Control of arrhythmic breathing in bimodal breathers: Amphibia

1988 ◽  
Vol 66 (1) ◽  
pp. 6-19 ◽  
Author(s):  
Robert G. Boutilier

Amphibians employ a system of gas exchange whereby various combinations of the lungs, gills, and skin are used to exploit gas exchanges in both air and water (bimodal breathing). Continuous lung ventilation is rarely observed in these animals. Instead, the dominant breath pattern is arrhythmic in nature and is believed to have evolved in response to a periodic need to supplement aquatic gas exchange. Such a need is largely dependent on the activity state of the animal concerned and its capacity for aquatic gas exchange. The overall control system appears to be one that turns lung ventilation on and off by trigger signals arising from chemo- and mechano-sensitive receptors responding to changing conditions during periods of breath holding and breathing. In amphibians in which the aquatic exchanger is a major avenue for CO2 elimination, [Formula: see text] levels in the lungs and blood do not change substantially in the latter stages of a breath hold. Under these conditions falling levels of oxygen may be the primary stimulus to terminate the breath hold and initiate breathing. There is, however, some interaction between the two gases since elevated CO2 levels affect the sensitivity of the predominantly O2-mediated response. Another major component in determining air-breathing patterns in these animals is their ability to delay the onset of breathing when certain behavioural activities take precedence over the need for additional gas exchange.

1988 ◽  
Vol 66 (1) ◽  
pp. 109-123 ◽  
Author(s):  
G. Shelton ◽  
P. C. Croghan

Control of breathing and gas exchange has been extensively investigated in unimodal animals, particularly mammals, in which ventilation is characteristically a regular and continuous process and gas exchange approximates to a steady-state system. Both static and dynamic models have been developed in control-theory analyses. Similar analyses are possible in unimodal fish, though few have been carried out. Control in bimodal animals, such as air-breathing fish and amphibians, is more difficult to understand and model. The evolutionary change from water to air breathing in vertebrates involves not only the adjustment of many control processes but also the development, in the early stages, of non steady states in gas exchangers, blood, and tissues. A simple control-system model, differing from mammalian counterparts in its greater emphasis on storage functions and its intermittently activated controller, is described for two suggested stages in the evolution of air breathing. The first of these stages is air gulping, in which a fixed and rather brief pattern of air breathing is activated by internal signals generated as a result of the inadequacy of the gills to provide sufficient oxygen for tissue metabolism. The second stage is that of burst breathing, in which lung ventilation is both begun and ended by internal signals so that burst duration is variable. The effects of adjusting parameters on variables of evolutionary importance, such as dive duration, burst duration, store renewal, and metabolic rate, can be examined in these two versions of the model. Refinements to incorporate arterial and venous compartments in the circulatory system, the shunting of venous and arterial blood streams in the heart, realistic oxygen dissociation curves, controller inputs from a wider range of sources, and the capacity to respond to some conditions with changes in ventilation rate as well as in burst and dive durations, are being developed. They should make the complex, non-steady-state interactions between gas exchangers, circulating blood, and tissues easier to understand and indicate the likely steps toward the evolution of steady-state systems seen in birds and mammals.


2000 ◽  
Vol 203 (11) ◽  
pp. 1671-1678 ◽  
Author(s):  
C.G. Farmer ◽  
D.R. Carrier

A number of anatomical characters of crocodilians appear to be inconsistent with their lifestyle as sit-and-wait predators. To address this paradoxical association of characters further, we measured lung ventilation and respiratory gas exchange during walking in American alligators (Alligator mississippiensis). During exercise, ventilation consisted of low-frequency, large-volume breaths. The alligators hyperventilated severely during walking with respect to their metabolic demands. Air convection requirements were among the highest and estimates of lung P(CO2) were among the lowest known in air-breathing vertebrates. Air convection requirements dropped immediately with cessation of exercise. These observations indicate that the ventilation of alligators is not limited by their locomotor movements. We suggest that the highly specialized ventilatory system of modern crocodilians represents a legacy from cursorial ancestors rather than an adaptation to a lifestyle as amphibious sit-and-wait predators.


2001 ◽  
Vol 281 (2) ◽  
pp. R490-R494 ◽  
Author(s):  
R. G. Boutilier ◽  
J. Z. Reed ◽  
M. A. Fedak

Breath-by-breath measurements of end-tidal O2 and CO2 concentrations in harbor porpoise reveal that the respiratory gas exchange ratio (RR; CO2 output/O2 uptake) of the first lung ventilation in a breathing bout after a prolonged breath-hold is always well below the animal's metabolic respiratory quotient (RQ) of 0.85. Thus the longest apneic pauses are always followed by an initial breath having a very low RR(0.6–0.7), which thereafter increases with each subsequent breath to values in excess of 1.2. Although the O2 stores of the body are fully readjusted after the first three to four breaths following a prolonged apneic pause, a further three to four ventilations are always needed, not to load more O2 but to eliminate built-up levels of CO2. The slower readjustment of CO2 stores relates to their greater magnitude and to the fact that they must be mobilized from comparatively large and chemically complex HCO[Formula: see text]/CO2 stores that are built up in the blood and tissues during the breath-hold. These data, and similar measurements on gray seals (12), indicate that it is the readjustment of metabolic RQ and not O2 stores per se that governs the amount of time an animal must spend ventilating at the surface after a dive.


1994 ◽  
Vol 197 (1) ◽  
pp. 429-436
Author(s):  
M Hedrick ◽  
S Katz ◽  
D Jones

The ventilatory patterns of air-breathing fish are commonly described as 'arrhythmic' or 'irregular' because the variable periods of breath-holding are punctuated by seemingly unpredictable air-breathing events (see Shelton et al. 1986). This apparent arrhythmicity contrasts with the perceived periodism or regularity in the gill ventilation patterns of some fish and with lung ventilation in birds and mammals. In this sense, periodism refers to behaviour that occurs with a definite, recurring interval (Bendat and Piersol, 1986). The characterisation of aerial ventilation patterns in fish as 'aperiodic' has been generally accepted on the basis of qualitative examination and it remains to be validated with rigorous testing. The bowfin, Amia calva (L.), is a primitive air-breathing fish that makes intermittent excursions to the air­water interface to gulp air, which is transferred to its well-vascularized gas bladder. Its phylogenetic position as the only extant member of the sister lineage of modern teleosts affords a unique opportunity to examine the evolution of aerial ventilation and provides a model for the examination of ventilatory patterns in primitive fishes. To establish whether Amia calva exhibit a particular pattern of air-breathing, we examined time series records of aerial ventilations from undisturbed fish over long periods (8 h). These records were the same as those used to calculate average ventilation intervals under a variety of experimental conditions (Hedrick and Jones, 1993). Their study also reported the occurrence of two distinct breath types. Type I breaths were characterised by an exhalation followed by an inhalation, whereas type II breaths were characterised by inhalation only. It was also hypothesized that the type I breaths were employed to meet oxygen demands, whereas the type II breaths were used to regulate gas bladder volume. However, they did not investigate the potential presence of a periodic ventilatory pattern. We now report the results of just such an analysis of ventilatory pattern that demonstrates a clear periodism to air-breathing in a primitive fish.


1988 ◽  
Vol 66 (1) ◽  
pp. 99-108 ◽  
Author(s):  
William K. Milsom

Arrhythmic breathing patterns of two basic types occur among the air-breathing vertebrates. These patterns, which appear to be dependent more on inputs from peripheral receptor groups than on a central generator, allow significant fluctuations in the partial pressures of O2 and CO2 in lungs, blood, and tissues with accompanying fluctuations of pH in body fluids. The major components of each pattern are the size and timing of each breath, the length of each episode of breathing, and the length of the pause between episodes of breathing. While each of these components appears to be under separate control, the relative roles of the various receptor groups in the control of each remain unclear. Similarities between data collected from reptiles and hibernating mammals suggest that the arrhythmic breathing patterns seen under physiological conditions in all air-breathing vertebrates may be manifestations of a common control system. The conversion from continuous to arrhythmic breathing seen in mammals entering hibernation further suggests that both continuous and arrhythmic breathing are manifestations of a common control system. The two distinct arrhythmic breathing patterns appear to arise from differences in the supramedullary integration of vagal input in different species. It is suggested that under conditions of reduced metabolic demand, these arrhythmic breathing patterns may represent an adaptive strategy which, in part, serves to reduce the energetic cost of ventilation.


2018 ◽  
Vol 285 (1877) ◽  
pp. 20180482 ◽  
Author(s):  
Daniel Garcia Párraga ◽  
Michael Moore ◽  
Andreas Fahlman

Hydrostatic lung compression in diving marine mammals, with collapsing alveoli blocking gas exchange at depth, has been the main theoretical basis for limiting N 2 uptake and avoiding gas emboli (GE) as they ascend. However, studies of beached and bycaught cetaceans and sea turtles imply that air-breathing marine vertebrates may, under unusual circumstances, develop GE that result in decompression sickness (DCS) symptoms. Theoretical modelling of tissue and blood gas dynamics of breath-hold divers suggests that changes in perfusion and blood flow distribution may also play a significant role. The results from the modelling work suggest that our current understanding of diving physiology in many species is poor, as the models predict blood and tissue N 2 levels that would result in severe DCS symptoms (chokes, paralysis and death) in a large fraction of natural dive profiles. In this review, we combine published results from marine mammals and turtles to propose alternative mechanisms for how marine vertebrates control gas exchange in the lung, through management of the pulmonary distribution of alveolar ventilation ( ) and cardiac output/lung perfusion ( ), varying the level of in different regions of the lung. Man-made disturbances, causing stress, could alter the mismatch level in the lung, resulting in an abnormally elevated uptake of N 2 , increasing the risk for GE. Our hypothesis provides avenues for new areas of research, offers an explanation for how sonar exposure may alter physiology causing GE and provides a new mechanism for how air-breathing marine vertebrates usually avoid the diving-related problems observed in human divers.


1963 ◽  
Vol 18 (3) ◽  
pp. 471-477 ◽  
Author(s):  
E. H. Lanphier ◽  
H. Rahn

Use of a recompression chamber permitted simulation of breath-hold dives to 33 ft of sea water (2 atm abs). Four normal subjects made such dives during rest and mild exertion while delivering alveolar gas samples at frequent intervals by a partial-rebreathing procedure. The course of alveolar gas exchange differed greatly from that in ordinary breath holding. Oxygen uptake remained at near normal levels until ascent owing to the maintenance of alveolar Po2 by increased ambient pressure. Reversal of CO2 transfer occurred during descent, and little CO2 moved in the normal direction until ascent. Greater uptake of oxygen and retention of CO2 in the body led to lower final values of both alveolar Po2 and Pco2 than in comparable breath holding at the surface. Hyperventilation made possible longer dives with harder work, and in these the Po2 reached very low values on ascent. One subject showed a final Po2 of 24 mm Hg with evidence of reversed O2 transfer. Acute hypoxia on ascent is a likely cause of drowning in breath-hold diving. Submitted on October 17, 1962


Critical Care ◽  
2021 ◽  
Vol 25 (1) ◽  
Author(s):  
Ludovico Messineo ◽  
Elisa Perger ◽  
Luciano Corda ◽  
Simon A. Joosten ◽  
Francesco Fanfulla ◽  
...  

Abstract Background Despite considerable progress, it remains unclear why some patients admitted for COVID-19 develop adverse outcomes while others recover spontaneously. Clues may lie with the predisposition to hypoxemia or unexpected absence of dyspnea (‘silent hypoxemia’) in some patients who later develop respiratory failure. Using a recently-validated breath-holding technique, we sought to test the hypothesis that gas exchange and ventilatory control deficits observed at admission are associated with subsequent adverse COVID-19 outcomes (composite primary outcome: non-invasive ventilatory support, intensive care admission, or death). Methods Patients with COVID-19 (N = 50) performed breath-holds to obtain measurements reflecting the predisposition to oxygen desaturation (mean desaturation after 20-s) and reduced chemosensitivity to hypoxic-hypercapnia (including maximal breath-hold duration). Associations with the primary composite outcome were modeled adjusting for baseline oxygen saturation, obesity, sex, age, and prior cardiovascular disease. Healthy controls (N = 23) provided a normative comparison. Results The adverse composite outcome (observed in N = 11/50) was associated with breath-holding measures at admission (likelihood ratio test, p = 0.020); specifically, greater mean desaturation (12-fold greater odds of adverse composite outcome with 4% compared with 2% desaturation, p = 0.002) and greater maximal breath-holding duration (2.7-fold greater odds per 10-s increase, p = 0.036). COVID-19 patients who did not develop the adverse composite outcome had similar mean desaturation to healthy controls. Conclusions Breath-holding offers a novel method to identify patients with high risk of respiratory failure in COVID-19. Greater breath-hold induced desaturation (gas exchange deficit) and greater breath-holding tolerance (ventilatory control deficit) may be independent harbingers of progression to severe disease.


Diagnostics ◽  
2021 ◽  
Vol 11 (4) ◽  
pp. 634
Author(s):  
Weon Jang ◽  
Ji Soo Song ◽  
Sang Heon Kim ◽  
Jae Do Yang

While magnetic resonance cholangiopancreatography (MRCP) is routinely used, compressed sensing MRCP (CS-MRCP) and gradient and spin-echo MRCP (GRASE-MRCP) with breath-holding (BH) may allow sufficient image quality with shorter acquisition times. This study qualitatively and quantitatively compared BH-CS-MRCP and BH-GRASE-MRCP and evaluated their clinical effectiveness. Data from 59 consecutive patients who underwent both BH-CS-MRCP and BH-GRASE-MRCP were qualitatively analyzed using a five-point Likert-type scale. The signal-to-noise ratio (SNR) of the common bile duct (CBD), contrast-to-noise ratio (CNR) of the CBD and liver, and contrast ratio between periductal tissue and the CBD were measured. Paired t-test, Wilcoxon signed-rank test, and McNemar’s test were used for statistical analysis. No significant differences were found in overall image quality or duct visualization of the CBD, right and left 1st level intrahepatic duct (IHD), cystic duct, and proximal pancreatic duct (PD). BH-CS-MRCP demonstrated higher background suppression and better visualization of right (p = 0.004) and left 2nd level IHD (p < 0.001), mid PD (p = 0.003), and distal PD (p = 0.041). Image quality degradation was less with BH-GRASE-MRCP than BH-CS-MRCP (p = 0.025). Of 24 patients with communication between a cyst and the PD, 21 (87.5%) and 15 patients (62.5%) demonstrated such communication on BH-CS-MRCP and BH-GRASE-MRCP, respectively. SNR, contrast ratio, and CNR of BH-CS-MRCP were higher than BH-GRASE-MRCP (p < 0.001). Both BH-CS-MRCP and BH-GRASE-MRCP are useful imaging methods with sufficient image quality. Each method has advantages, such as better visualization of small ducts with BH-CS-MRCP and greater time saving with BH-GRASE-MRCP. These differences allow diverse choices for visualization of the pancreaticobiliary tree in clinical practice.


1990 ◽  
Vol 63 (1) ◽  
pp. 117-139 ◽  
Author(s):  
Peter Greenaway ◽  
Caroline Farrelly
Keyword(s):  

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