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The Buteyko method emphasizes the importance of [[nasal breathing]], which protects the airways by humidifying, warming, and cleaning the air entering the lungs. In addition, breathing through the nose helps the body to maintain higher concentrations of carbon dioxide and nitric oxide in the lungs.<ref name=tanaka> Tanaka Y, Morikawa T, Honda Y, An assessment of nasal functions in control of breathing, J Appl Physiol 1988 Oct; 65(4): 1520-1524.</ref><ref name=dillon> Dillon WC, Hampl V, Shultz PJ, Rubins JB, Archer SL, Origins of breath nitric oxide in humans, Chest. 1996 Oct;110(4): p.930-938.</ref>
The Buteyko method emphasizes the importance of [[nasal breathing]], which protects the airways by humidifying, warming, and cleaning the air entering the lungs. In addition, breathing through the nose helps the body to maintain higher concentrations of carbon dioxide and nitric oxide in the lungs.<ref name=tanaka> Tanaka Y, Morikawa T, Honda Y, An assessment of nasal functions in control of breathing, J Appl Physiol 1988 Oct; 65(4): 1520-1524.</ref><ref name=dillon> Dillon WC, Hampl V, Shultz PJ, Rubins JB, Archer SL, Origins of breath nitric oxide in humans, Chest. 1996 Oct;110(4): p.930-938.</ref>


A majority of asthmatics have problems sleeping at night, and this is thought to be linked with poor posture or unconscious mouth-breathing. By keeping the nose clear and encouraging nasal breathing during the day, night-time symptoms can also improve. Other methods of encouraging nasal breathing are full-face [[CPAP]] machines - commonly used to treat [[sleep apnoea]] - or using a jaw-strap or paper-tape to keep the mouth closed during the night. However, a study in 2009 showed that nasal breathing alone was not enough to cause an improvement in asthma symptoms.<ref name=cooper2>Cooper S, Oborne J, Harrison T, Tattersfield A. Effect of mouth taping at night on asthma control--a randomised single-blind crossover study. '' Respir Med.'' 2009;103:813 PMID 19285849.</ref>
A majority of asthmatics have problems sleeping at night, and this is thought to be linked with poor posture or unconscious mouth-breathing. By keeping the nose clear and encouraging nasal breathing during the day, night-time symptoms can also improve. Other methods of encouraging nasal breathing are full-face [[CPAP]] machines - commonly used to treat [[sleep apnea]] - or using a jaw-strap or paper-tape to keep the mouth closed during the night. However, a study in 2009 showed that nasal breathing alone was not enough to cause an improvement in asthma symptoms.<ref name=cooper2>Cooper S, Oborne J, Harrison T, Tattersfield A. Effect of mouth taping at night on asthma control--a randomised single-blind crossover study. '' Respir Med.'' 2009;103:813 PMID 19285849.</ref>


Strictly nasal breathing during physical exercise is another key element of the Buteyko method. A study in 2008 found that it made exercise safer for asthmatics.<ref name=hallani> Hallani M, Wheatley JR, Amis TC, Enforced mouth breathing decreases lung function in mild asthmatics, Respirology. 2008 Jun;13(4): p.553-558.</ref> While breathing through the nose-only, asthmatics could attain a work intensity great enough to produce an aerobic training effect (based on heart rate and percentage of VO2 max).<ref name=morton> Morton AR, King K, Papalia S, Goodman C, Turley KR, Wilmore JH, Comparison of maximal oxygen consumption with oral and nasal breathing, Aust J Sci Med Sport 1995 Sep; 27(3): 51-55.</ref>
Strictly nasal breathing during physical exercise is another key element of the Buteyko method. A study in 2008 found that it made exercise safer for asthmatics.<ref name=hallani> Hallani M, Wheatley JR, Amis TC, Enforced mouth breathing decreases lung function in mild asthmatics, Respirology. 2008 Jun;13(4): p.553-558.</ref> While breathing through the nose-only, asthmatics could attain a work intensity great enough to produce an aerobic training effect (based on heart rate and percentage of VO2 max).<ref name=morton> Morton AR, King K, Papalia S, Goodman C, Turley KR, Wilmore JH, Comparison of maximal oxygen consumption with oral and nasal breathing, Aust J Sci Med Sport 1995 Sep; 27(3): 51-55.</ref>

Revision as of 04:39, 10 February 2010

The Buteyko method or Buteyko Breathing Technique is a practice used for the treatment of asthma. The method takes its name from the late Ukrainian doctor Konstantin Pavlovich Buteyko (Ukrainian: Бутейко), who first formulated its principles during the 1960s. The method is a physical therapy and several small clinical trials have shown that it can safely reduce asthma symptoms and the need for rescue medication, as well as increasing quality of life scores.[1][2][3] However, improvement takes time and commitment, requiring daily exercises over a period of weeks or months.

At the core of the Buteyko method is a series of breathing exercises that focus on nasal-breathing, breath-holding and relaxation. Buteyko's theory was that asthmatics "chronically overbreathe" and the exercises are designed to teach asthmatics to breathe less. The goal is to retrain breathing to a normal pattern, akin to certain forms of Yoga.

The British Guideline on the Management of Asthma 2008[4] grants permission for health professionals in the United Kingdom to recommend Buteyko, stating that the method "may be considered to help patients control the symptoms of asthma". The guideline also grades clinical research on Buteyko with a 'B' classification - indicating that high quality supporting clinical trials are available. No other complementary therapy has been endorsed by this body for the treatment of asthma.

The Method

Although variations exist among teachers of the technique in different countries, the three core principles of Buteyko remain the same: Reduced breathing, nasal breathing and relaxation.

Reduced Breathing Exercises

The core Buteyko exercises involve breath control; consciously reducing either breathing rate or breathing volume. Many teachers refer to Buteyko as 'breathing retraining' and compare the method to learning to ride a bicycle. Once time has been spent practicing, the techniques become instinctive and the exercises are gradually phased out as the condition improves. A common theme in Buteyko exercise is to hold one's breath until it is uncomfortable - producing a feeling of air hunger. This feeling mimics the feeling of breathlessness that asthmatics typically experience during an asthma attack.

Rather than using traditional peak flow measurements to monitor the condition of asthmatics, Buteyko uses an exercise called the Control Pause (CP), defined as the amount of time that an individual can comfortably hold breath after a normal exhalation. With regular Buteyko reduced-breathing practice, asthmatics tend to find that their CP gradually increases and in parallel their asthma symptoms decrease.

Nasal Breathing

The Buteyko method emphasizes the importance of nasal breathing, which protects the airways by humidifying, warming, and cleaning the air entering the lungs. In addition, breathing through the nose helps the body to maintain higher concentrations of carbon dioxide and nitric oxide in the lungs.[5][6]

A majority of asthmatics have problems sleeping at night, and this is thought to be linked with poor posture or unconscious mouth-breathing. By keeping the nose clear and encouraging nasal breathing during the day, night-time symptoms can also improve. Other methods of encouraging nasal breathing are full-face CPAP machines - commonly used to treat sleep apnea - or using a jaw-strap or paper-tape to keep the mouth closed during the night. However, a study in 2009 showed that nasal breathing alone was not enough to cause an improvement in asthma symptoms.[7]

Strictly nasal breathing during physical exercise is another key element of the Buteyko method. A study in 2008 found that it made exercise safer for asthmatics.[8] While breathing through the nose-only, asthmatics could attain a work intensity great enough to produce an aerobic training effect (based on heart rate and percentage of VO2 max).[9]

Relaxation

Dealing with asthma attacks is an important factor of Buteyko practice. The first feeling of an asthma attack is unsettling and can result in a short period of rapid breathing. By controlling this initial over-breathing phase, asthmatics can prevent a "vicious circle of over-breathing" from developing and spiraling into an asthma attack. This means that asthma attacks may be averted simply by breathing less.

Teachers note that the method is not a substitute for medical treatment and reliever medication should be kept handy at all times and used as required. Reduction of medication should be done under supervision of the doctor prescribing the medication, as some steroids and other drugs should not be ceased too quickly. This aspect of Buteyko is merely a change in lifestyle that can minimize the chance of an attack occurring and reduce the severity by remaining calm and in control of breathing.

Clinical Studies

Between 1962 and 1982, thirty five studies were undertaken in Russia that established Buteyko as a safe and effective treatment for asthma and other breathing disorders.[10] In the West, there have been six published randomised control trials of the Buteyko method since 1999.[1][2][11][12][13][14] All of these trials have shown either significant reductions in the need for medication or improvements in asthma control using the Buteyko method.

The most recent trial, conducted in Canada in 2008, took 129 patients with asthma and randomised them to receive a set of breathing exercises from either a Buteyko practitioner or a chest physiotherapist.[14] In the Buteyko group the proportion of patients achieving good control of their asthma increased from 40% at baseline to 79% at 6 months. This improvement was associated with a statistically significant reduction in the average dose of inhaled steroid. Improvements in asthma control were also seen in the group treated with chest physiotherapy.

A common thread among the trials[2][13] is a large reduction (commonly 80-90%) in reliever medication use. A reduction in steroid medication has been observed, but often over a longer time period. The Buteyko method has not been shown to improve lung function (or peak-flow), the conventional measurement of asthma, which measures the current level of constriction in the airways. Authors have noted that lung function does not decrease in these trials, despite the reduction in reliever and preventer medication.[11]

Some of the earliest Buteyko trials suffered from poor administration that could skew results. However, subsequent trials have taken into account these issues and replicated similar results under strictly controlled conditions.[1]

Theory

Chronic Hyperventilation Syndrome has been discussed in the medical literature for most of the last century. In fact, DaCosta is thought to have been the first to describe some of the symptoms in 1871, following a bizarre symptoms complex (including chronic fatigue) he found in soldiers during the American Civil War.[15] However, he did not associate these symptoms with over-breathing at that time. It was Goldman who discovered in 1922 that all of the symptoms, listed by DaCosta, were associated with involuntary hyperventilation.

In spite of the long history and many pages that have been written on the condition, chronic hyperventilation is rarely diagnosed by doctors.[16][17][18] Chronic hyperventilation develops from any chronic stress on the body[citation needed] leading to a depletion of carbon dioxide (CO2) and bicarbonate (HCO3-).[10][18] The respiratory center, situated in the brain stem, paces breathing in order to maintain pH according to the Henderson-Hasselbach equation:[19]

Hence, to maintain pH, the ratio of CO2 to bicarbonate in the cerebro-spinal fluid (CSF) needs to remain constant. Since the blood-brain barrier is extremely permeable to CO2, this is readily accomplished by regulation of breathing.[19] If the body is stressed, breathing increases, CO2 is reduced and a state of alkalosis develops. If this stress is sustained, the kidneys compensate by dumping bicarbonate in order to reestablish normal pH in the blood.[19][18]. However, the blood-brain barrier is only very slightly permeable to bicarbonate resulting in a very slow diffusion of bicarbonate from the CSF into the blood[19] if the stress is sustained for a very long time (chronic stress). When the stress eventually dissipates, the CSF is left with a low bicarbonate concentration.[19][18] To maintain pH the CO2 will also have to be kept low and a habituation to low CO2 will have taken place.[10] The resulting low CO2 and bicarbonate results in a profound derangement of normal body chemistry.[20][10][18][17][16]

The late consultant chest physician Claude Lum, said that chronic hyperventilation “presents a collection of bizarre and often apparently unrelated symptoms which may affect any part of the body, and any organ or any system ... for we are dealing with a profound biochemical disturbance, which is as real as hypoglycemia, and more far-reaching in its effects.”[18] From the Buteyko perspective, the inflammatory hyperresponsiveness and allergic hyper reactivity seen in asthma and bronchitis are the results of immune disturbances caused by chronic hyperventilation because of these biochemical derangements.[10]

The second component of asthma, bronchospasm, is easier to understand from a teleological perspective. There is clearly a reason for the existence of the smooth muscle in the walls of the bronchioles. Their role is to optimize ventilation of the lungs so that over ventilated airways (low CO2) can be constricted and under ventilated airways can be dilated. Carbon dioxide is a known muscle relaxant. One of the well known symptoms in acute hyperventilation is carpopedal spasm, a condition in which the skeletal muscles of fingers and toes go into spasm. Smooth muscle in the walls of some arteries and bronchioles is affected too, by low carbon dioxide. The smooth muscle in the blood vessels going to the brain contract during hyperventilation eventually leading to fainting. Blood flow to the brain is reduced by 2% for every 1mm Hg reduction in arterial CO2 tension.[16][21]

The mechanism behind smooth muscle spasm is thought to be as follows: Carbon dioxide is involved in the transport of Calcium across the cell walls. During hyperventilation calcium is re-distributed through the tissues, depleting the extra-cellular fluid and accumulating inside the cells. Thus trapped, it is unable to participate in the process of relaxing the smooth muscle, which then remains in spasm.[22] In people with a genetic predisposition to asthma, over breathing is known to cause bronchospasm.[23][20][24][18][16] In fact, in asthmatics even a single deep breath of the kind taken for performing lung function tests, airway resistance is increased by 71% while arterial carbon dioxide tension is reduced by 7 to 16mmHg.[25]

It follows that PEF and FEV1 lung function tests are not appropriate tests for testing asthmatics, because the testing procedure alters the quantity being measured.

There are many other effects of hyperventilation on the body. One of the most significant is poor oxygenation of the cells. Apart from constriction of blood vessels causing a reduction in blood flow, low CO2 increases the affinity of hemoglobin for oxygen. This is know as the Bohr effect, and results in the hemoglobin not offloading its oxygen where it is needed, [23][20][16][17] returning back to the lungs on a wasted trip. This is the cause of breathlessness and leads to more breathing, aggravating an already serious situation.

The Buteyko method is a simple educational program aimed at reversing chronic hyperventilation. In the same way as chronic stress leads to chronic hyperventilation, so too a deliberate reduction in breathing over a period of time reverses this process to restore CO2 back to a normal level.

Prevalence of hyperventilation in chronic disorders

Minute ventilation or respiratory minute volume is the volume of air which is inhaled (inhaled minute volume) or exhaled (exhaled minute volume) from a person's lungs in one minute. Medical respiratory data (see the table below) suggest that sick people breathe about 2-3 times more air at rest than the medical norm.

Condition Minute ventilation (± standard deviation) Number of patients Reference
Normal breathing 6 l/min None Medical textbooks: [26] [27] [28] [29]
Asthma 12 l/min 101 [30]
Asthma 15 l/min 8 [31]
Asthma 14.1 (±5.7) l/min 39 [32]
Heart disease 14 (±4) l/min 88 [33]
Heart disease 12.2 (±3.3) l/min 132 [34]
Heart disease 16 (±2) l/min 11 [35]
Heart disease 15 (±4) l/min 22 [36]
Diabetes 10-20 l/min 28 [37]
Diabetes 12-17 l/min 26 [38]
Cystic fibrosis 11-14 l/min 6 [39]
Cystic fibrosis 13 (±1.8) l/min 10 [40]
COPD 12.2 (±1.9) l/min 10 [41]
Liver cirrhosis 11-18 l/min 24 [42]
Hyperthyroidism 14.9 (±0.6) l/min 42 [43]
Epilepsy 12.8 l/min 12 [44]

There are many more medical studies that found 100% prevalence of chronic hyperventilation in patients with various chronic diseases (see respiratory data from www.normalbreathing.com).

References

  • Brashear R (1983). "Hyperventilation syndrome". Lung. 161 (5): 257–73. doi:10.1007/BF02713872. PMID 6138480.
  • DaCosta JM (1871). "On irritable heart: a clinical study of a form of functional cardiac disorder and its consequences". Am J Med Sci. 61: 17–53.
    for discussion on DaCosta's contribution, see: Jacob Mendez Da Costa doctor/2452 at Who Named It? and Da Costa's syndrome synd/2882 at Who Named It? as well as Wooley C (1982). "Jacob Mendez DaCosta: medical teacher, clinician, and clinical investigator". Am J Cardiol. 50 (5): 1145–8. doi:10.1016/0002-9149(82)90434-9. PMID 6753556.
  • Donnelly P (1991). "Exercise induced asthma: the protective role of CO2 during swimming". Lancet. 337 (8734): 179–80. doi:10.1016/0140-6736(91)90848-J. PMID 1670821. {{cite journal}}: Unknown parameter |month= ignored (help)
  • Morgan W (1983). "Hyperventilation syndrome: a review". Am Ind Hyg Assoc J. 44 (9): 685–9. PMID 6356858.
  • Neill W, Hattenhauer M (1975). "Impairment of myocardial O2 supply due to hyperventilation". Circulation. 52 (5): 854–8. PMID 1175266.
  • Pfeffer J (1984). "Hyperventilation and the hyperventilation syndrome". Postgrad Med J. 60 Suppl 2: 12–5. PMID 6431401.
  • Pfeffer J (1978). "The aetiology of the hyperventilation syndrome. A review of the literature". Psychother Psychosom. 30 (1): 47–55. doi:10.1159/000116639. PMID 358247.
  • Wheatley C (1975). "Hyperventilation syndrome: a frequent cause of chest pain". Chest. 68 (2): 195–9. doi:10.1378/chest.68.2.195. PMID 1149547.

Notes

  1. ^ a b c McHugh P, Aitcheson F, Duncan B, Houghton F. Buteyko Breathing Technique for asthma: an effective intervention. NZ Med J. 2003;116:1187 PMID 14752538. Free full text
  2. ^ a b c Bowler SD, Green A, Mitchell CA. Buteyko breathing techniques in asthma: a blinded randomised controlled trial. Med J Aust. 1998;169(11-12):575-8. PMID 9887897. Free full text
  3. ^ McHugh P, Duncan B, Houghton F. Buteyko breathing technique and asthma in children: a case series. NZ Med J. 2006;119:1234 PMID 16718299. Free full text
  4. ^ British Thoracic Society & Scottish Intercollegiate Guidelines Network (SIGN). British Guideline on the Management of Asthma. Guideline No. 101. Edinburgh:SIGN; 2008. (HTML, Full PDF, Summary PDF)
  5. ^ Tanaka Y, Morikawa T, Honda Y, An assessment of nasal functions in control of breathing, J Appl Physiol 1988 Oct; 65(4): 1520-1524.
  6. ^ Dillon WC, Hampl V, Shultz PJ, Rubins JB, Archer SL, Origins of breath nitric oxide in humans, Chest. 1996 Oct;110(4): p.930-938.
  7. ^ Cooper S, Oborne J, Harrison T, Tattersfield A. Effect of mouth taping at night on asthma control--a randomised single-blind crossover study. Respir Med. 2009;103:813 PMID 19285849.
  8. ^ Hallani M, Wheatley JR, Amis TC, Enforced mouth breathing decreases lung function in mild asthmatics, Respirology. 2008 Jun;13(4): p.553-558.
  9. ^ Morton AR, King K, Papalia S, Goodman C, Turley KR, Wilmore JH, Comparison of maximal oxygen consumption with oral and nasal breathing, Aust J Sci Med Sport 1995 Sep; 27(3): 51-55.
  10. ^ a b c d e Kazarinov VA (1990). "[The biochemical basis of KP Buteyko's theory of the diseases of deep respiration]". In Ed. Buteyko KP (ed.). [Buteyko Method: The experience of implementation in medical practice]. Moscow: Patriot Press. pp. 198–218. {{cite book}}: |format= requires |url= (help); External link in |chapterurl= (help); Unknown parameter |chapterurl= ignored (|chapter-url= suggested) (help)
  11. ^ a b Cooper, S; Oborne, J; Newton, S; Harrison, V; Thompson Coon, J; Lewis, S; Tattersfield, A. Effect of two breathing exercises (Buteyko and pranayama) in asthma: a randomised controlled trial. Thorax 2003;58:674 PMID 12885982. Abstract
  12. ^ A J Opat , M M Cohen , M J Bailey and M J Abramson. A Clinical Trial of the Buteyko Breathing Technique in Asthma as Taught by a Video. Journal of Asthma. 2000;37:557. PMID 11059522. Free full text
  13. ^ a b Slader C, Redde H, Spencer L, Belousova E, Armour C, Bosnic-Anticevich S, Thien F, Jenkins C. Double blind randomised controlled trial of two different breathing techniques in the management of asthma. Thorax 2006;61:651 PMID 16517572. Free full text
  14. ^ a b Cowie RL, Conley DP, Underwood MF, Reader PG. A randomised controlled trial of the Buteyko technique as an adjunct to conventional management of asthma. Respir Med. 2008;102:726 PMID 18249107.
  15. ^ Magarian GJ. Hyperventilation syndromes: infrequently recognized common expressions of anxiety and stress. Medicine. 1982;61(4):219-36. PMID 7045570.
  16. ^ a b c d e Sher TH. Recurrent chest tightness in a 28-year-old woman. Ann Allergy. 1991;67(3):310-4. PMID 1897807.
  17. ^ a b c Magarian GJ. Hyperventilation syndrome: a diagnosis begging for recognition. West J Med. 1983;138(5):733-6. PMID 6880192. Free full text
  18. ^ a b c d e f g Lum LC. Hyperventilation: the tip and the iceberg. J Psychosom Res. 1975;19(5-6):375-83. PMID 1214233. Free full text
  19. ^ a b c d e Guyton, AC (1996). Textbook of medical physiology (9th ed.). New York: WB Saunders. p. 98. ISBN 0721659446.
  20. ^ a b c Demeter SL, Cordasco EM. Hyperventilation syndrome and asthma. Am J Med. 1986;81(6):989-94. PMID 3541595.
  21. ^ Waites TF. Hyperventilation--chronic and acute. Arch Intern Med. 1978;138(11):1700-1. PMID 718322.
  22. ^ Guyton, AC (1996). Textbook of medical physiology (9th ed.). New York: WB Saunders. pp. 527–528. ISBN 0721659446.
  23. ^ a b Cluff RA. Chronic hyperventilation and its treatment by physiotherapy: discussion paper. J R Soc Med. 1984;77(10):855-62. PMID 6387113.
  24. ^ Hibbert GA, Chan M. Respiratory control: its contribution to the treatment of panic attacks. A controlled study. Br J Psychiatry. 1989 Feb;154:232-6. PMID 2673476.
  25. ^ Gayrard P, Orehek J, Grimaud C, CHarpin J. Bronchoconstrictor effects of a deep inspiration in patients with asthma. Am Rev Respir Dis. 1975;111(4):433-9. PMID 123713.
  26. ^ Ganong WF, Review of medical physiology, 15-th ed., 1995, Prentice Hall Int., London.
  27. ^ Guyton AC, Physiology of the human body, 6-th ed., 1984, Suanders College Publ., Philadelphia.
  28. ^ McArdle W.D., Katch F.I., Katch V.L., Essentials of exercise physiology (2-nd edition); Lippincott, Williams and Wilkins, London 2000.
  29. ^ Straub NC, Section V, The Respiratory System, in Physiology, eds. RM Berne & MN Levy, 4-th edition, Mosby, St. Louis, 1998.
  30. ^ McFadden ER & Lyons HA, Arterial-blood gases in asthma, The New Engl J of Med 1968 May 9, 278 (19): 1027-1032.
  31. ^ Johnson BD, Scanlon PD, Beck KC, Regulation of ventilatory capacity during exercise in asthmatics, J Appl Physiol. 1995 Sep; 79(3): 892-901.
  32. ^ Bowler SD, Green A, Mitchell CA, Buteyko breathing techniques in asthma: a blinded randomised controlled trial, Med J of Australia 1998; 169: 575-578.
  33. ^ Clark AL, Chua TP, Coats AJ, Anatomical dead space, ventilatory pattern, and exercise capacity in chronic heart failure, Br Heart J 1995 Oct; 74(4): 377-380.
  34. ^ Fanfulla F, Mortara , Maestri R, Pinna GD, Bruschi C, Cobelli F, Rampulla C, The development of hyperventilation in patients with chronic heart failure and Cheyne-Stokes respiration, Chest 1998; 114; p. 1083-1090.
  35. ^ Johnson BD, Beck KC, Olson LJ, O'Malley KA, Allison TG, Squires RW, Gau GT, Ventilatory constraints during exercise in patients with chronic heart failure, Chest 2000 Feb; 117(2): 321-332.
  36. ^ Dimopoulou I, Tsintzas OK, Alivizatos PA, Tzelepis GE, Pattern of breathing during progressive exercise in chronic heart failure, Int J Cardiol. 2001 Dec; 81(2-3): 117-121.
  37. ^ Tantucci C, Scionti L, Bottini P, Dottorini ML, Puxeddu E, Casucci G, Sorbini CA, Influence of autonomic neuropathy of different severities on the hypercapnic drive to breathing in diabetic patients, Chest. 1997 Jul; 112(1): 145-153.
  38. ^ Bottini P, Dottorini ML, M. Cordoni MC, Casucci G, Tantucci C, Sleep-disordered breathing in nonobese diabetic subjects with autonomic neuropathy, Eur Respir J 2003; 22: p. 654–660.
  39. ^ Tepper RS, Skatrud B, Dempsey JA, Ventilation and oxygenation changes during sleep in cystic fibrosis, Chest 1983; 84; p. 388-393.
  40. ^ Bell SC, Saunders MJ, Elborn JS, Shale DJ, Resting energy expenditure and oxygen cost of breathing in patients with cystic fibrosis, Thorax 1996 Feb; 51(2): 126-131.
  41. ^ Sinderby C, Spahija J, Beck J, Kaminski D, Yan S, Comtois N, Sliwinski P, Diaphragm activation during exercise in chronic obstructive pulmonary disease, Am J Respir Crit Care Med 2001 Jun; 163(7): 1637-1641.
  42. ^ Epstein SK, Zilberberg MD; Facoby C, Ciubotaru RL, Kaplan LM, Response to symptom-limited exercise in patients with the hepatopulmonary syndrome, Chest 1998; 114; p. 736-741.
  43. ^ Kahaly GJ, Nieswandt J, Wagner S, Schlegel J, Mohr-Kahaly S, Hommel G, Ineffective cardiorespiratory function in hyperthyroidism, J Clin Endocrinol Metab 1998 Nov; 83(11): 4075-4078.
  44. ^ Esquivel E, Chaussain M, Plouin P, Ponsot G, Arthuis M, Physical exercise and voluntary hyperventilation in childhood absence epilepsy, Electroencephalogr Clin Neurophysiol 1991 Aug; 79(2): 127-132.
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