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Metabolism, Temperature, and Ventilation

Jacopo P. Mortola, Michael Maskrey

10.1002/cphy.c100008

Source: Volume 1, Issue 4, October 2011

Published online: October 2011

Full Article on Wiley Online Library



Abstract

In mammals and birds, all oxygen used ( o2) must pass through the lungs; hence, some degree of coupling between o2 and pulmonary ventilation ( e) is highly predictable. Nevertheless, e is also involved with CO2 elimination, a task that is often in conflict with the convection of O2. In hot or cold conditions, the relationship between e and o2 includes the participation of the respiratory apparatus to the control of body temperature and water balance. Some compromise among these tasks is achieved through changes in breathing pattern, uncoupling changes in alveolar ventilation from e. This article examines primarily the relationship between e and o2 under thermal stimuli. In the process, it considers how the relationship is influenced by hypoxia, hypercapnia or changes in metabolic level. The shuffling of tasks in emergency situations illustrates that the constraints on e‐ o2 for the protection of blood gases have ample room for flexibility. However, when other priorities do not interfere with the primary goal of gas exchange, e follows metabolic rate quite closely. The fact that arterial CO2 remains stable when metabolism is changed by the most diverse circumstances (moderate exercise, cold, cold and exercise combined, variations in body size, caloric intake, age, time of the day, hormones, drugs, etc.) makes it unlikely that e and metabolism are controlled in parallel by the condition responsible for the metabolic change. Rather, some observations support the view that the gaseous component of metabolic rate, probably CO2, may provide the link between the metabolic level and e. © 2011 American Physiological Society. Compr Physiol 1:1679‐1709, 2011.

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Figure 1. Figure 1.

Body temperature (top) and arterial (or end‐tidal) pressure of CO2 (PCO2) in mammals of different body weight (in log scale). Each symbol is the average value of a different species. Data of Tb are collected from the literature; data of PCO2 are namely from the data compiled in ref. 322.
Figure 2. Figure 2.

Responses of pulmonary ventilation (e) and oxygen consumption (o2) to cold, expressed in percent of the values in warm conditions. Each symbol is the average of literature data pertinent to some avian (open triangles) or mammalian species (open circles). In first approximation, e and o2 increase in proportion, although in the large majority of cases the data points are slightly below the line of identitiy (dashed line), indicating a small tendency for a reduction of the ventilatory equivalent in the cold. Data of birds refer to pigeons [averaged from refs 23,27,47], parrots 54, chuckars 71, and penguins 73. Data of mammals are for deer mouse, marmot, rat, chipmunk, and other small rodents 65,69,70,146,386, bat 72, cat (anesthetized) 148, pig 198, sheep 214, man 192,337, and some marsupials [Tasmanian devil, during nonshivering conditions 339; kowari, at 0‐15°C 171; bandicoot 242; numbat 84; sandhill dunnart 484; chuditch 400; honey possum 83].
Figure 3. Figure 3.

Ventilation (e)‐Oxygen consumption (o2) values in rats during normoxia (open symbols) and hypoxia (filled symbols) in warm (circles, 25°C) and cold conditions (triangles, 10°C). Oblique dashed lines indicate isoventilatory equivalents (e/o2); in brackets are the mean partial pressures of arterial O2 and CO2, respectively. During cold, the ventilatory equivalent may be slightly lower than in warm conditions, with normal blood gases.

[Redrawn from ref. 386].
Figure 4. Figure 4.

Schematic summary of common effects of cold (left portion) and warm exposure (right portion) on some respiratory variables.
Figure 5. Figure 5.

Newborn dogs, 1‐week old, in warm (30°C) and cold (20° C) conditions. In the cold, the thermogenic effort (increased in oxygen consumption, o2) was not sufficient to maintain body temperature (Tb). Alveolar ventilation (a) increased appropriately to maintain arterial PCO2. Hence, the Q10 effect of Tb had no negative impact on the metabolic stimulus on a.

[Reconstructed from the data of ref. 380].
Figure 6. Figure 6.

Oxygen consumption‐ventilation relationship in human subjects during cold exposure at rest (open circles) and during muscle exercise (filled circles). The data points follow a unique relationship, irrespective of the factor raising metabolic rate.

[Redrawn from 337]
Figure 7. Figure 7.

Difference between hypoxic (∼10% inspired O2) and normoxic oxygen consumption (o2), normalized by body weight in newborn (open symbols) and adult mammals (filled symbols). Each symbol refers to a different species, listed in ref. 130,298. Horizontal dashed line indicates no difference between the hypoxic and normoxic o2. The oblique line is the line of identity. In general, the higher the o2 (per unit weight) in normoxia the greater its hypoxic drop.

[Slightly modified from ref. 300]
Figure 8. Figure 8.

Schema of the metabolism‐ventilation relationship in normoxia (any point on the continuous line, Paco2 = k) and hypoxia (dashed oblique line). Any point on the hypoxic line indicates the same degree of hyperventilation (Paco2 = 0.5 k). A greater hyperpnea (or hypoxic ventilatory response, HVR) is required when metabolic rate is high. Hence, at B the HVR, represented by Bhx‐B, is greater than at A, represented by Ahx‐A. The dashed arrows to Ahx′′, Bhx′, and Bhx′′ indicate instances of hypoxic hypometabolism. In these cases, the HVR is less than in the absence of hypoxic hypometabolism and could have a negative value (cases Bhx′′ and Ahx′′), even though the hyperventilation remains the same.
Figure 9. Figure 9.

Data of oxygen consumption (o2), alveolar ventilation (a), body temperature (Tb), and arterial pressure of CO2 (Paco2) in 11‐day‐old dogs exposed to various concentrations of O2, from normoxia (21%) to medium and severe hypoxia, in warm (ambient temperature 30°C) and cold (20°C) conditions. In the cold, o2 is high because of thermogenesis, and it plummets in hypoxia. The a responses vary drastically with temperature, even though the degree of hypoxic hypeventilation (drop in Paco2) is the same. Note that the important decrease in Tb during hypoxia in the cold does not modify the hyperventilation.

[Reconstructed from the original data of ref. 380]
Figure 10. Figure 10.

Oxen in severe heat. e, pulmonary ventilation; a, alveolar ventilation; d, dead space ventilation; Vt, tidal volume; f, breathing frequency. Paco2, arterial pressure of CO2. As hyperthermia progressed, the breathing pattern switched from rapid and shallow to deep and slow, aggravating the hypocapnia.

[From the data published in ref. 167, Table 4)]
Figure 11. Figure 11.

Breath‐by‐breath relationship of end‐tidal pressure of CO2 and pulmoanry ventilation in one human subject at normal (open circles) and elevated (closed circles) body temperature during hyperoxic rebreathing after prior hyperventilation. The arrow indicates the threshold of the response. Elevated temperature did not modify the threshold but increased the slope of the curve above the threshold, or e sensitivity to CO2.

[Redrawn from ref. 20]
Figure 12. Figure 12.

Relationship between the concentration of serum progesterone (in log scale) and arterial PCO2 in women during various phases of the reproductive cycle.

[redrawn from ref. 256)]
Figure 13. Figure 13.

Pharmacologic increase in metabolic rate (in multiples of resting oxygen consumption) with uncouplers of oxidative phosphorylation. Often, large increases in o2 caused no or small degree of hyperventilation. Dashed line, no change in arterial PCO2. Symbols are mean values in dogs (triangles) and rats (squares). Compiled from the data of refs 194,246,247,248,365,390.
Figure 14. Figure 14.

Mean values of oxygen consumption (o2), pulmonary ventilation (e), and ventilatory equivalent (e/o2) in chickens during the hatching process. IP and EP refer, respectively, to the early hatching phases of internal and external pipping. During these phases, the ventilatory equivalent is low because gas exchange is primarily through the chorioallantoic membrane.

[Modified from ref. 305)]


Figure 1.

Body temperature (top) and arterial (or end‐tidal) pressure of CO2 (PCO2) in mammals of different body weight (in log scale). Each symbol is the average value of a different species. Data of Tb are collected from the literature; data of PCO2 are namely from the data compiled in ref. 322.



Figure 2.

Responses of pulmonary ventilation (e) and oxygen consumption (o2) to cold, expressed in percent of the values in warm conditions. Each symbol is the average of literature data pertinent to some avian (open triangles) or mammalian species (open circles). In first approximation, e and o2 increase in proportion, although in the large majority of cases the data points are slightly below the line of identitiy (dashed line), indicating a small tendency for a reduction of the ventilatory equivalent in the cold. Data of birds refer to pigeons [averaged from refs 23,27,47], parrots 54, chuckars 71, and penguins 73. Data of mammals are for deer mouse, marmot, rat, chipmunk, and other small rodents 65,69,70,146,386, bat 72, cat (anesthetized) 148, pig 198, sheep 214, man 192,337, and some marsupials [Tasmanian devil, during nonshivering conditions 339; kowari, at 0‐15°C 171; bandicoot 242; numbat 84; sandhill dunnart 484; chuditch 400; honey possum 83].



Figure 3.

Ventilation (e)‐Oxygen consumption (o2) values in rats during normoxia (open symbols) and hypoxia (filled symbols) in warm (circles, 25°C) and cold conditions (triangles, 10°C). Oblique dashed lines indicate isoventilatory equivalents (e/o2); in brackets are the mean partial pressures of arterial O2 and CO2, respectively. During cold, the ventilatory equivalent may be slightly lower than in warm conditions, with normal blood gases.

[Redrawn from ref. 386].


Figure 4.

Schematic summary of common effects of cold (left portion) and warm exposure (right portion) on some respiratory variables.



Figure 5.

Newborn dogs, 1‐week old, in warm (30°C) and cold (20° C) conditions. In the cold, the thermogenic effort (increased in oxygen consumption, o2) was not sufficient to maintain body temperature (Tb). Alveolar ventilation (a) increased appropriately to maintain arterial PCO2. Hence, the Q10 effect of Tb had no negative impact on the metabolic stimulus on a.

[Reconstructed from the data of ref. 380].


Figure 6.

Oxygen consumption‐ventilation relationship in human subjects during cold exposure at rest (open circles) and during muscle exercise (filled circles). The data points follow a unique relationship, irrespective of the factor raising metabolic rate.

[Redrawn from 337]


Figure 7.

Difference between hypoxic (∼10% inspired O2) and normoxic oxygen consumption (o2), normalized by body weight in newborn (open symbols) and adult mammals (filled symbols). Each symbol refers to a different species, listed in ref. 130,298. Horizontal dashed line indicates no difference between the hypoxic and normoxic o2. The oblique line is the line of identity. In general, the higher the o2 (per unit weight) in normoxia the greater its hypoxic drop.

[Slightly modified from ref. 300]


Figure 8.

Schema of the metabolism‐ventilation relationship in normoxia (any point on the continuous line, Paco2 = k) and hypoxia (dashed oblique line). Any point on the hypoxic line indicates the same degree of hyperventilation (Paco2 = 0.5 k). A greater hyperpnea (or hypoxic ventilatory response, HVR) is required when metabolic rate is high. Hence, at B the HVR, represented by Bhx‐B, is greater than at A, represented by Ahx‐A. The dashed arrows to Ahx′′, Bhx′, and Bhx′′ indicate instances of hypoxic hypometabolism. In these cases, the HVR is less than in the absence of hypoxic hypometabolism and could have a negative value (cases Bhx′′ and Ahx′′), even though the hyperventilation remains the same.



Figure 9.

Data of oxygen consumption (o2), alveolar ventilation (a), body temperature (Tb), and arterial pressure of CO2 (Paco2) in 11‐day‐old dogs exposed to various concentrations of O2, from normoxia (21%) to medium and severe hypoxia, in warm (ambient temperature 30°C) and cold (20°C) conditions. In the cold, o2 is high because of thermogenesis, and it plummets in hypoxia. The a responses vary drastically with temperature, even though the degree of hypoxic hypeventilation (drop in Paco2) is the same. Note that the important decrease in Tb during hypoxia in the cold does not modify the hyperventilation.

[Reconstructed from the original data of ref. 380]


Figure 10.

Oxen in severe heat. e, pulmonary ventilation; a, alveolar ventilation; d, dead space ventilation; Vt, tidal volume; f, breathing frequency. Paco2, arterial pressure of CO2. As hyperthermia progressed, the breathing pattern switched from rapid and shallow to deep and slow, aggravating the hypocapnia.

[From the data published in ref. 167, Table 4)]


Figure 11.

Breath‐by‐breath relationship of end‐tidal pressure of CO2 and pulmoanry ventilation in one human subject at normal (open circles) and elevated (closed circles) body temperature during hyperoxic rebreathing after prior hyperventilation. The arrow indicates the threshold of the response. Elevated temperature did not modify the threshold but increased the slope of the curve above the threshold, or e sensitivity to CO2.

[Redrawn from ref. 20]


Figure 12.

Relationship between the concentration of serum progesterone (in log scale) and arterial PCO2 in women during various phases of the reproductive cycle.

[redrawn from ref. 256)]


Figure 13.

Pharmacologic increase in metabolic rate (in multiples of resting oxygen consumption) with uncouplers of oxidative phosphorylation. Often, large increases in o2 caused no or small degree of hyperventilation. Dashed line, no change in arterial PCO2. Symbols are mean values in dogs (triangles) and rats (squares). Compiled from the data of refs 194,246,247,248,365,390.



Figure 14.

Mean values of oxygen consumption (o2), pulmonary ventilation (e), and ventilatory equivalent (e/o2) in chickens during the hatching process. IP and EP refer, respectively, to the early hatching phases of internal and external pipping. During these phases, the ventilatory equivalent is low because gas exchange is primarily through the chorioallantoic membrane.

[Modified from ref. 305)]
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Article Title: Metabolism, Temperature, and Ventilation
 

How to Cite

Jacopo P. Mortola, Michael Maskrey. Metabolism, Temperature, and Ventilation. Compr Physiol 2011, 1: 1679-1709. doi: 10.1002/cphy.c100008