How Healthy Dogs Breathe: Respiratory Physiology Determines Physical Exam Findings
Respiration requires an integrated system of control (CNS), movement of a bellows (ribs and associated muscle) to draw air into the lungs, exchange of gas within the lung, and a feedback system (chemoreceptors, stretch receptors) to close the loop. This lecture will present some basic elements of the bellows part of this system, providing a basis for evaluation of respiratory patterns in the dog.
Lungs Collapse, Chests Spring Out
Lungs are a viscoelastic tissue suspended within the pleural cavity. If the chest is opened to the atmosphere the lungs collapse until small airway occlusion prevents further loss of gas. The collapse won't stop until the lung volume is quite a bit smaller than the normal functional residual capacity (FRC) in the intact animal. The lung volume in a normal animal is maintained by support from the thoracic wall. Because there is an airtight seal within the pleural space and the lungs are coupled to the chest wall with a viscous fluid, the tendency of the lungs to collapse is countered by the tendency of the ribs to spring out. Between breaths, these opposing forces yield a pleural pressure of -5 cm H2O at the 8th-9th interspace in an average size dog. Breathing takes place around this equilibrium, with most of the energy of breathing expended to increase the thoracic volume above the equilibrium point during inspiration.
The ribs in the dog (and cat) are arranged in such a manner that most movement, and the inspiratory effect of that movement, is related to cranial displacement of the ribs during inspiration (Figure 1). Because of the 'bucket handle' relationship between the ribs and the spine and the caudal sweep of the ribs when the lungs are at functional residual capacity (FRC), cranial displacement of the ribs results in an increase in thoracic diameter and intrathoracic volume, a reduction in pleural pressure, and inspiration.1 Therefore, any muscles that move the ribs forward and outward will contribute to inspiration, and any that move the ribs caudally and/or inward will contribute to exhalation. Until recently, the usual explanation for intercostal muscle function was based on the theory of Hamberger (1697-1755). He proposed that the external intercostals, because they where anchored high on the cranial rib (closer to its axis of rotation) and lower on the caudal rib (further away) at each intercostal space, must have a net effect of raising the caudal rib, producing inspiration. Similarly, the internal intercostals, with their origins high on the caudal rib and insertions lower on the cranial rib at each space, must have a net effect of pulling the cranial rib more caudally, producing exhalation. This served, without experimental verification, as the leading explanation for intercostal function until the 1980's. Since then major advances in understanding have been obtained by the efforts of a small number of physiologist using the dog as a model. From this work comes an appreciation that the act of breathing is very complex, and the effects of muscle activation depend on many factors including location (dorsoventral and craniocaudal), muscle mass, patterns of innervation, and locomotion.2
Respiratory Muscle and 'Abdominal Breathing'
The primary muscles of inspiration include the diaphragm, levator costae, internal intercostals (ventrocranial), and external intercostals (dorsocranial). The primary muscles of exhalation include the triangularis sterni and dorsocaudal internal intercostals. Accessory muscles of respiration are those that do not normally participate in breathing unless called upon during periods of high demand. Accessory muscles of inspiration include the scalenes and the sternomastoids. Accessory muscles of exhalation include the four abdominal muscle groups: rectus abdominis, external oblique, internal oblique, and transverses abdominis. Accessory muscles of respiration have other primary roles such as movement of the head and neck (sternomastoids), stabilization of the spine (scalene), flexors and rotators of the trunk (rectus and obliques), and their function is synchronized with breathing when conditions demand. Contraction of the abdominal muscles increases intra-abdominal pressure and forces the diaphragm to a more cranial position within the rib cage. They can only assist with exhalation, and the term "abdominal breathing" is therefore properly used to indicate vigorous exhalation.
Location, Location, Location
As depicted in Figures 2 and 3, the external and internal intercostals in the cranial intercostal spaces have an inspiratory bias, and the same muscles in the caudal intercostal spaces have an expiratory bias.
Figure 2. Inspiratory actions of the internal intercostals (left) and external intercostals (right). The shaded areas represent locations where the mechanical advantage and net respiratory effects favor inspiration at FRC. The portion of the internal intercostals between the bony rib elements of the first few spaces remain electrically silent during breathing, and the external intercostals in this region, when active, are active only during inspiration.
Figure 3. Expiratory actions of the internal intercostals (left) and external intercostal (right). The shaded areas represent locations where the mechanical advantage and net respiratory effects favor exhalation at FRC. This region of the internal intercostals, when active, is active only during expiration. This region of external intercostals is electrically silent during tidal breathing.
The muscle mass of the external intercostals is greatest in the dorsocranial region where they possess the greatest mechanical advantage for inspiration. The parasternal internal intercostals are a special group of internal intercostal muscles that play a greater role than the externals in inspiration during rest. These muscles also have a large mass and they possess a mechanical advantage for inspiration in every intercostal space. Their orientation is such that contraction produces outward movement of the distal rib relative to the sternum. They have a comparatively large effect on inspiration because they move the chondral aspect of the ribs outward, away from the midline. In the dog any given movement in the outward direction is roughly 4 times more effective at increasing lung volume than comparable movement in the cranial direction.3
The levator costae and parasternal and external intercostals are active during inspiration. Levator costae originate on the transverse process of the thoracic vertebrae and extend caudally to insert on the dorsal-cranial aspect of the rib so when they contract they rotate the ribs cranially. This muscle works in concert with the parasternal intercostals to provide most of the rostral rib displacement during inspiration. The levator costae and parasternal intercostals appear to function exclusively for breathing. In contrast, the function of the interosseous portions of the intercostal muscles may be given over to stabilization of the torso during activity. For example, in trotting dogs the activity of the intercostal muscles becomes synchronized with locomotion and drifts relative to the phase of respiration.4 Therefore, in active dogs the interosseous portions of the intercostal muscles are more important for stabilizing the trunk for locomotion than for any direct role in breathing. However, their action stabilizes the rib cage, which is essential for optimal function of the other respiratory muscles.
Exhalation: Never Passive in Dogs
The triangularis sterni and internal intercostals are active during expiration. In particular, the triangularis sterni muscle is active even during quiet breathing, and is independent of both body position and intercostal activity.5 Figure 4 illustrates the orientation of this muscle from a view inside the thorax. The muscle extends from the caudal half of the deep aspect of the sternum to the chondral (parasternal) portion of ribs 2-7. When it contracts, the triangularis sterni displaces the ribs caudally and the sternum cranially, positioning the ribs for a greater mechanical advantage and lengthening the parasternal intercostal muscles to enhance their function during the next breath.
The diaphragm is now considered to be a combination of two functionally discrete muscles, the costal and crural diaphragm. The muscles separate the abdominal cavity from the thoracic, and diaphragm function is essential for effective ventilation. Contraction of the diaphragm in inspiration causes it to flatten and move the liver and abdominal viscera caudally into the abdominal cavity. However, because it is anchored to the chodral arch and caudal ribs, contraction of the diaphragm pulls this region of the rib cage rostrally. When working in concert with the parasternal intercostals and levator muscles the diaphragm assists in the craniolateral rib displacement of inspiration to increase thoracic girth and volume. The effect on airway pressure of this combined effort is significantly greater than the sum of the individual contributions from diaphragm and rib muscles.6
Figure 5. Relationship between the diaphragm and ribs during exhalation (left) and inspiration (right). Essential aspects include the spherical shape of the dome region (which greatly enhances the muscle's mechanical advantage) and the anchor to the chondral arch.
Don't Confuse Fast Breathing with Panting
Panting is a thermoregulatory maneuver and is the most important method of evaporative cooling in dogs exposed to heat or exercise. It has minimal impact on gas exchange. When the skin (environmental trigger) or core temperature (exercise) temperature rise, respiration shifts to a pattern optimized to remove heat from the body. The diaphragm and other muscles of respiration generate a rhythmic motion that cycles at a frequency of 3.5-5 Hz. The precise frequency is closely related to the resonant frequency for the individual, thus body conformation and the unique characteristics of that individual's respiratory system determine the rate. The oropharynx and larynx move in synchrony to 'valve' the system and provide an efficient unidirectional flow of air over the evaporative surface of the mouth.7 When the need is minimal, dogs will pant through the nose. As need for heat loss increases, dogs oscillate between two patterns: a) inhalation through the nose, exhalation through the nose and mouth and b) inhalation through the nose and mouth, exhalation through the nose and mouth. Lingual blood flow increases 6 fold, and the tongue, wet from increased salivation, hangs out of the mouth as it lengthens to increase its surface area.8
Panting requires a dramatic increase in minute ventilation, but blood gases do not change appreciably (although in severe heat stress panting will cause a significant respiratory alkalosis for a short period). This is possible because most of the increase in ventilation that occurs during panting is dead space ventilation, and the inspiratory volume is only slightly larger than the anatomical dead space of the airways. Ventilation is maintained owing to the principles of jet ventilation: individual molecules of gas enter the trachea at very high speeds. Mixing of gas in distal airways is enhanced by asynchronous contractions of the crural and costal segments of the diaphragm, and there is net displacement of carbon dioxide out and oxygen in.9
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