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REVIEW

CURRENT
OPINION The differential diagnosis for failure to wean from
mechanical ventilation
Jonne Doorduin, Johannes G. van der Hoeven, and Leo M.A. Heunks

Purpose of review
In this review, we discuss the causes for a failed weaning trial and specific diagnostic tests that could be
conducted to identify the cause for weaning failure. We briefly highlight treatment strategies that may
enhance the chance of weaning success.
Recent findings
Impaired respiratory mechanics, respiratory muscle dysfunction, cardiac dysfunction, cognitive dysfunction,
and metabolic disorders are recognized causes for weaning failure. In addition, iatrogenic factors may be
at play. Most studies have focused on respiratory muscle dysfunction and cardiac dysfunction. Recent
studies demonstrate that both ultrasound and electromyography are valuable tools to evaluate respiratory
muscle function in ventilated patients. Sophisticated ultrasound techniques and biomarkers such as B-type
natriuretic peptide, are valuable tools to identify cardiac dysfunction as a cause for weaning failure. Once
a cause for weaning failure has been identified specific treatment should be instituted. Concerning
treatment, both strength training and endurance training should be considered for patients with respiratory
muscle weakness. Inotropes and vasodilators should be considered in case of heart failure.
Summary
Understanding the complex pathophysiology of weaning failure in combination with a systematic
diagnostic approach allows identification of the primary cause of weaning failure. This will help the
clinician to choose a specific treatment strategy and therefore may fasten liberation from mechanical
ventilation.
Keywords
cardiac failure, diaphragm, differential diagnosis, mechanical ventilation, weaning

INTRODUCTION the clinician to identify the cause for weaning


Weaning from mechanical ventilation covers the failure. Finally, we briefly discuss new treatment
entire process of liberating a patient from the venti- strategies that may fasten liberation from mechan-
lator and the endotracheal tube [1]. Weaning failure ical ventilation.
is usually defined as an unsuccessful spontaneous
breathing trial (SBT) or need for ventilator support
CAUSES OF WEANING FAILURE
(including noninvasive ventilation) within 48 h
after extubation [1]. In patients that require more The transition from positive inspiratory pressure
than 7 days of weaning after a first failed SBT, during mechanical ventilation to negative airway
mortality is significantly increased (13 vs. 7% of pressure during spontaneous breathing challenges
patients that need shorter weaning time [2]). The the patients’ physiological reserve. When an
pathophysiology of a failed weaning trial may be
complex, but it is in our opinion important to
Department of Critical Care Medicine, Radboud University Nijmegen
understand the reason for a failed weaning trial. Medical Center, The Netherlands
Identification of the cause of weaning failure will Correspondence to Leo M.A. Heunks, MD, PhD, Department of Critical
help the clinician to choose a rationale treatment Care Medicine, Radboud University Nijmegen Medical Center, Geert
strategy that improves the chances of success for the Grooteplein zuid 10, 6525 GA Nijmegen, The Netherlands. Tel: +31 24
next weaning trial. The aim of this study is to 36 17273; fax: +31 24 35 41612; e-mail: Leo.Heunks@radboudumc.nl
summarize the differential diagnosis of a failed Curr Opin Anesthesiol 2016, 29:150–157
weaning trial and discuss recent studies that help DOI:10.1097/ACO.0000000000000297

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The differential diagnosis for failure to wean Doorduin et al.

lungs and the chest wall. In a population of ARDS


KEY POINTS patients, compliance was found to be lower in the
 Withdrawal of positive inspiratory pressure during a failure group compared to successful weaning [4].
SBT challenges the patients’ cardiac, respiratory, Lung compliance may be reduced because of
neurological, and endocrine physiological reserve. alveolar filling (edema or pus), atelectasis, intersti-
tial lung disease, pulmonary fibrosis, and hyper-
 New diagnostic tools, including ultrasound, EMG, and
inflation. Pleural effusion, edema, obesity, and
plasma biomarkers help the clinician to narrow the
differential diagnosis of a failed weaning trial. elevated abdominal pressure decrease chest wall
compliance. Measurement of esophageal pressure
 Identification of the cause for weaning failure helps the (Pes) is required to differentiate lung compliance
clinician to design a rationale treatment strategy that from chest wall compliance. However, in clinical
may fasten liberation from mechanical ventilation.
practice when total respiratory compliance is
decreased clinical and/or radiological work-up will
generally identify the cause of reduced compliance.

imbalance develops between the patients’ venti-


latory needs and capacity, weaning fails. Below we Respiratory muscle dysfunction
will discuss the causes of weaning failure and the Critical illness has profound effects on respiratory
techniques that are most helpful in the diagnostic muscle structure and function [7], Rapid develop-
work-up. ment of diaphragm weakness, indicated by approxi-
mately a third reduction in diaphragm force, was
found in the first 5–6 days of invasive mechanical
Impaired respiratory mechanics ventilation in a small group of critically ill patients
The load imposed upon the respiratory muscles [8]. Diaphragm muscle fiber cross-sectional area is
is determined by the resistance and compliance of reduced by 25% in critically ill patients ventilated
the respiratory system and the presence of intrinsic for 7 days compared with patients referred for
positive end-expiratory pressure (PEEPi). An elective surgery [9]. In addition, in-vitro force gener-
increase in load is accompanied by an increase in ation of these fibers was severely reduced compared
work of breathing and as such may lead to weaning
&&
to controls. Goligher and colleagues [10 ] found
failure. Indeed airway resistance is higher in patients that in 44% of the ventilated ICU patients’ dia-
failing a weaning trial [3,4]. In the upper airways, phragm thickness, as assessed by ultrasound,
resistance may be increased by the artificial airway decreased by more than 10% in the first week on
and/or tracheal injury, including stenosis, tracheo- the ventilator. The reduction in diaphragm thick-
malacia, and granulation tissue. In tracheostomized
&&
ness was associated with weakness [10 ].
patients with weaning failure referred to a dedicated Clinical evaluation of respiratory muscle func-
weaning center, endoscopy revealed significant tra- tion in ventilated critically ill patients is a challenge.
cheal stenosis (>50% of tracheal lumen) in 5% Previously, we discussed the available techniques in
(14/288) of the patients [5]. Total 10 of these
&
detail [11 ,12]. Here, we will briefly discuss clinically
14 patients could be successfully decannulated after relevant and feasible techniques. Maximal inspira-
removal of granulation tissue. tory pressure and maximal expiratory pressure are
The presence of elevated small airway resistance tests of global respiratory muscle strength and can
is obvious in patients with chronic obstructive pul- be measured using a hand-held device connected to
monary disease (COPD) or asthma, but in acute the artificial airway. A maximal inspiratory pressure
respiratory distress syndrome (ARDS) airway resist- above 30 cmH2O is associated with a shorter time to
ance may be increased as well because of edema of the successful extubation [13]. Simultaneous recording
bronchial wall. As a result of increased airway resist- of Pes and gastric pressure (Pga) using dedicated
ance, expiratory flow is limited and consequently balloons allows calculation of transdiaphragmatic
PEEPi may develop. PEEPi elevates work of breathing pressure (Pdi ¼ Pga  Pes), a specific measure of dia-
via hyperinflation and by acting as a threshold for phragm contractility. The latter is useful for close
generation of inspiratory flow. Under dynamic con- monitoring and evaluation of diaphragm function
ditions, PEEPi can be determined only by using an in difficult-to-wean patients (Table 1). However, as
esophageal balloon. Although these balloons are mentioned before, acquisition and interpretation of
widely available, positioning of the catheter and Pes, Pga, and their derived measures, such as work of
&
interpretation of the signal is subject to pitfalls [6 ]. breathing, requires expertise.
The compliance of the respiratory system is Diaphragm ultrasonography is a practical and
determined by the elastic properties of both the noninvasive tool for assessment of diaphragm

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Intensive care and resuscitation

Table 1. Respiratory effects of a spontaneous breathing trial

Resp rate Edi DPes DPga DPdi PEEPi WOB PaO2 PaCO2
(per min) Vt (ml) (mV) (cm H2O) (cm H2O) (cm H2O) (cm H2O) (J/l) (mmHg) (mmHg)

PSa 34 211 20 12 1 13 5 1.0 75 56


5 min 36 246 48 25 1 26 10 2.1 61 56
10 min 37 260 43 24 2 26 9 2.0
60 min 23 352 52 30 2 32 10 2.6 70 57

Succesfull spontaneous breathing trial in a COPD patient despite an increase in PEEPi and WOB. COPD, chronic obstructive pulmonary disease; Edi, electrical
activity of the diaphragm; PaCO2, arterial carbondioxide partial pressure; PaO2, arterial oxygen partial pressure; Pdi, transdiaphragmatic pressure; PEEPi,
intrinisic positive end-expiratory pressure; Pes, esophageal pressure; Pga, gastric pressure; Resp rate, respiratory rate; Vt, tidal volume; WOB, work of breathing.
a
PS ¼ 5 cm H2O, PEEP ¼ 10 cm H2O.

thickness, thickening fraction, and displacement asynchrony [16], and assessment of respiratory
(Fig. 1). Using M-mode ultrasonography, diaphrag- workload [17,18].
matic dysfunction (vertical excursion <1 cm or par- Diaphragm electromyography (EMG) reflects
adoxic movements) was found in 24 of 82 patients neural respiratory drive to the diaphragm. The
who met criteria for an SBT [14]. These patients (processed) EMG signal can be obtained continu-
showed frequent early and delayed weaning ously using commercially available multielectrode
failures. DiNino and colleagues [15] found in esophageal catheters required for neurally adjusted
63 mechanically ventilated patients that dia- ventilatory assist ventilator mode (Maquet, Solna,
phragm thickening fraction above 30% predicts Sweden). The ratio between diaphragm EMG and
extubation success with a sensitivity and specificity tidal volume is called the neuro-ventilatory effi-
of 88 and 71%, respectively. Very recently, it was ciency (NVE). NVE has been shown to identify
proposed that thickening fraction of the diaphragm weaning failure in multiple studies [19–22].
as assessed with ultrasound could be used to detect Evidently, NVE is sensitive to changes in diaphragm
&&
dysfunction [10 ]. Future fields of ultrasonography function as well as a patient’s load of breathing.
application may be detection of patient-ventilator Diaphragm EMG may also be used to monitor

Expiration Inspiration
SC SC

ICS ICS
Dia
Dia
1.6 mm 2.4 mm

Liver Liver

Ultrasonography measurements:
Liver

- Thickness exp. = 1.6 mm


21

- Thickness insp. = 2.4 mm


Exp Insp Exp
- Thickness fraction = (2.4–1.6)/
1.6 = 50%
Liver 2.3 Cm - Displacement = 2.3 cm
A Lung

FIGURE 1. Normal diaphragm ultrasonography. From left-to-right, top-to-bottom: B-mode diaphragm thickness during
expiration, B-mode diaphragm thickness during inspiration, M-mode diaphragm displacement during normal inspiration,
measurements obtained from images. Dia, diaphragm; exp, expiration; ICS, intercostals muscles; insp, inspiration; SC,
subcutis.

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The differential diagnosis for failure to wean Doorduin et al.

respiratory muscle unloading [23], patient-venti- transmitral early diastolic filling velocity (E),
lator interaction [24], and the effect of residual measured by conventional pulsed wave Doppler,
sedation on respiratory drive [25]. In a preliminary the resulting E/Ea ratio closely correlates with left
observation, it was reported that diaphragm EMG ventricular filling pressure [30]. Moschietto and col-
can be used to detect development of fatigue after leagues [29] found in a nonselected population of
extubation [26]. 68 patients, performing an SBT, that the E/Ea ratio
before and during the SBT was higher in the failure
group than in the successful group. In this study, an
Cardiac dysfunction E/Ea ratio during the SBT of 14.5 predicted weaning
The lungs and heart are functionally and anatom- failure with a sensitivity of 75% and a specificity of
ically coupled and therefore transition of assisted 95.8%. It should be recognized that performing
breathing to unassisted breathing has profound ultrasound at the time of weaning failure might
cardiovascular effects that may induce weaning fail- be quite a challenge.
ure. First, during positive pressure ventilation the B-type natriuretic peptide (BNP) and N-terminal
intra-thoracic pressure (ITP) increases during inspi- (NT)-proBNP are cardiac biomarkers secreted by
ration, whereas during unassisted breathing ITP ventricular cardiomyocytes in response to increased
decreases during inspiration as a result of activation ventricular wall stress. Increases in BNP and
of the inspiratory muscles. The decrease in ITP NT-proBNP levels during the SBT are consistent with
during a weaning trial will enhance venous return weaning failure of cardiac origin, in which BNP
&&
by reducing right atrial pressure, end diastolic right performs better than NT-proBNP [31,32 ]. An
ventricular (RV) volume and as such in patients with increase in BNP levels by more than 12% allowed
normal cardiac function increase RV and left ven- diagnosing weaning failure from cardiac origin with
tricular (LV) output, but may result in heart failure a sensitivity of 76% and a specificity of 78%, with
in patients with compromised cardiac function. the pulmonary artery catheter as a reference method
&&
Second, increased sympathic tone (emotional stress, [32 ]. Mekontso Dessap and colleagues [33] showed
hypercapnia, and hypoxemia) may further increase that a BNP-guided fluid management strategy was
LV afterload. Finally, the transition to unassisted associated with a shorter duration of mechanical
breathing puts an elevated load on the respiratory ventilation, especially in patients with left ventric-
muscles, which increases oxygen consumption and ular systolic dysfunction. In conclusion, changes in
as such is a stress to the heart. The final effects of BNP levels are a reliable and feasible alternative to
unassisted breathing on the cardiovascular system the pulmonary artery catheter for diagnosing wean-
are much more complex. We refer to recent studies ing-induced pulmonary edema. A passive leg raising
&
for review [27 ,28]. Table 2 shows the cardiovascular before the SBT has also been suggested to identify
effects of a successful prolonged spontaneous weaning failure patients related to cardiac dysfunc-
&
breathing trial in a typical ICU patient. tion [34]. Recently, Dres and colleagues [27 ] devel-
As an alternative to the pulmonary artery oped an algorithm for management of weaning
catheter, less invasive techniques are currently used failure from cardiac origin.
to identify cardiac failure during a weaning trial.
Transthoracic echocardiography during an SBT can
identify both systolic and diastolic dysfunction [29]. Cognitive dysfunction
With tissue Doppler imaging, myocardial relaxation A serious and frequent psycho-organic disorder in
can be quantified by measuring the early diastolic critically ill patients is delirium. Critically ill
mitral annulus velocity (Ea). In combination with patients with a delirium have a seven times higher

Table 2. Cardiovascular effects of a spontaneous breathing trial

SvO2 PCWP PAP ABP CVP HR SpO2 PaO2 CO BNP Lactate


(%) (mmHg) (mmHg) (mmHg) (mmHg) (per min) (%) (mmHg) (l/min) (pg/ml) (mmol/l)

PSa 64 22 27/45 (35) 59/124 (79) 15 63 94 75 5.3 1358 1.0


5 min 62 23 27/40 (33) 67/158 (97) 11 68 92 61 6.4
60 min 65 25 25/42 (34) 70/163 (100) 10 70 94 70 6.3 1450 1.1

Succesfull spontaneous breathing trial in a COPD patient with a normal cardiavasular response. ABP, arterial blood pressure; BNP, B-type natriuretic peptide; CO,
cardiac output; COPD, chronic obstructive pulmonary disease; CVP, central venous pressure; HR, heart rate; PaO2, arterial oxygen partial pressure; PAP,
pulmonary artery pressure; PCWP, pulmonary capillary wedge pressure; SvO2, mixed venous oxygen saturation.
a
PS ¼ 5 cm H2O, PEEP ¼ 10 cm H2O.

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Intensive care and resuscitation

risk of prolonged mechanical ventilation [35]. THERAPEUTIC CONSEQUENCES


Moreover, it was found that delirium was associated Once a specific reason for weaning failure has been
with more respiratory and neurologic complications identified, the clinician should develop a strategy
and a reduced probability of successful extubation that increases the chances of successful weaning.
[36]. The Confusion Assessment Method for
the Intensive Care Unit is a validated tool to detect
delirium [37]. Apart from delirium, other psycho- Respiratory mechanics
logical factors may play a role in weaning failure. In patients with elevated airway resistance broncho-
It should be recognized that the inability to commu- dilators should be administered. Under certain
nicate physical and emotional needs, and venti- conditions (malpositioning, granulation tissue)
lator-dependence cause mental stress and the tracheostomy can enhance airway resistance
contribute to weaning failure [38]. Depressive dis- [47]. Specifically adapted tubes may be required.
orders are associated with weaning failure as well In patients with impaired respiratory compliance
[39]. Consultation of a psychiatrist is reasonable it is often obvious how mechanics can be improved,
when a psychological disorder is suspected. such as evacuation of pleural fluid or ascites,
diuretics to achieve negative fluid balance in case
of chest-wall or pulmonary edema [48].
Endocrine and metabolic disorders
The role of endocrine dysfunction in weaning fail-
ure has never been systematically evaluated, but is Respiratory muscle dysfunction
most likely of limited importance. Hypothyroidism Disuse is a prominent risk factor for the develop-
and adrenal insufficiency should be excluded in case ment of respiratory muscle weakness as pointed out
of clinical suspicion, as treatment options are avail- above. Therefore, it is reasonable to limit the
able. Malnutrition frequently occurs in critically ill duration of respiratory muscle inactivity, by using
patients and is associated with higher mortality [40], assisted modes for ventilation. Future studies should
but also with reduced muscle mass and as such determine the optimum time point for initiation of
contributes to difficult weaning, as discussed above. assisted ventilation and the level of unloading of the
inspiratory muscles.
Respiratory muscle strength training seems to
Iatrogenic factors be a reasonable intervention in weak patients. Most
The role of the clinician in weaning is crucial, in experience for respiratory muscle training has been
particular the assessment whether the patient still obtained in patients with COPD. For instance in a
requires ventilator support. In patients with randomized controlled trial (N ¼ 33; not on the
unplanned extubation, only 44% required reintu- ventilator) inspiratory muscle strength training
bation [41]. When unplanned extubation occurred improved respiratory muscle strength, 6-min walk-
during the weaning phase, only 30% required rein- ing distance and reduces dyspnea sensation, com-
tubation. Patients with successful unplanned extu- pared with sham training [49]. Very few studies have
bation during weaning phase spent less time on been performed in ventilated patients. The best
weaning the ventilator [41]. In a large clinical trial evidence up to now comes from Martin and
comparing weaning methods performed in a long- colleagues [50], demonstrating that inspiratory
term weaning facility [42], 32% of the patients muscle training in long-term ventilated patients
passed the initial screening weaning trial. This improves muscle strength and the chances of suc-
indicates that these patients were already weaned cessful weaning. Although many questions remain
upon arrival in this weaning facility, although this concerning optimal timing and protocol [51],
was unrecognized by the referring ICU team. These initiation of inspiratory muscle training appears
studies stress the importance to screen patients for reasonable in weak ventilated ICU patients diffi-
readiness for weaning and extubation. Appropriate cult-to-wean from the ventilator.
tests for weaning readiness have recently been In contrast to cardiac muscle dysfunction, no
reviewed elsewhere [43]. Under certain conditions drug is approved to optimize respiratory muscle
there may be a role for automated weaning [44]. function. However, some small pilot studies dem-
Asynchrony between the patient and ventilator onstrate that respiratory muscle contractility can be
is associated with increased duration of weaning enhanced pharmacologically [52]. Levosimendan is
[45] and even mortality [46]. Although it is reason- a relatively novel cardiac inotrope that improves
able to aim for optimal patient-ventilator inter- calcium sensitivity of the contractile proteins. In
action, no studies have been performed to study healthy study participants levosimendan improves
the effect on weaning outcome. contractile efficiency of the respiratory muscles [53].

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The differential diagnosis for failure to wean Doorduin et al.

A clinical trial in difficult-to-wean patients is architecture as assessed by polysomnography in


currently conducted (NCT01721434). Anabolic weaning patients [62]. In patients with confirmed
hormones that directly enhance contractile protein depressive disorder that affect weaning, treatment
synthesis are another potentially interesting with psychostimulants may be considered [63].
strategy to enhance respiratory muscle function.
In a randomized controlled trial, Schols et al. [54]
demonstrated that nandrolone together with Endocrine and metabolic disorders
high-caloric feeding enhances respiratory muscle The role of thyroid hormone replacement therapy in
strength in patients with COPD participating in difficult-to-wean patients has not been systemically
a rehabilitation program. The effect of anabolic evaluated. However, suppletion of thyroid hormone
steroids on peripheral or respiratory muscle strength in patients with proven hypothyroidism is reason-
in difficult-to-wean ICU patients has not been inves- able [64]. Huang and Lin [65] have demonstrated
tigated and the routine use is not recommended that in patients with confirmed adrenal insuffi-
today. ciency treatment with hydrocortisone fastens wean-
ing from the ventilator. No specific nutritional
therapy has been shown to improve weaning
Cardiac dysfunction outcome.
Routsi et al. [55] evaluated the effects of nitrogly-
cerin infusion on hemodynamics and weaning
outcome in difficult-to-wean patients with COPD CONCLUSION
and arterial hypertension. In these patients, nitro- The pathophysiology of weaning failure is complex
glycerin had beneficial hemodynamic effects during and requires a systematic differential diagnostic
a SBT, including reduction in pulmonary capillary approach to identify the primary cause for weaning
wedge pressure, right ventricular stroke work index, failure. Several tools and techniques are available to
and improved venous oxygen saturation. Moreover, discriminate between these causes. Identification of
whereas all patients [12] failed a weaning trial under the cause of weaning failure allows specific treat-
control conditions, 92% successfully completed the ment and thereby may fasten liberation from
SBT under nitroglycerin infusion. In patients with mechanical ventilation.
overt heart failure inotropes could be considered,
despite the absence of strong evidence. Levosimen- Acknowledgements
dan has been shown to improve cardiac output and
None.
reduce pulmonary capillary wedge pressure and
clinical outcome in patients with acute heart failure
[56,57]. The effects of levosimendan on weaning Financial support and sponsorship
outcome was evaluated in a small pilot study, None.
including 12 patients with systolic heart failure (left
ventricular ejection fraction 28  5%) [58]. After Conflicts of interest
levosimendan infusion seven of the 12 patients were L.H. has received travel grants and speakers fee from
weaned from mechanical ventilation within 51 h of Orion Pharma, Maquet Critical Care and Biomarin. L.H.
treatment. Although there is a strong rationale for has received an ongoing research grant from Orion
inotropes in patients with heart failure that are Pharma.
difficult-to-wean from the ventilator, clinical stud-
ies should confirm the favorable effect on outcome.
REFERENCES AND RECOMMENDED
READING
Papers of particular interest, published within the annual period of review, have
Cognitive dysfunction been highlighted as:
& of special interest
Reducing the level of sedation has been shown to && of outstanding interest

reduce duration of mechanical ventilation [59].


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