nach oben

European Journal of Applied Physiology

Erschienen in:

01.03.2004 | Review Article

Breathing around the clock: an overview of the circadian pattern of respiration

verfasst von: Jacopo P. Mortola

Erschienen in: European Journal of Applied Physiology | Ausgabe 2-3/2004

Einloggen, um Zugang zu erhalten

Abstract

This article reviews human and animal studies about the circadian patterns of physiological variables involved with the respiratory function. Some measures reflecting the mechanical properties of the lungs, such as functional residual capacity, forced expiratory volumes and airway resistance, change periodically with the time of the day. Also resting pulmonary ventilation (V̇ _E), tidal volume, and breathing rate follow circadian patterns. In humans, these patterns occur independently of the daily changes in activity, whereas, to some extent, they are linked to changes in the state of arousal. Differently, in some rodents, the circadian oscillations of the breathing pattern occur independently of the daily rhythms of either activity or state of arousal. Recent measurements of the breathing pattern for unlimited periods of time in undisturbed animals have indicated that the circadian changes occur in close temporal phase with those of oxygen consumption, carbon dioxide production, and body temperature. However, none of these variables can fully explain the circadian pattern of breathing, the origin of which remains unclear. Both in humans and in rats the V̇ _E responses to hypercapnia or hypoxia differ at various times of the day. In rats, the daily differences in V̇ _E responses are buffered by changes in metabolic rate, such that, unlike humans, the hyperventilation (defined as the increase in ventilation–metabolism ratio) remains constant throughout the 24 h. The presence of a biological clock is a major advantage in the adaptation to the environment, although it forces some variables to deviate periodically from their mean value. In humans, these deviations become apparent in conditions of hypoxia. Hence, a daily time-window exists in which the respiratory system is less capable of responding to challenges, a factor which may contribute to the findings that some cardio-respiratory symptoms and diseases peak at particular times of the day.

In humans, sleep usually occurs in one time-block of many hours. In many species, however, sleep occurs in bouts alternating with wakefulness throughout the whole 24 h (Meddis 1975)

The exception is at the equator, where L:D is 12:12 in any day of the year

The first recorded observations of an endogenous clock were presented about three centuries ago by the French astronomer Mairan who noticed that the daily L–D-dependent movements of leaflets and the opening and closure of flowers persisted even after the plant was placed in a closet and shielded from the external time cues

From the term circadian, from the Latin circa diem or about 1 day

Usually, arterial and alveolar values of PCO₂ are almost identical, and P _ACO₂ = (V̇CO₂/V̇ _A)·barometric pressure

The barometric technique basically consists in recording the change in ambient pressure generated by the breathing act of a subject or animal enclosed in a sealed chamber. In fact, during the inspiratory phase of the cycle, the inspired air is warmed and humidified from the ambient to the lung values, raising the chamber pressure. The opposite occurs in expiration. The historical development of this technique, and a review of its potential sources of errors, are presented in Mortola and Frappell (1998)

Allada R, Emery P, Takahashi JS, Rosbash M (2001) Stopping time: the genetics of fly and mouse circadian clocks. Ann Rev Neurosci 24:1091–1119CrossRefPubMed

Anholm JD, Powles ACP, Downey R III, Houston CS, Sutton JR, Bonnet MH, Cymerman A (1992) Operation Everest II: arterial oxygen saturation and sleep at extreme simulated altitude. Am Rev Respir Dis 145:817–826PubMed

Aschoff J, Pohl H (1970) Rhythmic variations in energy metabolism Fed Proc 29:1541–1552

Ashkenazi IE, Ribak J, Avgar DM, Klepfish A (1982) Altitude and hypoxia as phase shift inducers. Aviat Space Environ Med 53:342–346PubMed

Ballard RD, Saathoff MC, Patel DK, Kelly PL, Martin RJ (1989) Effect of sleep on nocturnal bronchoconstriction and ventilatory patterns in asthmatics. J Appl Physiol 67:243–249PubMed

Barnes PJ (1987) Circadian rhythms and airway function. Bull Eur Physiopathol Respir 23:532PubMed

Bishop B, Silva G, Krasney J, Salloum A, Roberts A, Nakano H, Shucard D, Rifkin D, Farkas G (2000) Circadian rhythms of body temperature and activity levels during 63 h of hypoxia in the rat. Am J Physiol 279: R1378–R1385

Bishop B, Silva G, Krasney J, Nakano H, Roberts A, Farkas G, Rifkin D, Shucard D (2001) Ambient temperature modulates hypoxic-induced changes in rat body temperature and activity differentially. Am J Physiol 280: R1190–R1196

Bonnet R, Jörres R, Heitmann U, Magnussen H (1991) Circadian rhythm in airway responsiveness and airway tone in patients with mild asthma. J Appl Physiol 71:1598–1605PubMed

Bosco G, Ionadi A, Panico S, Faralli F, Gagliardi R, Data P, Mortola JP (2003) Effects of hypoxia on the circadian patterns in men. High Alt Med Biol 4:305–318

Bovbjerg DH (2003) Circadian disruption and cancer: sleep and immune regulation. Brain Behav Immun 17: S48–S50CrossRefPubMed

Bülow K (1963) Respiration and wakefulness in man. Acta Physiol Scand 59 [Suppl 209]: 1–98

Casale R, Natali G, Colantonio D, Pasqualetti P (1992) Circadian rhythm of peak expiratory flow in children passively exposed and not exposed to cigarette smoke. Thorax 47:801–803PubMed

Cinkotai FF, Thomson ML (1966) Diurnal variation in pulmonary diffusing capacity for carbon monoxide. J Appl Physiol 21:539–542PubMed

Clark TJH, Hetzel MR (1977) Diurnal variation of asthma. Br J Dis Chest 71:87–92PubMed

Clayton JD, Kyriacou CP, Reppert SM (2001) Keeping time with the human genome. Nature 409:829–831CrossRefPubMed

Cohen RA, Albers HE (1991) Disruption of human circadian and cognitive regulation following a discrete hypothalamic lesion: a case study. Neurology 41:726–729PubMed

Czeisler CA, Weitzman ED, Moore-Ede MC, Zimmerman JC, Knauer RS (1980) Human sleep: its duration and organization depend on its circadian phase. Science 210:1264–1267PubMed

D’Alonzo GE, Steinijans VW, Keller A (1995) Measurements of morning and evening airflow grossly underestimate the circadian variability of FEV₁ and peak expiratory flow rate in asthma. Am J Resp Crit Care Med 152:1097–1099PubMed

Dempsey JA, Forster HV, Ainsworth DM (1995) Regulation of hyperpnea, hyperventilation, and respiratory muscle recruitment during exercise. In: Dempsey JA, Pack AI (eds) Regulation of breathing, 2nd edn. Marcel Dekker, New York, pp 1065–1134

Dreher D, Koller EA (1990) Circadian rhythms of specific airway conductance and bronchial reactivity to histamine: the effects of parasympathetic blockade. Eur Respir J 3:414–420PubMed

Drorbaugh JE, Fenn WO (1955) A barometric method for measuring ventilation in newborn infants. Pediatrics 16:81–87PubMed

Dupre RK, Romero AM, Wood SC (1988) Thermoregulation and metabolism in hypoxic animals. In: Gonzales NC, Fedde MR (eds) Oxygen transfer from atmosphere to tissues. Plenum, New York, pp 347–351

Fenelon K, Seifert EL, Mortola JP (2000) Hypoxic depression of circadian oscillations in sino-aortic denervated rats. Respir Physiol 122:61–69CrossRefPubMed

Fleetham J, West P, Mezon B, Conway W, Roth T, Kryger M (1982) Sleep, arousal, and oxygen desaturation in chronic obstructive pulmonary disease. The effect of oxygen therapy. Am Rev Respir Dis 126:429–433PubMed

Gaultier C, Reinberg A, Girard F (1977) Circadian rhythms in lung resistance and dynamic lung compliance of healthy children. Effects of two bronchodilators. Respir Physiol 31:169–182CrossRefPubMed

Gaultier C, Reinberg A, Motohashi Y (1988) Circadian rhythm in total pulmonary resistance of asthmatic children. Effects of a beta-agonist agent. Chronobiol Int 5:285–290PubMed

Gautier H (1996) Interactions among metabolic rate, hypoxia, and control of breathing. J Appl Physiol 81:521–527PubMed

Guagnano MT, Angelucci E, Data PG, Marroni A, Menduni P, Salomone N, Vetrini G, Sensi S (1986). Influenza dell’alta quota simulata in camera iperbarica sulla struttura temporale circadiana. Boll Soc It Biol Sper 62:427–434

Hayashi S, Toyoshima H, Miyanishi K, Tanabe N (1992) Circadian variations of sudden death. Jpn J Public Health 39:83–89

Henderson AJW, Carswell F (1989) Circadian rhythm of peak expiratory flow in asthmatic and normal children. Thorax 44:410–414PubMed

Hendricks JC (2003) Invited review: Sleeping flies don’t lie: the use of Drosophila melanogaster to study sleep and circadian rhythms. J Appl Physiol 94:1660–1672PubMed

Hetzel MR (1981) The pulmonary clock (editorial). Thorax 36:481–486PubMed

Hetzel MR, Clark TJH (1979) Does sleep cause nocturnal asthma? Thorax 34:749–754PubMed

Hetzel MR, Clark TJH (1980) Comparison of normal and asthmatic circadian rhythms in peak expiratory flow rates. Thorax 35:732–738PubMed

Hicks JW, Riedesel ML (1983) Diurnal ventilatory patterns in the Garter Snake, Thamnophis elegans. J Comp Physiol 149:503–510

Hsu JY, Stone RA, Logan-Sinclair RB, Worsdell M, Busst CM, Chung KF (1994). Coughing frequency in patients with persistent cough: assessment using a 24 hour ambulatory recorder. Eur Respir J 7:1246–1253PubMed

Jackson FR, Schroeder AJ, Roberts MA, McNeil GP, Kume K, Akten B (2001) Cellular and molecular mechanisms of circadian control in insects. J Insect Physiol 47:833–842

Jarsky TM, Stephenson R (2000) Effects of hypoxia and hypercapnia on circadian rhythms in the golden hamster (Mesocricetus auratus). J Appl Physiol 89:2130–2138PubMed

Kadle R, Folk GE Jr (1983) Importance of circadian rhythms in animal cell cultures. Comp Biochem Physiol A 76: 773–776CrossRefPubMed

Kelmanson IA (1991) Circadian variation of the frequency of sudden infant death syndrome and of sudden death from life-threatening conditions in infants. Chronobiologia 18:181–186PubMed

Kerr HD (1973) Diurnal variation of respiratory function independent of air quality. Experience with an environmentally controlled exposure chamber for human subjects. Arch Environ Health 26:144–152PubMed

Lundblad LKA, Irvin CG, Adler A, Bates JHT (2002) A reevaluation of the validity of unrestrained plethysmography in mice. J Appl Physiol 93:1198–1207PubMed

Marshall J (1977) Diurnal variation in occurrence of strokes. Stroke 8:230–231PubMed

Martin RJ (1993) Nocturnal asthma: circadian rhythms and therapeutic interventions. Am Rev Respir Dis 147: S25–S28PubMed

Martin RJ, Banks-Schlegel S (1998) Chronobiology of asthma. Am J Respir Crit Care Med 158:1002–1007PubMed

Meddis T (1975) On the function of sleep. Anim Behav 23:676–691PubMed

Mills JN (1953) Changes in alveolar carbon dioxide tension by night and during sleep. J Physiol (Lond) 122:66–80

Mills JN, Minors DS, Waterhouse JM (1978) Adaptation to abrupt time shifts on the oscillator(s) controlling human circadian rhythms. J Physiol (Lond) 285:455–470

Mitzner W, Tankersley C (2003) Interpreting Penh in mice. J Appl Physiol 94:828–831PubMed

Moore-Ede MC, Czeisler CA, Richardson GS (1983) Circadian timekeeping in health and disease. Part 2. Clinical implications of circadian rhythmicity. New Engl J Med 309:530–536PubMed

Mortola JP (1996) Ventilatory responses to hypoxia in mammals. In: Haddad GG, Lister G (eds) Tissue oxygen deprivation. From molecular to integrated function. Marcel Dekker, New York, pp 433–477

Mortola JP, Gautier H (1995) Interaction between metabolism and ventilation: Effects of respiratory gases and temperature. In: Dempsey JA, Pack AI (eds) Regulation of breathing, 2nd edn. Marcel Dekker, New York, pp 1011–1064

Mortola JP, Feher C (1998) Hypoxia inhibits cold-induced huddling in rat pups. Respir Physiol 113:213–222CrossRefPubMed

Mortola JP, Frappell PB (1998) On the barometric method for measurements of ventilation, and its use in small animals. Can J Physiol Pharmacol 76:937–944CrossRefPubMed

Mortola JP, Seifert EL (2000) Hypoxic depression of circadian rhythms in adult rats. J Appl Physiol 88:365–368PubMed

Mulcahy D, Purcell H, Fox K (1991) Should we get up in the morning? Observations on circadian variations in cardiac events. Br Heart J 65:299–301PubMed

Muller JE, Stone PH, Turi ZG, Rutherford JD, Czeisler CA, Parker C, Poole WK, Passamani E, Roberts R, Robertson T, Sobel BE, Willerson JT, Braunwald E, MILIS Study Group (1985) Circadian variation in the frequency of onset of myocardial infarction. N Engl J Med 313:1315–1322

Oosterhoff Y, Koëter GH, De Monchy JGR, Postma DS (1993) Circadian variation in airway responsiveness to methacoline, propranolol, and AMP in atopic asthmatic subjects. Am Rev Respir Dis 147:512–517PubMed

Pack AI (1995). Changes in respiratory motor activity during rapid eye movement sleep. In: Dempsey JA, Pack AI (eds) Regulation of breathing, 2nd edn. Marcel Dekker, New York, pp 983–1010

Panda A, McHardy GJR (1980) Diurnal variation in pulmonary diffusing capacity and expiratory volumes. Indian J Physiol Pharmacol 24:112–118PubMed

Pappenheimer JR (1977) Sleep and respiration of rats during hypoxia. J Physiol (Lond) 266:191–207

Peever JH, Stephenson R (1997) Day–night differences in the respiratory response to hypercapnia in awake adult rats. Respir Physiol 109:241–248PubMed

Petty TL (1988) Circadian variations in chronic asthma and chronic obstructive pulmonary disease. Am J Med 85:21–23

Phillipson EA, Bowes G (1986) Control of breathing during sleep. In: Cherniack NS, Widdicombe JG (eds) Handbook of physiology, section 3, The respiratory system, vol. II, Control of breathing, part 2. American Physiological Society, Bethesda, Md., pp 649–689

Poncet L, Pequignot JM, Cottet-Emard JM, Dalmaz Y, Denoroy L (1999) Altered daily rhythms of brain and pituitary indolamines and neuropeptides in long-term hypoxic rats. Am J Physiol 277: R66–R75PubMed

Ralph MR, Foster RG, Davis, FC, Menaker M (1990) Transplanted suprachiasmatic nucleus determines circadian period. Science 247:975–978PubMed

Raschke F, Möller KH, (1989) Untersuchungen zur Tagesrhythmik der Chemosensitivität und daren Beitrag zu nächtlichen Atmungsregulationsstörungen. Pneumologia 43:568–571

Reinberg A, Gervais P (1972) Circadian rhythms in respiratory functions, with special reference to human chronophysiology and chronopharmacology. Bull Physiopathol Respir (Nancy) 8:663–675

Refinetti R (2000) Circadian physiology. CRC, Boca Raton, Fla.

Refinetti R, Menaker M (1992) The circadian rhythm of body temperature. Physiol Behav 51:613–637PubMed

Reppert SM, Weaver DR (2002) Coordination of circadian timing in mammals. Nature 418:935–941CrossRefPubMed

Richalet JP, Rutgers V, Bouchet P, Rymer JC, Kéromès A, Duval-Arnould G, Rathat C (1989) Diurnal variations of acute mountain sickness, colour vision, and plasma cortisol and ACTH at high altitude. Aviat Space Environ Med 60:105–111PubMed

Saiki C, Mortola JP (1995) Hypoxia abolishes the morning-night differences of metabolism and ventilation in 6-day-old rats. Can J Physiol Pharmacol 73:159–164PubMed

Samel A, Vejvoda M, Wittiber K, Wenzel J (1998) Circadian rhythms and activity-rest cycle under different CO₂ concentrations. Aviat Space Environ Med 69:501–505PubMed

Schwartz WJ, Busis NA, Hedley-Whyte ET (1986) A discrete lesion of ventral hypothalamus and optic chiasm that disturbed the daily temperature rhythm. J Neurol 233:1–4PubMed

Seifert EL, Mortola JP (2002a) The circadian pattern of breathing in conscious adult rats. Respir Physiol 129:297–305CrossRefPubMed

Seifert EL, Mortola JP (2002b) Circadian pattern of ventilation during acute and chronic hypercapnia in conscious adult rats. Am J Physiol 282:R244–R251

Seifert EL, Mortola JP (2002c) Circadian pattern of ventilation during prolonged hypoxia in conscious rats. Respir Physiol Neurobiol 133:23–34CrossRefPubMed

Seifert EL, Knowles J, Mortola JP (2000) Continuous circadian measurements of ventilation in behaving adult rats. Respir Physiol 120:179–183PubMed

Shibata H, Horie O, Sugita M (1990) Studies on the deviation of short term FRC measurements with the closed-circuit method and on diurnal variation of FRC. Jpn J Clin Pathol 38:463–467

Sommmer B, Montaño LM, Chávez J, Gustin P, Vargas MH (1998) Guinea pig lung resistance shows circadian rhythmicity not influenced by ozone. Respir Physiol 113:223–229CrossRefPubMed

Spengler CM, Shea SA (2000) Endogenous circadian rhythm of pulmonary function in healthy humans. Am J Respir Crit Care Med 162:1038–1046PubMed

Spengler CM, Czeisler CA, Shea SA (2000) An endogenous circadian rhythm of respiratory control in humans. J Physiol (Lond) 526:683–694

Stadler P, Deegen E (1986) Diurnal variation of dynamic compliance, resistance and viscous work of breathing in normal horses and horses with lung disorders. Equine Vet J 18:171–178PubMed

Štefiková H, Šovciková E, Broniš M (1986) The circadian rhythm of selected parameters of heart rate variability. Physiol Bohemoslov 35:227–232PubMed

Stephenson R, Mohan MR, Duffin J, Jarsky TM (2000) Circadian rhythms in the chemoreflex control of breathing. Am J Physiol 278: R282–R286

Stephenson R, Liao KS, Hamrahi H, Horner RL (2001) Circadian rhythms and sleep have additive effects on respiration in the rat J Physiol (Lond) 536:225–235

Stupfel M, Pletan Y (1983) Respiratory ultradian rhythms of mean and low frequencies: a comparative physiological approach. Chronobiologia 10:283–292PubMed

Troyanov S, Ghezzo H, Cartier A, Malo JL (1994) Comparison of circadian variations using FEV₁ and peak expiratory flow rates among normal and asthmatic subjects. Thorax 49:775–780PubMed

Turner-Warwick M (1988) Epidemiology of nocturnal asthma. Am J Med 85:6–8

Vargas M, Jiménez D, León-Velarde F, Osorio J, Mortola JP (2001) Circadian patterns in men acclimatized to intermittent hypoxia. Respir Physiol 126:233–243CrossRefPubMed

Vogelbaum MA, Menaker M (1992) Temporal chimeras produced by hypothalamic transplants. J Neurosci 12:3619–3627PubMed

Weil JV (1986) Ventilatory control at high altitude. In: Cherniack NS, Widdicombe JG (eds) Handbook of physiology, section 3, The respiratory system, vol. II, Control of breathing, part 2. American Physiological Society, Bethesda, Md., pp 703–727

Woodin M, Stephenson R (1998) Circadian rhythms in diving behavior and ventilatory response to asphyxia in canvasback ducks Am J Physiol 274: R686–R693

Zulley J, Wever R, Aschoff J (1981) The dependence of onset and duration of sleep on the circadian rhythm of rectal temperature. Pflugers Arch 391:314–318PubMed

Titel: Breathing around the clock: an overview of the circadian pattern of respiration
verfasst von: Jacopo P. Mortola
Publikationsdatum: 01.03.2004
Verlag: Springer-Verlag
Erschienen in: European Journal of Applied Physiology / Ausgabe 2-3/2004
Print ISSN: 1439-6319
Elektronische ISSN: 1439-6327
DOI: https://doi.org/10.1007/s00421-003-0978-0

Neu im Fachgebiet Arbeitsmedizin

Elterliches Belastungserleben, Unaufmerksamkeits‑/Hyperaktivitätssymptome und elternberichtete ADHS bei Kindern und Jugendlichen: Ergebnisse aus der KiGGS-Studie

Open Access ADHS Leitthema

Die Aufmerksamkeitsdefizit‑/Hyperaktivitätsstörung (ADHS) ist eine der häufigsten psychischen Störungen im Kindes- und Jugendalter [ 1 ]. In Deutschland beträgt die Prävalenz einer elternberichteten ADHS-Diagnose bei Kindern und Jugendlichen 4,4 % …

Substanzkonsum und Nutzung von sozialen Medien, Computerspielen und Glücksspielen unter Auszubildenden an beruflichen Schulen

Open Access Leitthema

Die Begrenzung von Schäden durch Substanzkonsum und andere abhängige Verhaltensweisen von Jugendlichen und jungen Erwachsenen ist ein wichtiges Anliegen der öffentlichen Gesundheit. Der Übergang von der Adoleszenz zum jungen Erwachsenenalter ist …

Berufsbelastung und Stressbewältigung von weiblichen und männlichen Auszubildenden

Leitthema

In der Öffentlichkeit wird die berufliche Ausbildung oftmals unter ökonomischen Gesichtspunkten diskutiert: Mit den geburtenstarken Jahrgängen gehen erfahrene Fachkräfte in Rente und von nachfolgenden Generationen rücken zu wenige Arbeitskräfte …

Rauschtrinken in der frühen Adoleszenz

COVID-19 Leitthema

Alkohol ist in Deutschland die mit Abstand am häufigsten konsumierte psychoaktive Substanz. Mehr als 2 Drittel aller Erwachsenen im Alter von 18 bis 64 Jahren (70,5 %) hat 2021 in den letzten 30 Tagen Alkohol konsumiert [ 1 ]. Von diesen …

Springer Medizin

Abstract

Bitte loggen Sie sich ein, um Zugang zu diesem Inhalt zu erhalten

Weitere Artikel der Ausgabe 2-3/2004

The accuracy of volume estimates using ultrasound muscle thickness measurements in different muscle groups

Regulation of arterial blood pressure in humans during isometric muscle contraction and lower body negative pressure

Neuromuscular response to sustained low-level muscle activation: within- and between-synergist substitution in the triceps surae muscles

Short-term creatine supplementation does not improve muscle activation or sprint performance in humans

Oxidation of [13C]glucose ingested before and/or during prolonged exercise

Influence of muscle fibre type and pedal rate on the V̇O2-work rate slope during ramp exercise

Neu im Fachgebiet Arbeitsmedizin

Elterliches Belastungserleben, Unaufmerksamkeits‑/Hyperaktivitätssymptome und elternberichtete ADHS bei Kindern und Jugendlichen: Ergebnisse aus der KiGGS-Studie

Substanzkonsum und Nutzung von sozialen Medien, Computerspielen und Glücksspielen unter Auszubildenden an beruflichen Schulen

Berufsbelastung und Stressbewältigung von weiblichen und männlichen Auszubildenden

Rauschtrinken in der frühen Adoleszenz