Reduced tidal volume increases ‘air hunger’ at fixed PCO2 in ventilated quadriplegics

doi:10.1016/0034-5687(92)90131-F

Respiration Physiology

Volume 90, Issue 1, October 1992, Pages 19-30

Respiration Physiolo...

https://doi.org/10.1016/0034-5687(92)90131-F Get rights and content

Abstract

The act of breathing diminishes the discomfort associated with hypercapnia and breath-holding. To investigate the mechanisms involved in this effect, we studied the effect of tidal volume (V_T) on CO₂-evoked air hunger in 5 high-level quadriplegic subjects whose ventilatory capacity was negligible, and who lacked sensory information from the chest wall. Subjects were ventilated at constant frequency with a hyperoxic gas mixture, and end-tidal P_CO₂ was maintained at a constant but elevated level. V_T was varied between the subjects' normal V_T and a smaller V_T. Subjects used a category scale to rate their respiratory discomfort or ‘air hunger’ at 30–40 sec intervals. In 4 of 5 subjects there was a strong inverse relationship between breath size and air hunger ratings. The quality of the sensation associated with reduced V_T was nearly identical to that previously experienced with CO₂ alone. We conclude that afferent information from the lungs and upper airways is sufficient to modify the sensation of air hunger.

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Evidence only proves low surpasses high tidal volume (V_T) for acute respiratory distress syndrome (ARDS). Intermediate V_T is a common setting for ARDS patients and has been demonstrated as effective as low V_T in non-ARDS patients. The effectiveness of intermediate V_T in ARDS has not been studied and is the objective of this study.
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Totally 382 patients, with 6958 ventilator settings eligible for lung protection, were classified into low (mean V_T = 6.7 ml/kg), intermediate (mean V_T = 8.9 ml/kg) and high (mean V_T = 11.2 ml/kg) V_T groups. With similar baseline ARDS and ICU severities, intermediate and low V_T groups did not differ in 28-D mortality (47% vs. 63%, P = 0.06) or other outcomes such as 90-D mortality, ventilator-free days, ventilator-dependence rate. Multivariate analysis revealed high V_T was independently associated with 28-D and 90-D mortality, but intermediate V_T was not significantly associated with 28-D mortality (HR 1.34, CI 0.92–1.97, P = 0.13) or 90-D mortality. When the intermediate and low V_T groups were matched in propensity scores (n = 66 for each group), their outcomes were also not significantly different.
Intermediate V_T, with its outcomes similar to small V_T, is an acceptable option for ventilated ARDS patients. This conclusion needs verification through clinical trials.
La evidencia solo demuestra que el volumen tidal (V_T) bajo supera al alto para el síndrome de dificultad respiratoria aguda (ARDS). La V_T intermedia es un escenario común para los pacientes con ARDS y se ha demostrado que es tan eficaz como la V_T baja en pacientes sin ARDS. No se ha estudiado la eficacia de la V_T intermedia en el ARDS y es el objetivo de este estudio.
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Mortalidad 28-D.
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La V_T intermedia, con resultados similares a la V_T pequeña, es una opción aceptable para pacientes con ARDS ventilados. Esta conclusión necesita verificación a través de ensayos clínicos.
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Citation Excerpt :
However, non-invasive human electrophysiological recordings were unable to give inferences to deep structures such as the hippocampus or thalamus due to limitation in spatial resolution. Neuroimaging research in dyspnea to-date has mostly studied brain substrates using chemoreceptor or mechanoreceptor stimuli (Banzett et al., 2000; Manning et al., 1992; Moosavi et al., 2003; Peiffer, Costes, Herve, & Garcia-Larrea, 2008; Peiffer, Poline, Thivard, Aubier, & Samson, 2001; von Leupoldt et al., 2008, 2009). These studies found that aversive stimuli, including resistive loads, hypercapnia, and hypoxia, induce significant neural activation in the thalamus, sensorimotor cortex and limbic structures in healthy participants.
The involvement of neural substrates in respiratory sensory gating remained unclear. This study aimed to investigate cortical and subcortical activations associated with respiratory sensory gating by using functional magnetic resonance imaging. First, we hypothesized that paired occlusions would induce neural activation in cortical and subcortical areas, including the thalamus and sensorimotor cortices. Secondly, we hypothesized that, in terms of parameter estimates in the general linear model, the activation effect size β ratios (β_paired/β_single) would be less than 2 due to central neural gating mechanism. Forty-six healthy participants were included in the study. Our analyses showed that the βpaired/βsingle ratios for the supramarginal gyrus, basal ganglia, thalamus, and middle frontal gyrus were less than 2. In conclusion, our results demonstrated a non-linear relationship regarding brain neural activations in response to paired versus single occlusions, suggesting that respiratory sensory information is gated at the subcortical and cortical levels.
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In health, the near-eucapnic, highly efficient hyperpnea during mild-to-moderate intensity exercise is driven by three obligatory contributions, namely, feedforward central command from supra-medullary locomotor centers, feedback from limb muscle afferents, and respiratory CO₂ exchange (V̇CO₂). Inhibiting each of these stimuli during exercise elicits a reduction in hyperpnea even in the continuing presence of the other major stimuli. However, the relative contribution of each stimulus to the hyperpnea remains unknown as does the means by which V̇CO2 is sensed. Mediation of the hyperventilatory response to exercise in health is attributed to the multiple feedback and feedforward stimuli resulting from muscle fatigue. In patients with COPD, diaphragm EMG amplitude and its relation to ventilatory output are used to decipher mechanisms underlying the patients’ abnormal ventilatory responses, dynamic lung hyperinflation and dyspnea during exercise. Key contributions to these exercise-limiting responses across the spectrum of COPD severity include high dead space ventilation, an excessive neural drive to breathe and highly fatigable limb muscles, together with mechanical constraints on ventilation. Major controversies concerning control of exercise hyperpnea are discussed along with the need for innovative research to uncover the link of metabolism to breathing in health and disease.
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The clinical term dyspnea (a.k.a. breathlessness or shortness of breath) encompasses at least three qualitatively distinct sensations that warn of threats to breathing: air hunger, effort to breathe, and chest tightness. Air hunger is a primal homeostatic warning signal of insufficient alveolar ventilation that can produce fear and anxiety and severely impacts the lives of patients with cardiopulmonary, neuromuscular, psychological, and end-stage disease. The sense of effort to breathe informs of increased respiratory muscle activity and warns of potential impediments to breathing. Most frequently associated with bronchoconstriction, chest tightness may warn of airway inflammation and constriction through activation of airway sensory nerves. This chapter reviews human and functional brain imaging studies with comparison to pertinent neurorespiratory studies in animals to propose the interoceptive networks underlying each sensation. The neural origins of their distinct sensory and affective dimensions are discussed, and areas for future research are proposed. Despite dyspnea's clinical prevalence and impact, management of dyspnea languishes decades behind the treatment of pain. The neurophysiological bases of current therapeutic approaches are reviewed; however, a better understanding of the neural mechanisms of dyspnea may lead to development of novel therapies and improved patient care.
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To the best of our knowledge, no studies have examined the relationship of low tidal volume ventilation strategies to adverse psychiatric outcomes; however, there are numerous reasons to think a link may exist. Low tidal volume ventilation strategies conflict with the most straightforward form of symptomatic relief from dyspnea: a bigger breath.37 Patients with ARDS who are receiving low-tidal volume breaths are more likely to experience dyspnea and more likely to be mechanically ventilated for a prolonged period of time, which may put them at increased risk for development of PTSD symptoms.25
Dyspnea is an uncomfortable sensation with the potential to cause psychological trauma. Patients presenting with acute respiratory failure, particularly when tidal volume is restricted during mechanical ventilation, may experience the most distressing form of dyspnea known as air hunger. Air hunger activates brain pathways known to be involved in posttraumatic stress disorder (PTSD), anxiety, and depression. These conditions are considered part of the post-intensive care syndrome. These sequelae may be even more prevalent among patients with ARDS. Low tidal volume, a mainstay of modern therapy for ARDS, is difficult to avoid and is likely to cause air hunger despite sedation. Adjunctive neuromuscular blockade does not prevent or relieve air hunger, but it does prevent the patient from communicating discomfort to caregivers. Consequently, paralysis may also contribute to the development of PTSD. Although research has identified post-ARDS PTSD as a cause for concern, and investigators have taken steps to quantify the burden of disease, there is little information to guide mechanical ventilation strategies designed to reduce its occurrence. We suggest such efforts will be more successful if they are directed at the known mechanisms of air hunger. Investigation of the antidyspnea effects of sedative and analgesic drugs commonly used in the ICU and their impact on post-ARDS PTSD symptoms is a logical next step. Although in practice we often accept negative consequences of life-saving therapies as unavoidable, we must understand the negative sequelae of our therapies and work to minimize them under our primary directive to “first, do no harm” to patients.
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Reduced tidal volume increases ‘air hunger’ at fixed PCO2 in ventilated quadriplegics

Abstract

Respir. Physiol.

Breathlessness during different forms of ventilatory stimulation: a study of mechanisms in normal subjects and respiratory patients

Clin. Sci.

Diaphragm activity during breath-holding: factors related to its onset

J. Appl. Physiol.

High-level quadriplegics perceive lung volume change

J. Appl. Physiol.

‘Air hunger’ arising from increased PCO2 in mechanically ventilated quadriplegics

Respir. Physiol.

‘Air hunger’ from increased PCO2 persists after complete neuromuscular block in humans

Respir. Physiol.

Effects of changes in CO2 partial pressure on the sensation of respiratory drive

J. Appl. Physiol.

Respiratory associated rhythmic firing of midbrain neurones in cats: Relation to level of respiratory drive

J. Physiol. (London)

Respiratory associated rhythmic firing of thalamic neurons: Relation to level of respiratory drive

FASEB J.

Effects of voluntary constraining of thoracic displacement during hypercapnia

J. Appl. Physiol.

Reduced tidal volume increases ‘air hunger’ at fixed P_CO₂ in ventilated quadriplegics

‘Air hunger’ arising from increased P_CO₂ in mechanically ventilated quadriplegics

‘Air hunger’ from increased P_CO₂ persists after complete neuromuscular block in humans

Effects of changes in CO₂ partial pressure on the sensation of respiratory drive