑ Corresponding author.

E-mail address: Dr_osman80@yahoo.com (A.M Osman).

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The Egyptian Journal of Radiology and Nuclear Medicine

j o u r n a l h o m e p a g e : w w w s c i e n c e d i r e c t c o m / l o c a t e / e j r n m

outcome of weaning process in comparison with other weaning

parameters

2 Patients and methods

2.1 Patients

This is a prospective study conducted over 68 patients who

admitted in different ICU units – Ain Shams University with

differ-ent causes with the majority of cases were selected post

opera-tively All patients were mechanically ventilated through a

tracheostomy or endotracheal tube Written consents were taken

from the patients’ guardians or their relative to participate in this

study according to the rules of ethical committee The study

con-ducted over the period from August 2015 to August 2016

2.2 The criteria of weaning

All ICU patients who met the criteria to start weaning process

according toTable 1were included in this study

2.3 Exclusion criteria

 Patients < 18 years old

 Any patient with known neuromuscular disorder

 Any patient with primary US revealed unilateral/bilateral

absent diaphragmatic mobility

 Any patient with post esophageal or thoracic surgeries due to

intra-operative diaphragmatic manipulation

2.4 Study design

The patients who selected to start weaning according the

crite-ria shown inTable 1 were disconnected from the ventilators to

allow spontaneous breath trial (SBT) Each diaphragm was

evalu-ated to rule out absent diaphragmatic mobility in either side; when

detected the patient was excluded from the study This followed by

complete diaphragmatic and lung US

2.5 Diaphragmatic US

 US machines: Logic E9 (GE) and Honda electronics HS-2100

Por-table ultrasound machine 3.5 MHz convex probe as well as 9–

11 MHz linear probe were used

 Patient position: Semi-recumbent position

 Diaphragmatic thickness assessment: The linear US probe was

placed intercostally perpendicular to the chest wall in the 8th

or 9th intercostals space between the anterior and mid axillary

line The diaphragm appeared as three layered structure (two

parallel echogenic lines representing the pleura and the

peri-toneum with central hypoechoic space representing the

diaphragmatic muscle) The diaphragmatic thickness was

measured from the middle of the pleural line to the middle of the peritoneal line The thickness was measured during the end inspiration and the end expiration This was repeated to take the average followed by DTF calculation = (Thickness at the end inspiration – thickness at the end expiration)/Thickness

at the end expiration

 Diaphragmatic excursion (E): The convex probe is placed sub-costally parallel to the inetrcostal space to measure the range

of the diaphragmatic movement using M-mode method with the cursor crossing the diaphragm and assess the high and low peak points as indicator for the diaphragmatic mobility range

2.6 Lung ultrasound

 Patient position: supine and lateral decubitus positions

 Technique: Each lung was divided into 3 zones underwent examination anteriorly and posteriorly using B-mode to assess the degree of lung aeration with total 12 zones to be examined

 Image interpretation and lung US score: (Table 2)

2.7 Analysis of data The patients were divided into two groups according to their response to weaning trials with group A showed successful wean-ing (SW) and transferred to the ward while group B showed failed weaning (FW) followed by re-intubation and machine ventilation after 48 h The diaphragmatic E, DTF and lung US measurements were collected for each group and correlated with some selected weaning criteria namely; PaO2, PaCO2, Respiratory rate (RR), max-imum inspiratory force (MiP) and Rapid shallow breath index (RSBI),

The analysis data was done using IBM SPSS (Statistical Program for Social Science version 24.0, IBM Corp., USA, 2016) Data were expressed as Mean ± SD for quantitative parametric measures The following tests were done:

1 Comparison between two independent mean groups for para-metric data using Student t test

2 Pearson correlation test to study the possible association between each two variables among each group for parameteric data

The probability of error at 0.05 was considered sig., while at 0.01 and 0.001 are highly sig

3 Diagnostic validity test: diagnostic sensitivity, specificity, nega-tive and posinega-tive predicnega-tive values (NPV, PPV) and efficacy Finally scoring system was put to use diaphragmatic E, DTF and lung US during the weaning process

Table 1

Illustrates the selective criteria to start the weaning for the ICU patients.

Arterial blood gases

(ABG)

Respiratory rate Respiratory mechanics

 PaO 2 > 60 mmHg

 Pa CO 2 < 50 mmHg

 FiO 2 < 0.5

 PaO 2 /FiO 2 > 200 mg

 PEEP < 5 CmH 2 O

<30–35 breath/min  Tidal volume (TV) > 5 ml/kg

 Vital capacity (VC) > 10 ml/kg

 PI max < 15 to 30 CmH 2 O

 Ve 4–10 L/min

 RSBI < 100 breath/min/L

 P0.1 < 2 CmH 2 O

Table 2 Illustrates the lung US score for detection of the degree of lung aeration (10) Points for each lung

zone (12 zones)

Degree of lung aeration

Pattern

aeration

Horizontal A-line (no more than two B-line)

of aeration

Multiple B-line either regularly spaced or irregularly spaced

2 points Severe loss of

aeration

Multiple coalescent B-lines

of aeration

Lung consolidation Total score From 0 to 36

3 Results

The study was conducted over 68 patients, their ages ranged

between 45 years old and 65 years old with a mean age 56 years

50 patients showed success weaning process representing group

A (SW) forming 73.5% while 18 patients failed weaning and

re-intubated after 48 h from the trial representing group B (FW)

forming 26.5% The results of the different US parameters, blood

gases and respiratory mechanics mainly the mean value, t-value

as well as the significance are illustrated inTables 3 and 4 Regarding the diaphragmatic E, all patients with diaphragmatic

E above value 22 mm showed successful weaning while all patients below 11 mm showed failed weaning The values between 11 mm

to 22 mm showed 7 cases from group A (SW) and 3 cases from group B (FW).10 mm was the cut off value with 83.3% sensitivity, 100% specificity, 94.3% negative predictive value and 100% positive predictive value It showed 95.6% efficacy with significant correlation with other parameters mainly the RSBI and MiP (Figs 1–3 and 6) The area under curve (AUC) was 0.833

The DTF showed that; all patients with DTF values above 31% showed successful weaning while all patients with DTF below 29% showed failed weaning The patients with DTF values between 29% and 31% showed success weaning among 5 patients and failed weaning among 2 cases 28% a cut off value showed 88.9% sensitiv-ity, 100% specificsensitiv-ity, 96.2% negative predictive value and 100% pos-itive predictive value It showed 97.1% efficacy with significant correlation with other parameters mainly the RSBI and MiP (Figs 1,

2, 4 and 6) The area under curve (AUC) was 0.889

Table 3

Illustrates the different US parameters, blood gases and respiratory mechanics results in between the two groups, group A (success weaning) and group B (failed weaning).

Group A (success weaning)(SW) Group B (failed weaning)(FW) t-value Sig.

E = Excursion DTF = Diaphragmatic thickness fraction RR = respiratory rate MiP = maximum inspiratory pressure RSBI = Rapid shallow breathing index.

Table 4

Shows suggested score system for the diaphragmatic E, DTF and lung US when used as

weaning parameters.

High probability of

success weaning

Intermediate probability

High probability for failed weaning Diaphragmatic

E score

Fig 1 A male patient 50 years old admitted in ICU following gastric surgery Weaning trial started 4 days after admission A The diaphragmatic E was about 29 mm in average B The diaphragm thickness at end inspiration was about 4 mm in average while at end expiration was about 3 mm in average with DTF = 33% The weaning process completed and the patient was transferred to the ward after two days.

Lastly, the pleural US with cut off value 12 showed 100%

sensi-tivity, 96% specificity, 100% negative predictive value and 90%

pos-itive predictive value It showed 97.1% efficacy with highly

significant correlation with the other parameters The area under

curve (AUC) was 0.942 (Figs 5 and 6)

According to the previous results; a score was put for both the

Diaphragmatic E and DTF as well as the lung US when used as

weaning parameters as follow (Table 3)

4 Discussion

The weaning process of ICU patients is a complex process with

an estimated 20% failure rate[3] The weaning process start

deci-sion depends on multiple indices and parameters mainly the

arte-rial blood gases and the respiratory mechanics with all parameters reflecting the diaphragmatic function in an indirect manner Wrong decision in weaning start with high failure rate leads to cardio-respiratory distress, prolonged ICU admission and increase mortality rates Also, the delay in weaning decision increase the risk of ventilator associated pneumonia and diaphragmatic atro-phy[11,12]

US which is widely available inside the ICU; provide direct, bed side and rapid visualization and assessment of the diaphragmatic mobility and diaphragmatic function as the main respiratory mus-cle which may be used as indicator for the weaning outcome

In our study, 18 patients experienced failed weaning trial and underwent re-intubation and re-ventilated mechanically within

48 h representing 26.5% of the study population This is almost

Fig 2 A male patient 62 years old admitted in ICU following radical cystectomy surgery Weaning trial started 6 days after admission A The diaphragmatic E was about

6 mm in average B The Diaphragm thickness at end inspiration was about 2.5 mm in average while at end expiration was about 2 mm in average with DTF = 25% The weaning process failed and the patient was re-intubated 48 h after starting weaning trial.

Fig 3 Illustrates the values of the diaphragmatic E between group A and group B.

consistent with Esteban et al Saeed et al and Baess et al who

showed failure rate about 20%, 26.7% and 23.3% respectively

[2,13,14] This is in controversy to Ferrari et al who reported 63%

failure rate[6] This is explained due to non uniform rule in study

population selection with different causes for mechanical

ventila-tion as well as different ventilaventila-tion periods before starting weaning

process which may affect the outcome of the weaning process

We used M-mode to evaluate the diaphragmatic E and to assess

the degree of mobility as it was easier than the B-mode during

dealing with non cooperative ICU patients M-mode was also used

by multiple authors for example Umbrello et al Baess et al and

Boussuges et al with the latter one studies the role of M-mode

in evaluation the diaphragmatic mobility among 210 healthy

indi-viduals[1,14,15] While some author studied the mobility using

B-mode as Saeed et al whose study showed non ICU patients

facili-tating the use of B-mode in assessment of the diaphragmatic

mobility[13]

Our results were correlated with many weaning parameters including blood gases and respiratory mechanics as seen inTable 3 with RSBI was one of the most widely used parameter by the other authors for comparison [1,13,14] In the present study, the RSBI was ranging between 50 and 97 breath/min/L between group A (SW) with 71.6 average value while ranging between 105 and

125 breath/min/L between group B (FW) with 113.9 average value Saeed et al found that average RSBI = 91 between patients with success weaning and became 123.6 between patients with failed weaning[13] DTF, E and lung US showed significant to high signif-icant correlation with the other parameters including the arterial blood gases as well as the respiratory mechanics mainly the RSBI and MiP and this is similar to other previous trials[6,13,14]

In the present study, 10 mm Diaphragmatic E was the cut off value with 83.3% sensitivity and 100% specificity This is consistent with many authors who reported 10–11 mm Diaphragmatic E as a cut off value in assessment of the weaning outcome with different

Fig 5 Illustrates the value of lung US score between group A and group B Notice that all patients with lung US score above 17 (line A) showed failed weaning while patients with score below 13 (line B) showed successful weaning All patients with score between 13 and 17 showed 2 cases belonging to group A and 1 case belonging to group B.

Fig 4 Illustrates the values of the DTF between group A and group B.

degrees of sensitivity and specificity Saeed et al reported 86.4%

sensitivity and 87.5% specificity while Baess et al found 69.5%

sen-sitivity and 71.4% specificity Also, Jiang et al reported 84% and 83%

sensitivity and specificity respectively[13,14,16,17]

Regarding the DTF, The cut off value of 28% showed 88.9%

sen-sitivity, 100% specificity in our study This is close to Baess et al

and Di Nino et al who reported 30 % DTF cut off value yet with

sen-sitivity about 69.57%, 88% and specificity about 71.43%, 71%

respectively [14,18] This is in controversy to Ferrari et al who

reported higher cut off value = 36% with 82% sensitivity and 88%

specificity[6] Also, Umbrello et al found lesser cut off value = 20%

[1]

Although there are minor changes regarding the diagnostic

validity results comparing with the previous trials, yet all approve

that E and DTF are good indicators for weaning outcome The DTF

was more reliable than E with higher sensitivity and higher efficacy

and better AUC score consistent with Umbrello et al and Baess

et al [1,14] Also, the finding of lung ultrasound was consistent

with Soummer et al as well as Caltabeloti and Rouby[10,19]

Finally, ultrasound score was generated which can be helpful

and of value when used during the weaning trials with high

sensi-tivity and specificity comparable with the other weaning

parame-ters The US characterize by being rapid, non invasive and widely

available However, the main limitation was being operator

dependable technique and also, the ultrasound technique

limita-tions such as presence of pneumothorax as well as the morbid

obe-sity interfering with best window for diaphragm visualization

5 Conclusion

Diaphragmatic and lung ultrasound provide rapid and non

inva-sive indices for weaning process with high accurate results in

com-parison to the other traditional indices as blood gases and the

respiratory mechanics So, they can be used as predictive

parame-ters to assess the weaning process outcome

References

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[12] Hudson MB, Smuder AJ, Nelson WB, et al Both high level pressure support ventilation and controlled mechanical ventilation induce diaphragm dysfunction and atrophy Crit Care Med 2012;40(4):1254–60

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[14] Baess A, Abdallah TH, Emara DM, et al Diaphragmatic ultrasound as a predictor of successful extubation from mechanical ventilation: thickness, displacement, or both? Egypt J Bronchol 2016;10:162–6

[15] Boussuges A, Gole Y, Blanc P Diaphragmatic motion studied by m-mode ultrasonography: methods, reproducibility, and normal values Chest 2009;135(2):391–400

[16] Jiang JR, Tsai TH, Jerng JS, et al Ultrasonographic evaluation of liver/spleen movement and extubation outcome Chest 2004;126(1):179–85

[17] Kim WY, Suh HJ, Hong SB, et al Diaphragm dysfunction assessed by ultrasonography: influence on weaning from mechanical ventilation Crit Care Med 2011;39(12):2627–30

[18] Di Nino E, Gartman EJ, Sethi JM, et al Diaphragm ultrasound as a predictor of successful extubation from mechanical ventilation Thorax 2014;69(5):423–7 [19] Caltabeloti FP, Rouby JJ Lung ultrasound: a useful tool in the weaning process? Rev Bras Ter Intensiva 2016;28(1):5–7

Fig 6 Illustrates the diagnostic validity including the sensitivity (sen.), specificity (spec.), negative predictive value (NPV), positive predictive value (PPV) and efficacy for the cut off value of different US parameters.