Voluntary and reflex cough and the expiration reflex; implications for aspiration after stroke
Introduction
Aspiration, possibly followed by lung infections including pneumonia, is a serious risk after central nervous disorders such as stroke [1], [2]. Tests to determine the risk of aspiration are therefore important to prevent, by appropriate care and treatment, its occurrence. These tests assess the normality or otherwise of the various physiological mechanisms that prevent aspiration.
The site of aspiration into the lungs is the larynx. There are two main types of laryngeal mechanism that prevent aspiration: those that close the glottis and those that expel material that might be inhaled into the lungs. Both are usually present and synchronized. The glottal closure reflex, in response to mechanical stimulation of the vocal fold region, can occur in isolation without involvement of the respiratory muscles [3], but usually is accompanied by the laryngeal expiration reflex (LER) [4], [5]. ‘True cough’, either voluntary (VC) or reflex (RC), starts with an inspiration that might draw material into the lungs (aspiration) before expelling it [4], [5], [6].
Different studies use different end-points: (A) aspiration/risk of aspiration, also assessed by methods such as barium (or other material) swallow or videofluoroscopy; or (B) chest infections/pneumonia or their risk, assessed clinically. There have been many studies on the use of cough in assessing the risk of aspiration in patients with dysphagia, not necessarily due to stroke, and some of these will be quoted here. When the end result is pneumonia, its occurrence will depend on prior treatment of the patient, which in turn depends on provisional assessment of its risk. These relationships are complex.
This review will deal only with the protective and defensive reflexes under the general heading ‘cough’. However it cannot deal in detail with all the vast literature on cough, stroke and the risk of aspiration The use of methods to test the LER will be emphasized, because of all the cough tests it is theoretically the most ‘anti-aspiration’; it is also the most neglected, although simple to test. We have developed and are using such a method to test the LER in stroke patients [7]. In this review we compare the use of LER with other cough tests. More sophisticated methods involving intubation (e.g. videofluoroscopic swallowing examination; fibreoptic endoscopic examination of swallowing; fibreoptic endoscopic evaluation of swallowing with sensory testing) may include cough induced by mechanical stimulation of the laryngeal mucosa. These important methods will not be reviewed here, where the primary concern is with cough mechanisms, although some of them have been claimed as ‘gold standard’ for the assessment of risk of aspiration. (‘Only alchemists believe in gold standards’; anon).
A problem with assessing the information on cough and aspiration in patients after stroke is that most studies involve subjective identification or estimation of the ‘strength‘ of the cough. They usually lack measurements of the cough itself. Cough is portrayed as present or absent, or subjectively graded usually on a three point scale (present, weak, absent). However objective analyses of cough (by airflow, gastric pressure, expiratory muscle EMGs, chest wall acceleration and sound generation) are available and not only allow identification of the different types and patterns of cough [8], [9], [10], [11], [12], [13], but also provide valuable information of the way neurological disease may disco-ordinate the neural mechanisms of cough (see later). Fig. 1 illustrates some parameters that can be derived from airflow and gastric pressures in voluntary cough [10].
Thus cough is a highly complex process, and few would agree that all we need to measure is a recording of cough sounds, or to listen to them [14]. However cough sound intensity has been shown to correlate with some other parameters of cough [9].
Section snippets
Types of cough, including after stroke
Three different types of cough are described in the textbooks: voluntary and reflex cough (VC and RC), and the expiration reflex (ER). (Speaking semantically the ER is not a cough because it does not start with an inspiration, but it is convenient to include it as a ‘cough’). There are probably further subdivisions. There are at least five different types of vagal afferent sensors which can cause cough [15], [16], and they and their interactions would be expected to produce different patterns
Comparisons between methods
It is not practical, for reasons of space, to summarize all the many results of comparing any two different methods for assessing ‘cough’ after stroke. No-one seems to have compared three (or four) methods in the same patients. Often the results include sensitivity, selectivity and specificity values for the two methods chosen, but space does not allow these important values to be detailed here. The general impression is that any of the methods is valuable in pointing to the risk of aspiration,
Discussion
We have described and briefly assessed four methods using cough for the assessment of the risk of aspiration and pneumonia after stroke. Each has its advocates who provide evidence to support their views (although none claims a method to be a gold standard!). The choice of test may depend on other features: the condition of the patient, the practicality of use in different clinical environments, and the availability and desirability of invasive techniques to assess risk. Most authors agree, and
Statement of interest
JGW, RAS and RES have shared interests in Pneumoflex Systems LLC, that produces a device to stimulate the LER.
Acknowledgments
We are grateful to Drs. C. Smith Hammond and K.Ward for allowing us to use Figs. and results from their papers, and for helpful discussions.
References (42)
- et al.
Cough and glottic-stop reflex sensitivity in health and disease
Thorax
(2005) - et al.
Predicting aspiration in patients with ischemic stroke. Comparison of clinical signs and aerodynamic measures of voluntary cough
Chest
(2009) - et al.
Capsaicin exposure elicits complex airway defensive motor patterns in normal humans in a concentration-dependent manner
Pulm Pharmacol Therap
(2007) - et al.
Vagal afferent nerves regulating the cough reflex
Respir Physiol Neurobiol
(2006) - et al.
Cough induced by high-frequency chest percussion in healthy volunteers and patients with common cold
Respir Med
(2004) - et al.
Cough and aspiration
Chest
(2009) - et al.
Cough and aspiration of food and liquids due to oral-pharyngeal dysphagia. ACCP evidence-based clinical practice guidelines
Chest
(2006) Cough and aspiration of food and liquids due to oral pharyngeal dysphagia
Lung
(2008)- et al.
Cough: what’s in a name?
Eur Respir J
(2006) Before we get started; What is a cough?
Lung
(2008)
Voluntary and reflex cough: Similarities and differences
Pulm Pharamcol Ther
Assessing the laryngeal cough reflex and the risk of developing pneumonia after stroke
Arch Phys Med Rehabil
Assessment of aspiration risk in stroke patients with quantification of voluntary cough
Neurology
Acute ischaemic hemispheric stroke is associated with impairment of reflex in addition to voluntary cough
Eur Respir J
Defective motor control in coughing in Parkinson’s disease
Am J Respir Crit Care Med
Cough and other respiratory reflexes
Rebuttal: cough is an expiratory sound
Lung
Encoding of the cough reflex
Pulm Pharmacol Therap
Respiratory reflexes from the trachea and bronchi of the cat
J Physiol
Urge-to-cough: what can it teach us about cough?
Lung
Clinical cough I: the urge-to-cough: a respiratory sensation
Handb Exp Pharmacol
Cited by (37)
Myosteatosis predicting risk of transition to severe COVID-19 infection
2022, Clinical NutritionCitation Excerpt :We speculate that myosteatosis with weakening thoracic muscle in our cohort may have resulted in a diminished effort for coughing, which may partly be responsible for disease progression. Coughing is the most direct protective mechanism against lung infections, requiring coordinated activation and movement of respiratory muscles and internal laryngeal muscles [22,37]. A prior study of healthy older men and women has showed that reduced muscle strength was significantly associated with decreased lung function, implying the inter-dependence between muscle strength and vital capacity lung function [38].
Respiratory Muscle Training Reduces Respiratory Complications and Improves Swallowing Function After Stroke: A Systematic Review and Meta-Analysis
2022, Archives of Physical Medicine and RehabilitationCitation Excerpt :Lastly, afferent stimulation of the sensory receptors of the tongue and oropharynx provided by respiratory muscle training may increase the activity of the swallowing center in the medulla oblongata of the brainstem.50,51 Based on a previous study,52 voluntary coughs have been closely related to aspiration in terms of airway protection mechanism during swallowing. It was found that the intensity of coughing correlated with the risk of airway aspiration.
Low thoracic muscle radiation attenuation is associated with postoperative pneumonia following partial hepatectomy for colorectal metastasis
2020, HPBCitation Excerpt :The pathophysiological mechanism which may underlie the association between myosteatosis in the thoracic compartment and pneumonia is not clear. It is known that coughing is the most immediate protective mechanism from aspiration, requiring the coordinated activation of inspiratory, expiratory, and intrinsic laryngeal muscles.41,42 Sillanpaa et al. investigated interdependency between muscle strength and spirometric pulmonary functions in healthy older men and women and observed that reduced muscle strength was associated with reduced pulmonary function.43
The assessment of the peak of reflex cough in subjects with acquired brain injury and tracheostomy and healthy controls
2020, Respiratory Physiology and NeurobiologyDetermining Peak Cough Flow Cutoff Values to Predict Aspiration Pneumonia Among Patients With Dysphagia Using the Citric Acid Reflexive Cough Test
2018, Archives of Physical Medicine and RehabilitationMeasuring voluntary and reflexive cough strength in healthy individuals
2017, Respiratory MedicineCitation Excerpt :Dysphagic patients frequently have dystussia (disordered cough response) which has been shown to be associated with increased risk of aspiration pneumonia [11–14]. Voluntary cough and reflexive cough are physiologically different [1,15,16] and, as such, are affected differently in neurological disorders [17–19]. Cough reflex testing (CRT) in neurologically-impaired patients, particularly those who have had a stroke, has been shown to be effective in identifying individuals with impaired cough sensitivity who are at risk of silent aspiration (aspiration without cough) and development of pneumonia [12].