Airway protection and coordination of breathing and swallowing : in health and anesthesia

Swallowing and breathing is coordinated to ensure that the airway is protected from aspiration. During the pharyngeal phase of swallowing, breathing is interrupted to allow safe passage of bolus. However, details on the complex coordination of breathing and swallowing and their precise temporal relationship are not fully understood. Respiratory complications are common in the postoperative period and drugs used in anesthesia impair pharyngeal function and airway protection in young adults. The aims of this thesis were first to characterize key mechanisms for airway protection, i.e. pharyngeal function and coordination of breathing and swallowing and secondly to describe the impact of age and drugs used in anesthesia.

A newly developed airflow discriminator was validated by comparisons with spirometry, diaphragmal and abdominal EMG and integrated with pharyngeal manometry and videoradiography into a multimodal platform recording swallowing and breathing simultaneously with high temporal resolution. Normal coordination of breathing and swallowing was studied in young volunteers, while swallowing different bolus types, changing body position and during hypercapnia. Moreover, effects of morphine and midazolam were studied at two occasions during spontaneous decay of drug concentration. Effects of partial neuromuscular block were examined during rocuronium infusion in elderly volunteers (>65 years) at steady state adductor pollicis train-of-four ratios of 0.70, 0.80 and >0.90.

The airflow discriminator proved highly reliable and provided detailed information on timing of respiratory airflow unambiguously in relation to pharyngeal and diaphragmatic activity. The diaphragm was activated in the apneic period during swallowing, presumably a mechanism for preserving respiratory volume and to promote expiratory airflow after swallowing. This finding has to our knowledge not been described in humans before. Coordination between breathing and swallowing remained mostly unchanged regardless of age, body position, bolus characteristics, respiratory drive or partial neuromuscular block. In contrast, morphine and midazolam dys-coordinated breathing and swallowing, increasing the incidence of inspiration immediately after swallowing. Moreover, clinically relevant doses of morphine and midazolam caused pharyngeal dysfunction and impaired airway protection in young adults. Partial neuromuscular block profoundly aggravated age-dependent pharyngeal dysfunction by predominantly impairing mechanical properties of the pharynx.

In conclusion, swallowing occurs during expiration in young and elderly individuals and drugs used in anesthesia cause pharyngeal dysfunction and dys-coordination of breathing and swallowing, ultimately compromising the protection of the airway against aspiration.

List of scientific papers

I. Hårdemark Cedborg AI, Sundman E, Bodén K, Kuylenstierna R, Ekberg O, Witt Hedström H, Eriksson LI. Coordination of spontaneous swallowing with respiratory airflow and diaphragmatic and abdominal muscle activity in healthy adults. Experimental Physiology. 2009, Apr; 94 (4): 459-68.
https://doi.org/10.1113/expphysiol.2008.045724

II. Hårdemark Cedborg AI, Bodén K, Witt Hedström H, Kuylenstierna R, Ekberg O, Eriksson LI. Sundman E. Breathing and swallowing in normal man--effects of changes in body position, bolus types, and respiratory drive. Neurogastroenterology and Motility. 2010, Nov; 22 (11): 1201-8.
https://doi.org/10.1111/j.1365-2982.2010.01551.x

III. Hårdemark Cedborg AI, Sundman E, Bodén K, Witt Hedström H, Kuylenstierna R, Ekberg O, Eriksson LI. Effects of morphine and midazolam on pharyngeal function, airway protection and coordination of breathing and swallowing in healthy adults. [Manuscript]

IV. Hårdemark Cedborg AI, Sundman E, Bodén K, Kuylenstierna R, Ekberg O, Witt Hedström H, Eriksson LI. Pharyngeal function and breathing pattern during partial neuromuscular block in the elderly. Effects on airway protection. Anesthesiology. 2013. [Accepted]
https://doi.org/10.1097/ALN.0000000000000043