Competition between gas exchange and speech production in ventilated subjects

https://doi.org/10.1016/S0301-0511(98)00024-6Get rights and content

Abstract

Competition between airflow requirements for speaking and gas exchange occurs in ventilator-dependent tracheotomized subjects who can `steal' air from alveolar ventilation during the ventilator's inflation phase to produce sound. We wondered whether these subjects adopted strategies to minimize hypoventilation when speaking, particularly when ventilatory drive and respiratory discomfort are increased by hypercapnia. We recorded speech and ventilatory and speaking volumes in five ventilated subjects during reading and extemporaneous speech. All subjects spoke during the ventilator's inflation (and expiratory) phase, losing approximately 15% of their inspired tidal volume. During induced hypercapnia (15 mmHg increase in PetCO2) which caused shortness of breath, all subjects could still speak adequately. Two subjects `adapted' to hypercapnia by reducing the air used for speaking during inflation. In contrast, one subject reacted, as normal subjects do, by increasing the airflow per syllable (a mal-adaptive strategy in ventilated subjects). These changes were modest despite the strong hypercapnic stimulus.

Introduction

The ventilatory requirements for gas exchange must compete for the use of the breathing apparatus during many behaviors including coughing, changing posture, crying, defecation, hiccuping, laughing, playing wind instruments, singing, sneezing, speaking, sniffing, swallowing, swimming, vomiting, and whistling. To meet these requirements, there are several anatomical sources of motor command of the respiratory muscles, including the brainstem, the limbic system, and the motor cortex (reviewed by Shea (1996)). The situations when particular motor `centers' prevail are probably best illustrated by non-REM sleep for the brainstem respiratory motor complex (e.g. Harper, 1991), by emotions for the limbic system (e.g. laughing, Munschauser et al., 1991), and by volitional breathing maneuvers for the motor cortex (e.g. Ramsay et al., 1993). However, in most circumstances we cannot be certain of the extent of the contribution of each motor command source to the final respiratory motoneuron activity. Functionally, the fact that the automatic respiratory control system (probably brainstem) can be fettered by the behavioral control system (probably forebrain) is best demonstrated by the ease of voluntarily holding one's breath. Conversely, the limit of the breath hold itself is a dramatic example of when the automatic respiratory control system overcomes the behavioral control system.

One of the best ways to study the competition between automatic and behavioral respiratory control is to study speech. Normal subjects speak during expiration-utilizing air that already has been used for gas exchange. Since the mean airflow required for speech is often greater than resting ventilation, normal subjects usually hyperventilate when speaking at rest (e.g. Bunn and Mead, 1971, Phillipson et al., 1978). In contrast to normal subjects, the airflow required for speech competes with the flow required for gas exchange in subjects who are maintained on positive pressure ventilators with an unsealed tracheotomy tube (fenestrated, or cuffless). These subjects can `steal' air from alveolar ventilation during the ventilator's inflation phase to produce sound by diverting air around the tracheotomy tube and up through the larynx. Speech can occur whenever the translaryngeal pressure is sufficient to vibrate the vocal folds—≈2 cmH2O. Any speech during the ventilator's inflation phase will result in relative hypoventilation.

We have used this novel situation of antagonism between speaking and breathing that occurs in ventilator-dependent subjects to gain insight into the interaction between the behavioral and the reflex control of breathing in humans. We performed this study at the subjects' baseline eucapnic level, and during experimentally induced hypercapnia to increase the reflex ventilatory drive. During both states, we determined how much these subjects hypoventilate during speech, and whether they adopt strategies to minimize this hypoventilation. Such strategies could include reducing the amount of speech (delayed onset of speech; decreased syllables/s), or the amount of air used for speech (decreased volume/syllable) during the inflation phase of the ventilator cycle. Another possible adaptation would be to activate accessory inspiratory muscles that have been spared by the injury or disease, such as sternocleidomastoid muscles—if this activation occurred during the expiratory pause of ventilator cycle this could provide an `extra' inspiration. We reasoned that the need for the subjects to use adaptive speech strategies to conserve air is greater if the ventilatory drive and breathlessness are increased. We also acknowledged the possibility that ventilated subjects might react, as normal subjects do when respiratory drive is increased, by increasing the flow per syllable (e.g. Bunn and Mead, 1971, Doust and Patrick, 1981)—even though this could prove mal-adaptive in ventilated subjects by causing relatively greater hypoventilation.

Section snippets

Subjects

We studied three men and two women who had normal hearing, intelligible speech, normal language, normal cognition, and who had depended on positive-pressure ventilatory support for 3 years or longer due to spinal cord lesions or muscular dystrophy. Individual subject information is provided in Table 1 wherein the identity numbers correspond to those used in our previous studies of these subjects (Banzett et al., 1987, Banzett et al., 1989, Hoit et al., 1994). As commonly observed in

Sensations

Following speaking while eucapnic, no unusual sensations were noted by the subjects, except subject #8 who found it tiring. In contrast, following speaking while hypercapnic, three of the five subjects spontaneously described feelings of being `short of breath' or `out of breath'. Of the other two subjects, #8 spontaneously described speaking during the hypercapnic condition as `exhausting', and when specifically asked he said that he had `less than' the right amount of air. Subject #10 also

Summary

The competition between the airflow requirements for speaking and for gas exchange was studied in ventilator-dependent tracheotomized subjects who `steal' air from ventilation during the ventilator's inflation phase to produce sound. These subjects modestly hypoventilated when speaking. While there were no systematic changes among this small group of subjects, some did adopt strategies to minimize the hypoventilation during speaking when we increased ventilatory drive. This was particularly

Acknowledgements

This work was supported by grants from the National Institute of Health (HL-46690) and the National Institute on Deafness and Other Communication Disorders (DC-00030, DC-01409). We gratefully acknowledge the contributions of Robert Brown, MD, and we extend special thanks to the subjects who participated in this study.

References (23)

  • J.H. Doust et al.

    The limitation of exercise ventilation during speech

    Respir. Physiol.

    (1981)
  • R. Banzett et al.

    High-level quadriplegics perceive lung volume change

    J. Appl. Physiol.

    (1987)
  • R.B. Banzett et al.

    `Air hunger' arising from increased pCO2 in mechanically ventilated quadriplegics

    Respir. Physiol.

    (1989)
  • E. Bloch-Salisbury et al.

    Air hunger induced by acute hypercapnia adapts to chronic hypercapnia in ventilated humans

    J. Appl. Physiol.

    (1996)
  • J.C. Bunn et al.

    Control of ventilation during speech

    J. Appl. Physiol.

    (1971)
  • M. Draper et al.

    Expiratory pressures and air flow during speech

    Br. Med. J.

    (1960)
  • M. Durand et al.

    Effect of feeding on the chemical control of breathing in the newborn infant

    Pediatr. Res.

    (1981)
  • Harper, R.M., 1991. State-dependent elctrophysiological changes in central nervous system activity. In: Haddad, G.G.,...
  • J.D. Hoit et al.

    Age and speech breathing

    J. Speech Hear. Res.

    (1987)
  • J.D. Hoit et al.

    Speech breathing in women

    J. Speech Hear. Res.

    (1989)
  • J.D. Hoit et al.

    Speech production during mechanical ventilation in tracheostomized individuals

    J. Speech Hear. Res.

    (1994)
  • Cited by (0)

    View full text