Assessments and exercises of cough strength in critically ill patients: a literature review

Introduction

Background

Airway clearance is crucial for maintaining airway patency in critically ill patients and depends on the mucociliary escalator, expiratory flow, and cough strength (1). In patients receiving noninvasive ventilation (NIV) or high-flow nasal cannula (HFNC) oxygen therapy to prevent intubation or reintubation, a weak cough is a significant risk factor for therapy failure (2,3). In intubated patients, a strong cough alone is not a reliable predictor of successful extubation, as they may be reintubated for other reasons. However, a weak cough and large amounts of secretion are important predictors of extubation failure and reintubation (4-8). A weak cough is also associated with an increased incidence of tracheostomy, prolonged mechanical ventilation duration, extended hospital stays, and increased mortality (9-11). Critically ill patients with diseases of the airways, nerves, and muscles often exhibit a weak cough, particularly those with high-risk factors such as advanced age, obesity, smoking, diabetes, pulmonary infections, and recent surgeries (12). Therefore, assessing and exercising cough strength are especially important for managing critically ill patients.

There are significant differences between voluntary and involuntary coughs. The voluntary cough consists of three phases: the inspiratory phase, controlled by the volume of inhaled air; the compressive phase, characterized by elevated intrapulmonary pressure; and the expulsive phase, during which the glottis suddenly opens and strong coughs are produced by rapid airflow through the airways (13,14). The involuntary or protective cough consists of four phases (irritation, inspiration, compression, and expulsion) and can be induced by inhaling irritants, such as capsaicin in healthy patients, or by administering 2 mL of saline into the airways of patients with artificial airways (4,15). The primary neurophysiological difference in the mechanics of voluntary and involuntary coughs is that the latter originates in the brainstem (16,17). Notably, the expiratory and accessory muscles are more active during voluntary cough (18-20). The voluntary cough is activated to indicate the patient’s strength in clearing the airways, while the involuntary cough reflects the capacity to protect the airways. This distinction is particularly important for patients at higher risk of silent aspiration and aspiration pneumonia (18,20,21).

Objective

This review aims to summarize current practices in assessing and exercising cough strength. We present this article in accordance with the Narrative Review reporting checklist (available at https://jtd.amegroups.com/article/view/10.21037/jtd-24-1673/rc).

Methods

Literature search

We conducted a systematic search of the PubMed, Embase, and ScienceDirect using specific keywords for publications up to December 31, 2023. The search strategy included the following keywords: (“cough assessment” OR “cough intensity” OR “cough ability” OR “cough capacity” OR “cough strength” OR “cough strength score”). The search strategy summary is in Table 1. A total of 281 related articles were identified, and we ultimately enrolled 26 of them. The characteristics of these studies are summarized in Table 2. Commonly used methods for assessing cough strength are summarized in Table 3. We also searched for cough exercises using the keywords: (“cough training” OR “cough exercise”). A total of 1,407 related articles were identified, and we ultimately enrolled 73 of them. The characteristics of these studies are summarized in Table 4. This search aimed to identify all studies related to the assessment and exercises of cough ability in critically ill patients.

Eligibility criteria

We included the following types of literature: randomized controlled trials, non-randomized trials, observational studies (case-control, cohort, and cross-sectional studies), proof-of-concept studies, research protocols, and case reports or series. Studies were eligible if they met these criteria: Subjects: Hospitalized adult patients. Language: Publications in English, including full-text articles or abstracts.

Data abstraction

Two independent evaluators reviewed all selected studies based on the inclusion criteria outlined above. In cases of discrepancies in data extraction or assessment, a single investigator was consulted to resolve the inconsistencies. The following information was extracted from each study: author(s), publication year, country, study type, sample size, patient characteristics (e.g., medical conditions), assessment method, conclusions/results and other relevant information.

Assessing cough strength

Cough peak flow (CPF) and peak expiratory flow (PEF)

CPF measures the maximum expiratory flow during a patient’s cough after a complete deep inspiration, with the glottis first closed and then opened. CPF is regarded as the gold standard for assessing cough strength and is significantly influenced by disease status and the overall physical condition of patients (24,47). A CPF <270 L/min indicates a weakened cough in healthy adults, while a CPF <160 L/min in patients with neuromuscular disorders and dysphagia is associated with a high risk of infectious pneumonia (44). Additionally, patients with a CPF <160 L/min immediately after extubation are at high risk of reintubation (48-50). PEF measures the maximum expiratory flow after a complete deep inspiration through an open glottis, and is therefore generally lower than CPF. In intubated patients, CPF and PEF are often used interchangeably in several studies (23-25,35,41). In fact, PEF is more suitable for assessing cough strength in intubated and tracheostomized patients because the artificial airway inhibits glottis closure, thus affecting the compressive phase of cough (48). Compared to other methods for assessing cough intensity, a PEF <60 L/min is the strongest predictor of extubation failure and is independently associated with in-hospital mortality in critically ill patients (4,22).

Plethysmography is the most accurate method for calculating CPF; however, it can be challenging to use with patients in the intensive care unit (ICU). A flowmeter is preferable for measuring CPF/PEF at the bedside, although accuracy can vary among different instruments (51). In non-intubated patients, CPF can be measured using a flowmeter and a mask. In intubated or tracheostomized patients, PEF can be directly measured using built-in flowmeters in the ventilator, based on the flow-time curve generated during pressure support ventilation [pressure support: 6–8 cmH₂O; positive end-expiratory pressure (PEEP): <5 cmH₂O] when patients exert maximum effort to cough. This method is more convenient for patients with artificial airways (30). PEF can also be measured using a separate flowmeter connected to the ventilator pipeline, and its accuracy is typically superior to that of built-in instruments (4). For patients who cannot cooperate, involuntary cough can be induced by administering 2 mL of saline into the airway and then connecting the flow spirometer as quickly as possible (15,27). Occasionally, 2 mL of saline may not be sufficient to induce involuntary cough in patients, and an additional injection of normal saline may be considered (52). The effectiveness of voluntary versus involuntary coughs in assessing PEF remains controversial. Some studies have found that PEF obtained during voluntary cough, rather than involuntary cough, is a better predictor of reintubation (27). However, Almeida et al. reported no significant difference in reintubation rates among the voluntary cough, saline stimulus, and suction tube stimulus groups (53). Common methods for measuring CPF/PEF are summarized in Figure 1.

Figure 1 Methods for measurement of CPF and PEF. (A) CPF of non-intubated patients; (B) PEF of intubated patients with separate flowmeter; (C) PEF of intubated patients with built-in flowmeter. CPF, cough peak flow; PEF, peak expiratory flow.

All factors that can influence any of the four phases of the cough reflex can theoretically also influence CPF/PEF(37). Moreover, forced vital capacity and maximum inspiratory pressure are both highly sensitive to decreased cough strength (54). However, unlike CPF/PEF, the following volume and pressure measurements—including forced vital capacity, forced expiratory volume in the first second, vital capacity, functional residual capacity, maximum inspiratory pressure, and maximum expiratory pressure—are not predictive of extubation failure (54,55).

Semiquantitative cough strength score (SCSS)

The SCSS, first proposed by Khamiees et al. in 2001, is an objective measurement of cough strength ranging from 0 to 5, as follows: 0= no cough on command, 1= audible movement of air without an audible cough, 2= weakly audible cough, 3= clearly audible cough, 4= strong cough, and 5= multiple sequential strong coughs. It can be used to assess cough strength in patients with or without an artificial airway (56,57). The SCSS is useful for bedside assessments and is highly repeatable among experienced respiratory therapists. When comparing SCSS with PEF, an SCSS score of 3 corresponds to a PEF of 60 L/min (28). The predictive power of the SCSS is slightly lower than that of PEF, although its specificity is higher (4,58,59). Notably, the SCSS, when combined with another relevant index of extubation outcomes, such as the Glasgow Coma Scale, can provide a more reliable predictive model (36). The SCSS can also be used to assess non-intubated patients and predict the failure of NIV (26).

White card test (WCT)

The WCT is used to assess cough strength in patients with artificial airways. The WCT requires the patient to cough 3–4 times toward a white card placed approximately 1–2 cm in front of the endotracheal cannula. If secretions are present or the card becomes wet, it is considered a positive result, providing an initial impression of the amount and characteristics of the secretions (39). The extubation failure rate associated with negative WCT results is three times greater than that associated with positive results (57). However, compared to PEF, a PEF <60 L/min is a superior predictor of extubation failure compared to a negative WCT result (39). Although relatively few studies have reported direct comparisons between the WCT and SCSS, the WCT is generally more accurate (4). Additionally, it is important to note that a positive WCT result may be influenced by the evaluator’s subjective judgment, particularly when the card is only slightly wet, which presents a disadvantage of the WCT.

Diaphragm ultrasound

Diaphragm ultrasound is a noninvasive and convenient imaging modality that is highly repeatable and can be easily performed in the ICU. It can be used to assess cough strength in patients with or without artificial airways (60). The passive excursion of the diaphragm refers to the distance it moves from its original position during end-expiration to end-inspiration (38,61). Passive diaphragm excursion during expiration in healthy adults has been shown to significantly correlate with CPF when coughing with maximum effort (42). Furthermore, diaphragm excursion is greater during involuntary cough than during voluntary cough (62). Diaphragm thickening fraction (DTF) refers to the change in diaphragm thickness when the patient breathes deeply with maximum effort and is calculated as follows: [(end-inspiration thickness) – (end-expiration thickness)]/(end-expiration thickness). DTF correlates with diaphragmatic activity and reflects the work of breathing of the diaphragm (63,64). However, no studies have investigated the association between DTF and cough strength. Based on current evidence, diaphragm ultrasound is inappropriate as a sole criterion for assessing cough strength, as the results are influenced by sex, age, height, position during the examination, and the technician’s experience (65).

Cuff pressure change (ΔP_cuff)

The difference between peak and baseline cuff pressure is defined as ΔP_cuff (40). Generally, a cuff pressure gauge (cuff manometer) is used to monitor changes in the pressure of laryngeal masks and intubation tubes before and after coughing. It can only assess cough strength in patients with artificial airways. ΔP_cuff is highly correlated with PEF, and the cutoff value for predicting extubation failure is reportedly 28 cmH₂O (40). However, changes in cuff pressure can be influenced by bronchial and lung compliance, the measurement method, and the diameter of the cannula.

Other methods

Cough sound power and energy are strongly correlated with physiological measures, such as esophageal pressure and CPF, as well as the subjective perception of cough strength (31,46). This method can be used to assess cough strength in patients without artificial airways. Umayahara et al. (32) established a model to accurately calculate CPF based on cough sounds collected using a microphone positioned less than 30 cm from the patient’s mouth (33). This method could be particularly useful for non-intubated patients using speaking valves. Maximum phonation time is also a surrogate marker for respiratory function and airway clearance indices (45). However, more evidence is needed for its application in the ICU.

Sonoscore is the average decibel level of three consecutive coughs performed with maximum effort. Currently, there is only one related study that involved patients receiving invasive mechanical ventilation (43). The results indicated that a Sonoscore <67.1 dB was able to predict extubation failure.

Electromyography (EMG) is a useful modality for evaluating respiratory muscle activity and can be used to assess cough strength in patients with or without artificial airways. During voluntary coughing, EMG signals increase for the rectus, oblique, transverse abdominal, internal intercostal, and external anal sphincter muscles (66,67). EMG activity of the abdominal wall is related to cough flow, expired volume, and cough sound amplitude (137). However, EMG is a valuable diagnostic tool for patients with good motor function but reduced cough strength (66). It can effectively assess cough threshold and power in both healthy adults and individuals with spinal cord injuries (66,138). Compared to concentric needle electrodes, surface electrodes are better suited for obtaining accurate measurements of whole-muscle EMG activity (67).

Esophageal pressure varies with intrathoracic pressure; therefore, cough intensity is highly correlated with changes in esophageal pressure. Contraction of the abdominal muscles generates positive gastric pressure during coughing. Changes in internal gastric pressure, central venous pressure, bladder pressure, and rectal pressure are similar to those in esophageal pressure and also reflect cough strength, although small discrepancies exist among these parameters (34). These pressure-related indices can be used to assess cough strength in patients with or without artificial airways. Monitoring changes in pressure requires invasive catheterization, and the pressure sensor only functions correctly when the catheter is properly positioned.

Clearance and expectoration of mucus, including mucociliary transport, sputum weight (dry and wet), and sputum volume, are commonly used as primary or secondary outcomes in studies assessing the effectiveness of cough exercise tools (139). These measures also serve as supplementary indicators of cough ability. Current research shows that improved cough ability is often linked to increased sputum production (all P<0.05) (140). Measuring sputum volume at a single time point has inherent limitations and may not fully capture the patient overall cough capacity. To address this, dynamic observation over a specific time frame may be needed to assess sputum output as a measure of cough capacity. Additionally, due to individual variability, improvements in cough ability should be evaluated by comparing each patient’s performance before and after the intervention.

Most available data on assessing cough strength focus on healthy individuals or well-defined groups, such as the elderly, intubated patients, and those with neuromuscular disorders. However, clinical data remain limited for patients with glottic insufficiency or dysphagia after extubation.

Cough exercises

Given the consequences of weak cough, timely and early training in cough and expectoration is essential for patients at high risk of cough decline, as well as for those who already have reduced cough strength. Increased cough strength can enhance lung function and improve outcomes (29,141-143) (Table 4). Although various methods exist for cough training in critically ill patients, all are based on three fundamental principles: increasing inhaled volume, increasing expiratory flow, and oscillation (144). Commonly used methods for cough exercises are summarized in Table 5.

Increase inhaled volume

Inhaled volume is the most important indicator of respiratory health in adult patients with either a single or continuous cough (86,90,145). Furthermore, maximum inspiratory pressure is more significantly associated with cough strength than maximum expiratory pressure for both voluntary and involuntary coughs. Therefore, increasing inspiratory muscle strength and inspiratory volume is essential for enhancing cough strength (70). Intermittent positive pressure breathing (91), NIV (80), and continuous positive airway pressure (85,122) can all passively increase inhaled volume and are effective. Some home ventilators can achieve these effects effectively (70). Voluntary exercise tools, such as the incentive spirometer (IS), have been shown to significantly increase maximum inspiratory capacity in both hospitalized and discharged patients (104,146-148). Notably, the effectiveness of the IS largely depends on the patient’s effort, and the addition of a reminder bell can lead to significant improvements (49,82,149). Additionally, it is important to avoid the adverse consequences of excessive use (150). Early mobilization, inspiratory muscle strength training, and certain forms of electrical muscle stimulation (94,136) can also improve inhaled volume in critically ill patients, as well as in those with neuromuscular diseases and postoperative patients (79,81,84,151). The inhaled volume of patients receiving mechanical ventilation can be increased by augmenting the conveying volume through the volumetric cough mode of the ventilator, thereby gradually raising the inhaled volume to provide a convenient target for the patient (49).

Increase expiratory flow

Exercising the expiratory muscles can effectively increase expiratory flow and improve cough capacity, particularly in patients with neuromuscular diseases (92,96,99-103,105,106,108,115,116,123,124). Setting resistance during the expiratory phase through positive expiratory pressure therapy can achieve a similar effect to PEEP for training the expiratory muscles (87,117,119,144). Different devices have specific requirements for patients during use; for example, the patient must be in either an upright or sitting position when using a flutter device (68,83,109). Some cough training methods, such as forced expiratory technology, active cycle of breathing techniques (134), autogenic drainage (69), and mechanical insufflation-exsufflation (72,73,78,111,120,129), can enhance both inspiratory volume and expiratory flow, thereby increasing expectoration and facilitating the expulsion of sputum (152,153). Despite insufficient evidence, mechanical insufflation-exsufflation is commonly used in patients with neuromuscular diseases to aid expectoration (154). Expiratory muscle training can also enhance muscle strength and cough capacity (125,126,131-133,155), and it seems to be more effective for improving CPF compared to inspiratory muscle training (113). In addition to mechanical aids, manual aids can also facilitate increased expiratory airflow, including expiratory rib cage compression (98), manual chest compression (114), expiratory flow acceleration (118) and abdominal wall compression, among others (71,76,77,88,89,127,128,135).

Oscillation

Oscillations in the airway or external to the chest wall can effectively transmit to the airway to facilitate sputum release (156). High-frequency oscillation can effectively increase tidal volume and inspiration duration, reduce respiratory rate, and result in deeper and slower breaths (95,97,110,121,130,157). Consequently, mean PEF will be greater (74). Commonly used techniques in the ICU include clapping and vibration, oscillating positive expiratory pressure (OPEP) (112), high-frequency chest wall oscillation (75), and intrapulmonary percussion ventilation (IPV) (158-162). Aside from IPV, there is no significant difference in the use of these devices; however, IPV is more effective and beneficial for airway clearance (160,163). The MetaNeb^® System (Hill-Rom Holdings, Inc., Chicago, IL, USA) was recently introduced for the mobilization of secretions, lung expansion therapy, and the treatment and prevention of pulmonary atelectasis (164).

All of the above-mentioned means and methods of improving cough ability are not strictly contraindicated. All airway clearance techniques have a good safety profile when the patient is generally stable (139). For patients who can cooperate and have good compliance, they can take tools or methods with high autonomy to exercise, such as IS, OPEP, etc. If the patient is difficult to cooperate or has poor compliance, it would be more suitable for these patients to receive passive expectoration methods, such as IPV, MI-E, airway suction, etc. (93).

Currently, cough exercises are widely used in clinical practice; however, optimal effects are often not achieved because most of these techniques maintain rather than improve patient status (107,165). Cough exercises should be encouraged for critically ill patients; however, many do not tolerate prolonged training, necessitating the presence of a respiratory therapist or physical therapist. Furthermore, there is a lack of high-quality evidence regarding the appropriate power, frequency, and duration for cough exercises in critically ill patients (144,166). Therefore, further research is warranted to develop individualized training methods and parameters, as well as to enhance patients' tolerance and cooperation.

Conclusions

Weak cough in critically ill patients is linked to an increased risk of extubation failure, prolonged mechanical ventilation, longer ICU and hospital stays, and higher mortality. Therefore, it is crucial to select appropriate methods for assessing and exercising cough strength in ICU patients. CPF/PEF, SCSS, and WCT are relatively simple and widely used methods. The key elements of cough exercises typically include increasing inhaled volume, enhancing expiratory flow, and incorporating oscillation. Developing personalized programs and effective action plans is essential for cough exercises which largely depends on patient cooperation and persistence.

Acknowledgments

None.

Footnote

Reporting Checklist: The authors have completed the Narrative Review reporting checklist. Available at https://jtd.amegroups.com/article/view/10.21037/jtd-24-1673/rc

Peer Review File: Available at https://jtd.amegroups.com/article/view/10.21037/jtd-24-1673/prf

Funding: This study was financially supported by grants from the Foundation for Young Researchers of Zhongshan Hospital (grant No. 2021ZSQN22).

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://jtd.amegroups.com/article/view/10.21037/jtd-24-1673/coif). The authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.

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