Is the Lung Built for Exercise? Advances and Unresolved Questions

Abstract

Nearly 40 yr ago, Professor Dempsey delivered the 1985 ACSM Joseph B. Wolffe Memorial Lecture titled: "Is the lung built for exercise?" Since then, much experimental work has been directed at enhancing our understanding of the functional capacity of the respiratory system by applying complex methodologies to the study of exercise. This review summarizes a symposium entitled: "Revisiting 'Is the lung built for exercise?'" presented at the 2022 American College of Sports Medicine annual meeting, highlighting the progress made in the last three-plus decades and acknowledging new research questions that have arisen. We have chosen to subdivide our topic into four areas of active study: (i) the adaptability of lung structure to exercise training, (ii) the utilization of airway imaging to better understand how airway anatomy relates to exercising lung mechanics, (iii) measurement techniques of pulmonary gas exchange and their importance, and (iv) the interactions of the respiratory and cardiovascular system during exercise. Each of the four sections highlights gaps in our knowledge of the exercising lung. Addressing these areas that would benefit from further study will help us comprehend the intricacies of the lung that allow it to meet and adapt to the acute and chronic demands of exercise in health, aging, and disease.

FIGURE 1—

Hypothesis: in the untrained, the capacity for O₂ transport by the pulmonary system (lungs and chest wall) far exceeds that of the cardiovascular system and the oxidative capacity of the limb locomotor muscles. The high $\stackrel{.}{\mathbf{V}}{\mathbf{O}}_{2\mathbf{max}}$ in the highly trained athlete is accompanied by increased capacities of the left heart, locomotor muscle mitochondria and capillarity, and red cell mass, but with minimal alteration in lung structure between trained and untrained. Thus, eventually the capacity of the pulmonary system for O₂ transport cannot meet the superior demands imposed by the limbs and cardiovascular systems; arterial blood gas and acid–base homeostasis fail, and the lungs become a significant limitation to performance capacity. Original caption from Dempsey (2).

FIGURE 2—

Muscle Organ Xtalk: The “Exercise Factor.” As proposed two decades ago by Bente Pedersen and colleagues, contracting muscle operates as an endocrine organ producing and secreting hundreds of myokines, which exert their effects in autocrine, paracrine, or endocrine fashion. Xtalk effects of a select number of these myokines have been shown to occur between the skeletal muscle and several other organs as well as within the muscle itself. This review focuses on whether exercise training might grow, restore, or prevent loss of structure/function in the young, aging, or diseased lung and whether the metabolic and anti-inflammatory effects of the “exercise factor” might represent one avenue for this influence on the lung and specifically on respiratory bronchiolar secretory cells, as it does for other organs. Modified from Severinsen and Pedersen (13).

FIGURE 3—

The relationship between airway generation, airway resistance, and OCT measured luminal area. A, Airway resistance for a given airway generation. Airway generations measured using OCT in panels C and D are highlighted in black. Also included is Poiseuille’s equation to highlight the importance of airway radius. B, Airway tree highlighting how airway generations are numbered. C, Individual female and male luminal area data measured using OCT for airway generations 4–8. D, Fourth- to eighth-airway-generation OCT images of a representative female subject. The imaging probe, which is 0.9 mm in diameter, can be seen within the airway lumen in OCT images. OCT data in panels C and D are from Peters et al. (77).

FIGURE 4—

Research questions related to pulmonary gas exchange illustrated in a schematic diagram of a three-compartment lung. In order for efficient gas exchange to occur, there must be delivery of fresh gas to the alveoli that is well matched to perfusion of the pulmonary capillaries. Here, low (0.1, in this case because of airway obstruction), optimal (1), and high (10, in this case because of reduced perfusion) ventilation–perfusion ratios are shown. When ventilation–perfusion ratio is not close to 1, gas exchange is less efficient. Oxygen and carbon dioxide diffuse passively down their concentration gradients, and diffusion may be incomplete in some circumstances. Blood that bypasses gas exchange is termed a shunt. Alone or in combination, ventilation–perfusion mismatch, diffusion limitation, and/or shunt decreases pulmonary gas exchange efficiency and causes hypoxemia. This is reflected in the AaDO₂. Some unresolved research questions regarding pulmonary gas exchange impairments with exercise relate to the following: 1) differences in the AaDO₂ by sex and with aging, 2) direct evidence for exercise-induced interstitial edema affecting ventilation–perfusion mismatch, 3) mechanisms of exercise-induced diffusion limitation for oxygen, and 4) possible circumstances where intrapulmonary arteriovenous anastomoses affect gas exchange in humans.

FIGURE 5—

Schematic of a “two-way street” of sympathetic vasoconstrictor activity emanating from both limb and respiratory muscle metaboreceptors during exercise, which serves to constrain blood flow and O₂ transport. High-intensity contractions of both sets of muscles cause increased group III and IV afferent activity leading to a sympathetically mediated vasoconstriction of respiratory and limb locomotor muscle vasculatures, thereby contributing to their mutual fatigue during whole-body exercise. Figure and original caption from Sheel et al. (35).