Original Article
A Mechanism of Central Sleep Apnea in Patients with Heart Failure
N Engl J Med 1999; 341:949-954September 23, 1999
- Abstract
Background
Breathing is controlled by a negative-feedback system in which an increase in the partial pressure of arterial carbon dioxide stimulates breathing and a decrease inhibits it. Although enhanced sensitivity to carbon dioxide helps maintain the partial pressure of arterial carbon dioxide within a narrow range during waking hours, in some persons a large hyperventilatory response during sleep may lower the value below the apneic threshold, thereby resulting in central apnea. I tested the hypothesis that enhanced sensitivity to carbon dioxide contributes to the development of central sleep apnea in some patients with heart failure.
Methods
This prospective study included 20 men who had treated, stable heart failure with left ventricular systolic dysfunction. Ten had central sleep apnea, and 10 did not. The patients underwent polysomnography and studies of their ventilatory response to carbon dioxide.
Results
Patients who met the criteria for central sleep apnea had significantly more episodes of central apnea per hour than those without central sleep apnea (mean [±SD], 35±24 vs. 0.5±1.0 episodes per hour). Those with sleep apnea also had a significantly larger ventilatory response to carbon dioxide than those without central sleep apnea (5.1±3.1 vs. 2.1± 1.0 liters per minute per millimeter of mercury, P=0.007), and there was a significant positive correlation between ventilatory response and the number of episodes of apnea and hypopnea per hour during sleep (r=0.6, P=0.01).
Conclusions
Enhanced sensitivity to carbon dioxide may predispose some patients with heart failure to the development of central sleep apnea.
Media in This Article
Figure 1
The Slopes of the Ventilatory Response to Carbon Dioxide in Patients with and Those without Central Sleep Apnea.Table 1
Characteristics of the Patients with and Those without Central Sleep Apnea.Article Activity
- Article
Normally, the rate and depth of breathing are regulated by a negative-feedback system that maintains the partial pressure of arterial carbon dioxide within a narrow range throughout life. Changes in the partial pressure of carbon dioxide lead to changes in ventilation, so that the greater the sensitivity to carbon dioxide, the greater the ventilatory response.
Among normal persons there is considerable variation in sensitivity to carbon dioxide, which may in part be related to familial (genetic) influences.1-4 In a study of patients with chronic obstructive pulmonary disease, Mountain and associates1 found that diminished sensitivity to carbon dioxide, which presumably preceded the onset of pulmonary disease, increased the risk of chronic hypercapnia in patients with established pulmonary disease. Similarly, Moore et al.5 described a patient with a familial diminution in sensitivity who had respiratory failure.
The results of these studies,1,5 given our understanding of the operation of the negative-feedback system that controls ventilation, suggest that in persons with cardiopulmonary disorders, an increase in carbon dioxide sensitivity minimizes perturbations in the partial pressure of arterial carbon dioxide, thus protecting them against the long-term pathologic consequences of hypercapnia. Although this protective mechanism is advantageous during waking hours, the increased sensitivity can potentially destabilize breathing during sleep.6-9
During sleep, ventilation decreases and the partial pressure of carbon dioxide rises by 3 to 6 mm Hg. If during sleep the partial pressure of carbon dioxide decreases below a certain level, referred to as the apneic threshold, which is close to the waking level, ventilation ceases (a condition called central sleep apnea), and the partial pressure of carbon dioxide is restored to its previous level.
The partial pressure of carbon dioxide may fluctuate during sleep. In persons with increased sensitivity to carbon dioxide, the negative-feedback system that controls breathing elicits a large ventilatory response when the partial pressure of carbon dioxide rises; the consequent hyperventilation, by driving the partial pressure of carbon dioxide below the apneic threshold, results in central apnea. As a result of the apnea, the partial pressure of carbon dioxide rises again, which leads to an increase in ventilation. In this way, cycles of central apnea and hyperventilation recur during sleep.
Although central sleep apnea is a relatively rare condition,10 it is common in patients with heart failure.11-14 In a prospective study of 81 ambulatory patients with treated, stable heart failure due to systolic dysfunction, my colleagues and I found that about 40 percent of the patients had central sleep apnea.14
On the basis of the correlation in normal persons between sensitivity to arterial carbon dioxide during waking hours and ventilatory oscillation during sleep8 and considering the increased sensitivity to carbon dioxide of patients with idiopathic central sleep apnea,15 I tested the hypothesis that enhanced sensitivity to carbon dioxide may contribute to the development of central sleep apnea in patients with heart failure.
Methods
Patients
Twenty patients with heart failure were studied, 10 of whom had central sleep apnea and 10 of whom did not.14 The patients were part of a prospective study designed to determine the prevalence and mechanisms of sleep apnea in heart failure. The details of that study have been published previously.14,16,17 The protocol was approved by the institutional review board of the University of Cincinnati, and written informed consent was obtained from all patients.
All 20 patients underwent polysomnographic studies after a night of adaptation in the sleep laboratory. Within 24 hours before or after the polysomnographic studies, radionuclide ventriculography, pulmonary-function tests, and tests to measure the ventilatory response to carbon dioxide were performed. Samples of venous blood and arterial blood for measurement of electrolytes and arterial-blood gases were obtained in the morning, before the ventilatory response was measured.
Polysomnography
Polysomnography was performed with the use of standard techniques, as described previously.18,19 To determine the stages of sleep, an electroencephalogram (with two channels), chin electromyogram (with one channel), and electro-oculogram (with two channels) were obtained. Thoracoabdominal excursions were measured qualitatively by respiratory inductance plethysmography (Respitrace, Ambulatory Monitoring, Ardsley, N.Y.) or with pneumatic respiration transducers (Grass Instruments, Quincy, Mass.) placed over the rib cage and abdomen. Airflow was monitored qualitatively with an oronasal thermocouple (model TCTIR, Grass Instruments). Arterial-blood oxyhemoglobin saturation was recorded with the use of a pulse oximeter. These variables were recorded on a multichannel polygraph (model 78D, Grass Instruments).
An episode of apnea was defined as the cessation of inspiratory airflow for at least 10 seconds. An episode of obstructive apnea was defined as the absence of airflow in the presence of rib-cage and abdominal excursions. An episode of central apnea was defined as the absence of rib-cage and abdominal excursions and the absence of airflow. Hypopnea was defined as a reduction in airflow lasting 10 seconds or more and associated with at least a 4 percent decrease in arterial oxyhemoglobin saturation, an electroencephalographic arousal,20 or both. The number of episodes of apnea and hypopnea per hour is referred to as the apnea–hypopnea index. The number of episodes of obstructive apnea and hypopnea per hour is referred to as the obstructive apnea–hypopnea index, and the number of episodes of central apnea per hour is referred to as the central-apnea index. The apnea–hypopnea index was used to define the presence or absence of clinically important sleep apnea, as previously described14 (≥15 episodes per hour indicated the presence of apnea, and <15 episodes per hour indicated its absence). In addition, patients with central sleep apnea had to have a central-apnea index of at least five episodes per hour.
The number of episodes of arousal per hour is referred to as the arousal index. The results of all the polysomnographic studies were pooled and scored without knowledge of any laboratory data, including the carbon dioxide ventilatory response.
Studies of Pulmonary Function and Ventilation
Pulmonary-function tests, measurements of maximal inspiratory and expiratory pressures, and arterial-blood gas and pH measurements were performed as described previously.21,22 Measurements of ventilation, oxygen consumption, carbon dioxide production, and the ventilatory response to carbon dioxide (the hypercapnic ventilatory response) were performed in our laboratory as described previously.22-24 In brief, the tests were performed while the patients were sitting, wearing a nose clip, and breathing through a mouthpiece connected to a low-resistance, two-way valve. Measurements were started several minutes after a steady state had been achieved, as evidenced by the finding of a stable end-tidal partial pressure of carbon dioxide. First, minute ventilation, oxygen consumption, and carbon dioxide production were measured.22 The hyperoxic hypercapnic ventilatory response22-24 was determined by Read's rebreathing method.25 Linear regression was used to determine the slope according to the following equation: ventilation = S × (the partial pressure of carbon dioxide–B), where S is the slope of the hypercapnic ventilatory response and B is the intercept (on the x axis, which represents the partial pressure of carbon dioxide) of the line that relates ventilation to the partial pressure of carbon dioxide. The mean (±SD) value for the slope of the ventilatory response to carbon dioxide in 10 normal men in our laboratory was 2.92±0.92 liters per minute per millimeter of mercury (range, 1.02 to 4.1).22
In conducting the tests of ventilatory response, extreme caution was exercised to ensure uniformity in technique. All the tests were performed by one investigator. The patients were not allowed to drink caffeinated products on the morning of the tests. Tests were performed at least two hours after a meal, and the patients were asked to empty their bladders before the tests. The patients were familiarized with the equipment and breathed through the mouthpiece for several minutes before measurement began. An assistant monitored the patients continuously to ensure that they remained awake.
To compare the hypercapnic ventilatory response between patients with and those without central sleep apnea, the slope of the response was adjusted for the patients' body-surface area, oxygen consumption, carbon dioxide production, maximal voluntary ventilation, and forced vital capacity, since these factors affect the ventilatory response.
Characteristics of the Patients
Ten of the patients with heart failure did not meet the criteria for sleep apnea (i.e., they had scores on the apnea–hypopnea index of <15 episodes per hour14). In these patients, the apnea–hypopnea index ranged from 0 to 6.8 episodes per hour, the obstructive apnea–hypopnea index was 0, and the central apnea index ranged from 0 to 3.2 episodes per hour. In the 10 patients with heart failure who did meet the criteria for central sleep apnea, the apnea–hypopnea index ranged from 19.5 to 107.2 episodes per hour, the obstructive apnea–hypopnea index ranged from 0 to 0.8 episode per hour, and the central-apnea index ranged from 6.1 to 79.1 episodes per hour. None of the patients had apneic episodes during waking hours.
The patients in the two groups were matched with respect to the results of their pulmonary-function tests, although some differences did exist. The patients in the two groups were also similar with respect to their medications. Medications included an angiotensin-converting–enzyme inhibitor (in 10 patients without central sleep apnea and 8 patients with central sleep apnea), furosemide (in 8 and 9 patients, respectively), digoxin (in 10 and 9 patients, respectively), and hydralazine (in 1 patient in each group). None of the patients were receiving beta-blockers, morphine derivatives, benzodiazepines, theophylline, or acetazolamide.
Statistical Analysis
The Mann–Whitney test was used to assess differences between patients with and those without central sleep apnea, and chi-square analysis was used to analyze proportions. A two-sided P value of less than 0.05 was considered to indicate statistical significance. Values are reported as means. Spearman rank correlation was used to analyze the apnea–hypopnea index in relation to the unadjusted slope of the ventilatory response to carbon dioxide and the slope adjusted for body-surface area, oxygen consumption, carbon dioxide production, maximal voluntary ventilation, and forced vital capacity. All the calculations were done with InStat software, version 2.03 (GraphPad, San Diego, Calif.).
Results
There were no significant differences between the patients who met the criteria for central sleep apnea and those who did not with respect to demographic characteristics or various laboratory measurements (Table 1Table 1
Characteristics of the Patients with and Those without Central Sleep Apnea.), the results of pulmonary-function tests (except for the percentage of predicted forced expiratory volume in one second) (Table 2Table 2
Results of Pulmonary-Function Tests.), or measurements of ventilation (Table 3Table 3
Assessment of Ventilation.). Table 4Table 4
Characteristics of the Patients during Sleep. lists the characteristics of sleep and disordered breathing events and oxyhemoglobin saturation during sleep in the patients. Among patients with central sleep apnea, the mean central-apnea index was 35±24 episodes per hour. As a result, these patients had arterial oxyhemoglobin desaturation and an excessive number of arousals from sleep (Table 4). However, total sleeping time and the proportion of time spent in each stage of sleep did not differ significantly between these patients and those without central sleep apnea.The unadjusted slope of the ventilatory response to carbon dioxide was significantly greater among patients with heart failure who had central sleep apnea than among those who did not have apnea (Table 3), although there was some overlap in values (Figure 1Figure 1
The Slopes of the Ventilatory Response to Carbon Dioxide in Patients with and Those without Central Sleep Apnea.). This difference remained significant when the ventilatory response was adjusted for body-surface area, forced vital capacity, maximal voluntary ventilation, oxygen consumption, and carbon dioxide production. The ventilatory response to carbon dioxide before and after adjustment for these variables was 2.3 to 3.5 times as great in patients with central sleep apnea as in those without it (Table 3). Furthermore, there were significant correlations between the apnea–hypopnea index and the slope of the ven-tilatory response before adjustment (r=0.6, P=0.01) and after adjustment for forced vital capacity (r=0.6, P=0.008), maximal voluntary ventilation ratio (r=0.6, P=0.005), carbon dioxide production (r=0.6, P= 0.003), and oxygen consumption (r=0.6, P=0.005).Discussion
The principal finding of this study is that patients with heart failure who had central sleep apnea had a significantly greater sensitivity to carbon dioxide (by a factor of 2.3 to 3.5) than patients with heart failure who did not have central sleep apnea, as assessed by the ventilatory response to carbon dioxide. There was also a significant, positive correlation between sensitivity to carbon dioxide and the number of episodes of apnea and hypopnea per hour during sleep.
An enhanced sensitivity to carbon dioxide could destabilize breathing during sleep. During sleep, the partial pressure of carbon dioxide rises and becomes the most potent stimulus of rhythmic breathing.27 If the partial pressure of carbon dioxide decreases below the apneic threshold, breathing ceases. This state of central apnea results in an increase in the partial pressure of carbon dioxide, which in the presence of enhanced sensitivity to carbon dioxide elicits a large hyperventilatory response. This response may in turn lower the partial pressure of carbon dioxide below the apneic threshold. The result is periodic breathing with recurring cycles of apnea and hyperventilation.
In this study, in addition to differences in sensitivity to carbon dioxide between patients with and those without central sleep apnea, there was a significant and positive correlation between sensitivity and the number of episodes of apnea and hypopnea per hour. This finding further emphasizes the potential destabilizing effect of enhanced sensitivity to carbon dioxide on breathing during sleep in patients with heart failure.
The administration of oxygen decreases the number of episodes of central sleep apnea in patients with heart failure.11-13 In a study of patients with heart failure and systolic dysfunction, periodic breathing improved and sensitivity to carbon dioxide decreased significantly after one week of nocturnal administration of supplemental nasal oxygen.28 Although the exact cause-and-effect relation cannot be determined, the results of that study suggest that the decreased sensitivity to carbon dioxide may have contributed to the improvement in periodic breathing during sleep.
Mechanisms underlying the initiation and maintenance of central sleep apnea are complex.29,30 In addition to sensitivity, other factors have been implicated. The finding of a low partial pressure of arterial carbon dioxide during waking hours is highly predictive of central sleep apnea, since the level may drop below the apneic threshold during sleep.31-33 Likewise, a low metabolic rate34 and low functional residual capacity6,7,9 may contribute to periodic breathing during sleep. In the current study, there were no significant differences between groups in the partial pressure of carbon dioxide, oxygen consumption and carbon dioxide production (measures of metabolic rate), or functional residual capacity. Circulation time was not measured; however, a prolonged circulation time may not be a key factor in the genesis of central sleep apnea, but it may be important in determining the length of ventilatory cycles35,36 and in maintaining periodic breathing.36 In experiments in dogs,36 circulation time had to be increased severalfold before spontaneous periodic breathing could occur, and even then, it occurred in a minority of the animals.
In this study there was some overlap in the ventilatory response to carbon dioxide between patients with and those without central sleep apnea (Figure 1), a finding that emphasizes the importance of other mechanisms in the development of central sleep apnea. One critical factor is the apneic threshold during sleep, and whether this threshold differs between patients with heart failure who have central sleep apnea and those who do not have sleep apnea.
It is well known that increased sensitivity of the respiratory system to carbon dioxide or hypoxia may destabilize breathing during sleep. The relative contributions of the peripheral arterial chemoreceptors (the carotid bodies) and of the central chemoreceptors (those within the medulla of the brain stem) to the enhanced sensitivity and the consequent periodic breathing and central sleep apnea remain unclear, although it is generally believed that the central chemoreceptors have the larger role in sensitivity to carbon dioxide. In one study, during periods of natural sleep in unanesthetized dogs, hypocapnia that was confined to the carotid body did not result in central apnea.37 This finding supports the role of the central chemoreceptors in the genesis of central sleep apnea.30,37 However, the sensitivity of the chemoreceptors may further change under conditions of heart failure. The increased sensitivity to carbon dioxide in heart failure appears to be specific to central but not obstructive sleep apnea.38
Both acquired and genetic factors may affect the ventilatory response to carbon dioxide.1-5,37 In the current study, the two groups of patients with heart failure were well matched: differences in sex, age, body-mass index, base-line ventilation, partial pressures of arterial carbon dioxide and oxygen, metabolic rate, respiratory-muscle strength, and pulmonary function, all of which can affect the ventilatory response,39 did not account for the large and significant differences in sensitivity to carbon dioxide between the two groups. In addition, the mean values for arterial blood pressure, heart rate, and left ventricular ejection fraction, as well as the cardiovascular medications, were similar in the two groups. Of the medications they used, only hydralazine is a known respiratory stimulant.40 One patient in each group was receiving hydralazine.
Loss of sleep has been shown to decrease sensitivity to carbon dioxide,41 but in the current study, the mean total sleeping time was similar in the two groups. Sleep was more often interrupted (fragmented) in the patients who had central sleep apnea, but sleep fragmentation in the absence of sleep loss has not been shown to affect sensitivity to carbon dioxide.42
The variation in ventilatory drive that has been noted among randomly selected normal persons is considerably smaller within families, and strong correlations in ventilatory drive among family members have been reported.2,3 The clustering and correlation of ventilatory drive among family members suggest that there are familial (presumably genetic) influences on the chemical control of ventilation. It is therefore conceivable that in my patients, familial enhancement of the ventilatory response to carbon dioxide predisposed them to the development of central sleep apnea after the onset of heart failure. This supposition is consistent with observations in patients with chronic obstructive pulmonary disease, a disorder in which diminished sensitivity to carbon dioxide (of a familial nature) predisposes patients to hypercapnia.1 However, among normal persons, the range of the ventilatory response to carbon dioxide is broad.2 Alternatively, patients with heart failure who have central sleep apnea could have spontaneously increased sensitivity to carbon dioxide, independent of familial or genetic influences.
In summary, in this study, patients with heart failure who had central sleep apnea had enhanced sensitivity to carbon dioxide. In addition, the degree of sensitivity was correlated with the severity of central sleep apnea, a finding that supports the possibility that increased sensitivity has a destabilizing effect on breathing during sleep.
Supported by Merit Review grants from the Department of Veterans Affairs.
I am indebted to Candice R. Brown for technical assistance and to Faye A. Jones for secretarial assistance.
Source Information
From the Pulmonary Service, Veterans Affairs Medical Center, and the Department of Medicine, University of Cincinnati College of Medicine — both in Cincinnati.
Address reprint requests to Dr. Javaheri at the Pulmonary Section (111F), VA Medical Center, 3200 Vine St., Cincinnati, OH 45220, or at javaheri,shahrokh@cincinnati.va.gov.
- References
References
1
Mountain R ,Zwillich C ,Weil J . Hypoventilation in obstructive lung disease: the role of familial factors. N Engl J Med 1978;298:521-525
Full Text | Web of Science | Medline2
Weil JV. Pulmonary hypertension and cor pulmonale in hypoventilating patients. In: Weit EK, Reeves JT, eds. Pulmonary hypertension. Mount Kisco, N.Y.: Futura Publishing, 1984:321-40.
3
Saunders NA ,Leeder SR ,Rebuck AS . Ventilatory response to carbon dioxide in young athletes: a family study. Am Rev Respir Dis 1976;113:497-502
Web of Science | Medline4
Kawakami Y ,Yamamoto H ,Yoshikawa T ,Shida A . Chemical and behavioral control of breathing in adult twins. Am Rev Respir Dis 1984;129:703-707
Web of Science | Medline5
Moore GC ,Zwillich CW ,Battaglia JD ,Cotton EK ,Weil JV . Respiratory failure associated with familial depression of ventilatory response to hypoxia and hypercapnia. N Engl J Med 1976;295:861-865
Full Text | Web of Science | Medline6
Cherniack NS ,Longobardo GS . Cheyne-Stokes breathing: an instability in physiologic control. N Engl J Med 1973;288:952-957
Full Text | Web of Science | Medline7
Cherniack NS . Respiratory dysrhythmias during sleep. N Engl J Med 1981;305:325-330
Full Text | Web of Science | Medline8
Chapman KR ,Bruce EN ,Gothe B ,Cherniack NS . Possible mechanisms of periodic breathing during sleep. J Appl Physiol 1988;64:1000-1008
CrossRef | Web of Science | Medline9
Khoo MCK ,Kronauer RE ,Strohl KP ,Slutsky AS . Factors inducing periodic breathing in humans: a general model. J Appl Physiol 1982;53:644-659
Web of Science | Medline10
White DP. Central sleep apnea. In: Kryger MH, Roth T, Dement WC, eds. Principles and practice of sleep medicine. 2nd ed. Philadelphia: W.B. Saunders, 1994:630-41.
11
Yamashiro Y ,Kryger MH . Sleep in heart failure. Sleep 1993;16:513-523
Web of Science | Medline12
Bradley TD ,Floras JS . Pathophysiologic and therapeutic implications of sleep apnea in congestive heart failure. J Card Fail 1996;2:223-240
CrossRef | Medline13
Javaheri S . Central sleep apnea-hypopnea syndrome in heart failure: prevalence, impact, and treatment. Sleep 1996;19:Suppl:S229-S231
Web of Science | Medline14
Javaheri S ,Parker TJ ,Liming JD , et al. Sleep apnea in 81 ambulatory male patients with stable heart failure: types and their prevalences, consequences, and presentations. Circulation 1998;97:2154-2159
Web of Science | Medline15
Xie A ,Rutherford R ,Rankin F ,Wong B ,Bradley TD . Hypocapnia and increased ventilatory responsiveness in patients with idiopathic central sleep apnea. Am J Respir Crit Care Med 1995;152:1950-1955
Web of Science | Medline16
Javaheri S ,Parker TJ ,Wexler L , et al. Occult sleep-disordered breathing in stable congestive heart failure. Ann Intern Med 1995;122:487-492[Erratum, Ann Intern Med 1995;123:77.]
Web of Science | Medline17
Javaheri S ,Parker TJ ,Wexler L ,Liming JD ,Lindower P ,Roselle GA . Effect of theophylline on sleep-disordered breathing in heart failure. N Engl J Med 1996;335:562-567
Full Text | Web of Science | Medline18
Dowdell WT ,Javaheri S ,McGinnis W . Cheyne-Stokes respiration presenting as sleep apnea syndrome: clinical and polysomnographic features. Am Rev Respir Dis 1990;141:871-879
Web of Science | Medline19
Javaheri S ,Colangelo G ,Lacey W ,Gartside PS . Chronic hypercapnia in obstructive sleep apnea-hypopnea syndrome. Sleep 1994;17:416-423
Web of Science | Medline20
EEG arousals: scoring rules and examples: a preliminary report from the Sleep Disorders Atlas Task Force of the American Sleep Disorders Association
Web of Science21
Javaheri S ,Bosken CH ,Lim SP ,Dohn MN ,Greene NB ,Baughman RP . Effects of hypohydration on lung functions in humans. Am Rev Respir Dis 1987;135:597-599
Web of Science | Medline22
Javaheri S ,Guerra LF . Lung function, hypoxic and hypercapnic ventilatory responses, and respiratory muscle strength in normal subjects taking oral theophylline. Thorax 1990;45:743-747
CrossRef | Web of Science | Medline23
Javaheri S ,Guerra LF . Effects of domperidone and medroxyprogesterone acetate on ventilation in man. Respir Physiol 1990;81:359-370
CrossRef | Medline24
Javaheri S ,Colangelo G ,Corser B ,Zahedpour MR . Familial respiratory chemosensitivity does not predict hypercapnia of patients with sleep apnea-hypopnea syndrome. Am Rev Respir Dis 1992;145:837-840
Web of Science | Medline25
Read DJC . A clinical method for assessing the ventilatory response to carbon dioxide. Australas Ann Med 1967;16:20-32
Medline26
Carskadon MA, Dement WC. Normal human sleep. In: Kryger MH, Roth T, Dement WC, eds. Principles and practice of sleep medicine. 2nd ed. Philadelphia: W.B. Saunders, 1994:16-25.
27
Skatrud JB ,Dempsey JA . Interaction of sleep state and chemical stimuli in sustaining rhythmic ventilation. J Appl Physiol 1983;55:813-822
Web of Science | Medline28
Andreas S ,von zur Muhlen F ,Stevens J ,Kreuzer H . Nocturnal oxygen and hypercapnic ventilatory response in patients with congestive heart failure. Respir Med 1998;92:426-431
CrossRef | Web of Science | Medline29
Khoo MCK. Periodic breathing. In: Crystal RG, West JB, eds. The lung: scientific foundations. Vol. 2. New York: Raven Press, 1991:1419-31.
30
Dempsey JA ,Smith CA ,Harms CA ,Chow CM ,Saupe KW . Sleep-induced breathing instability. Sleep 1996;19:236-247
Web of Science | Medline31
Naughton M ,Benard D ,Tam A ,Rutherford R ,Bradley TD . Role of hyperventilation in the pathogenesis of central sleep apnea in patients with congestive heart failure. Am Rev Respir Dis 1993;148:330-338
Web of Science | Medline32
Hanly P ,Zuberi N ,Gray R . Pathogenesis of Cheyne-Stokes respiration in patients with congestive heart failure: relationship to arterial PCO2. Chest 1993;104:1079-1084
CrossRef | Web of Science | Medline33
Javaheri S ,Corbett WS . Association of low PaCO2 with central sleep apnea and ventricular arrhythmias in ambulatory patients with stable heart failure. Ann Intern Med 1998;128:204-207
Web of Science | Medline34
Cherniack NS, Longobardo GS. Effect of metabolic rate on the occurrence of periodic breathing. In: Issa FG, Suratt PM, Remmers JE, eds. Sleep and respiration. New York: Wiley–Liss, 1990:167-76.
35
Hall MJ ,Xie A ,Rutherford R ,Ando SI ,Floras JS ,Bradley TD . Cycle length of periodic breathing in patients with and without heart failure. Am J Respir Crit Care Med 1996;154:376-381
Web of Science | Medline36
Guyton AC ,Crowell JW ,Moore JW . Basic oscillating mechanism of Cheyne-Stokes breathing. Am J Physiol 1956;187:395-398
Web of Science | Medline37
Smith CA ,Saupe KW ,Henderson KS ,Dempsey JA . Ventilatory effects of specific carotid body hypocapnia in dogs during wakefulness and sleep. J Appl Physiol 1995;79:689-699
Web of Science | Medline38
Wilcox I ,McNamara SG ,Dodd MJ ,Sullivan CE . Ventilatory control in patients with sleep apnoea and left ventricular dysfunction; comparison of obstructive and central sleep apnea. Eur Respir J 1998;11:7-13
CrossRef | Web of Science | Medline39
Kelsen SG. Control of breathing. In: Montenegro HD, ed. Chronic obstructive pulmonary disease. New York: Churchill Livingstone, 1984:65-116.
40
Keller CA ,Shepard JW Jr ,Chun DS ,Dolan GF ,Vasquez P ,Minh VD . Effects of hydralazine on hemodynamics, ventilation, and gas exchange in patients with chronic obstructive pulmonary disease and pulmonary hypertension. Am Rev Respir Dis 1984;130:606-611
Web of Science | Medline41
White DP ,Douglas NJ ,Pickett CK ,Zwillich CW ,Weil JV . Sleep deprivation and the control of ventilation. Am Rev Respir Dis 1983;128:984-986
Web of Science | Medline42
Espinoza H ,Thornton AT ,Sharp D ,Antic R ,McEvoy RD . Sleep fragmentation and ventilatory responsiveness to hypercapnia. Am Rev Respir Dis 1991;144:1121-1124
CrossRef | Web of Science | Medline
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Claudio Passino, Alberto Giannoni, Francesca Mannucci, Concetta Prontera, Franco Filipponi, Paola Carrai, Michele Emdin, Giosuè Catapano. (2010) Abnormal hyperventilation in patients with hepatic cirrhosis: Role of enhanced chemosensitivity to carbon dioxide. International Journal of Cardiology
CrossRef18
Akira Tamura, Shinichi Ando, Yukie Goto, Yoshiyuki Kawano, Kazuhiro Shinozaki, Munenori Kotoku, Junichi Kadota. (2010) Washout Rate of Cardiac Iodine-123 Metaiodobenzylguanidine is High in Chronic Heart Failure Patients With Central Sleep Apnea. Journal of Cardiac Failure 16:9, 728-733
CrossRef19
Resham Baruah, Darrel P. Francis. (2010) Chemoreflex sensitivity and congenital heart disease. International Journal of Cardiology 144:1, 94-95
CrossRef20
Kirk Kee, Scott A. Sands, Bradley A. Edwards, Philip J. Berger, Matthew T. Naughton. (2010) Positive Airway Pressure in Congestive Heart Failure. Sleep Medicine Clinics 5:3, 393-405
CrossRef21
S. Javaheri. (2010) Positive Airway Pressure Treatment of Central Sleep Apnea with Emphasis on Heart Failure, Opioids, and Complex Sleep Apnea. Sleep Medicine Clinics 5:3, 407-417
CrossRef22
Gerrit C. Hagenah, Claus Luers, Denise Prager, Sabine Blaschke. (2010) Association of Cheyne–Stokes respiration and cardiac cachexia in congestive heart failure. International Journal of Cardiology 142:3, 298-300
CrossRef23
Brian B. Koo, Kingman P. Strohl, Carl B. Gillombardo, Frank J. Jacono. (2010) Ventilatory patterning in a mouse model of stroke. Respiratory Physiology & Neurobiology 172:3, 129-135
CrossRef24
S. Javaheri. (2010) Central Sleep Apnea. Clinics in Chest Medicine 31:2, 235-248
CrossRef25
Christian Binggeli, Isabella Sudano, Roberto Corti, Lukas Spieker, Rolf Jenni, Thomas F Lüscher, Georg Noll. (2010) Spontanous periodic breathing is associated with sympathetic hyperreactivity and baroreceptor dysfunction in hypertension. Journal of Hypertension 28:5, 985-992
CrossRef26
Bhavneesh Sharma, Robert Owens, Atul Malhotra. (2010) Sleep in Congestive Heart Failure. Medical Clinics of North America 94:3, 447-464
CrossRef27
Amy M. Fowler, Jonathan J. Dutton. (2010) Floppy Eyelid Syndrome as a Subset of Lax Eyelid Conditions: Relationships and Clinical Relevance (an ASOPRS Thesis). Ophthalmic Plastic & Reconstructive Surgery 26:3, 195-204
CrossRef28
A. Vazir, P.C. Hastings, M.J. Morrell, J. Pepper, M.Y. Henein, S. Westaby, P.A. Poole-Wilson, M.R. Cowie, A.K. Simonds. (2010) Resolution of central sleep apnoea following implantation of a left ventricular assist device. International Journal of Cardiology 138:3, 317-319
CrossRef29
Mahdi Chowdhury, Suzanne Adams, David J. Whellan. (2010) Sleep-Disordered Breathing and Heart Failure: Focus on Obstructive Sleep Apnea and Treatment With Continuous Positive Airway Pressure. Journal of Cardiac Failure 16:2, 164-174
CrossRef30
Laila AlDabal, Ahmed S. BaHammam. (2010) Cheyne-Stokes Respiration in Patients with Heart Failure. Lung 188:1, 5-14
CrossRef31
T. Bitter, D. Horstkotte, O. Oldenburg. (2009) Therapie der Cheyne-Stokes-Atmung bei Herzinsuffizienz. Somnologie - Schlafforschung und Schlafmedizin 13:4, 204-210
CrossRef32
Samuel L. Krachman, Gilbert E. D’Alonzo, Irene Permut, Wissam Chatila. (2009) Treatment of sleep disordered breathing in congestive heart failure. Heart Failure Reviews 14:3, 195-203
CrossRef33
Roberta Poletti, Claudio Passino, Alberto Giannoni, Luc Zyw, Concetta Prontera, Francesca Bramanti, Aldo Clerico, Massimo Piepoli, Michele Emdin. (2009) Risk factors and prognostic value of daytime Cheyne–Stokes respiration in chronic heart failure patients. International Journal of Cardiology 137:1, 47-53
CrossRef34
Olaf Oldenburg, Thomas Bitter, Marcus Wiemer, Christoph Langer, Dieter Horstkotte, Cornelia Piper. (2009) Pulmonary capillary wedge pressure and pulmonary arterial pressure in heart failure patients with sleep-disordered breathing. Sleep Medicine 10:7, 726-730
CrossRef35
T. Bitter, L. Faber, D. Hering, C. Langer, D. Horstkotte, O. Oldenburg. (2009) Sleep-disordered breathing in heart failure with normal left ventricular ejection fraction. European Journal of Heart Failure 11:6, 602-608
CrossRef36
Austin Chin Chwan Ng, Saul Benedict Freedman. (2009) Sleep disordered breathing in chronic heart failure. Heart Failure Reviews 14:2, 89-99
CrossRef37
Alberto Giannoni, Michele Emdin, Francesca Bramanti, Giovanni Iudice, Darrel P. Francis, Antonio Barsotti, Massimo Piepoli, Claudio Passino. (2009) Combined Increased Chemosensitivity to Hypoxia and Hypercapnia as a Prognosticator in Heart Failure. Journal of the American College of Cardiology 53:21, 1975-1980
CrossRef38
Richard S.T. Leung. (2009) Sleep-Disordered Breathing: Autonomic Mechanisms and Arrhythmias. Progress in Cardiovascular Diseases 51:4, 324-338
CrossRef39
Takuji Toyama, Ryotaro Seki, Shu Kasama, Naoki Isobe, Shigeki Sakurai, Hitoshi Adachi, Hiroshi Hoshizaki, Shigeru Oshima, Koichi Taniguchi. (2009) Effectiveness of Nocturnal Home Oxygen Therapy to Improve Exercise Capacity, Cardiac Function and Cardiac Sympathetic Nerve Activity in Patients With Chronic Heart Failure and Central Sleep Apnea. Circulation Journal 73:2, 299-304
CrossRef40
Sudhansu Chokroverty. 2009. Sleep Disturbances in General Medical Disorders. , 550-580.
CrossRef41
Jaime M. Beecroft, James Duffin, Andreas Pierratos, Christopher T. Chan, Philip McFarlane, Patrick J. Hanly. (2009) Decreased chemosensitivity and improvement of sleep apnea by nocturnal hemodialysis. Sleep Medicine 10:1, 47-54
CrossRef42
Akira Tamura, Yoshiyuki Kawano, Junichi Kadota. (2009) Carvedilol Reduces the Severity of Central Sleep Apnea in Chronic Heart Failure. Circulation Journal 73:2, 295-298
CrossRef43
M. M. Siccoli, P. O. Valko, D. M. Hermann, C. L. Bassetti. (2008) Central periodic breathing during sleep in 74 patients with acute ischemic stroke – Neurogenic and cardiogenic factors. Journal of Neurology 255:11, 1687-1692
CrossRef44
Virend K. Somers, David P. White, Raouf Amin, William T. Abraham, Fernando Costa, Antonio Culebras, Stephen Daniels, John S. Floras, Carl E. Hunt, Lyle J. Olson, Thomas G. Pickering, Richard Russell, Mary Woo, Terry Young. (2008) Sleep Apnea and Cardiovascular Disease. Journal of the American College of Cardiology 52:8, 686-717
CrossRef45
Jong Yong A. Foo, Stephen J. Wilson, Gordon R. Williams, Margaret-Ann Harris, David M. Cooper. (2008) Investigation of Pulse Transit Time Characteristics During Single and Recurrent Obstructive Respiratory Events. Journal of Clinical Monitoring and Computing 22:4, 327-332
CrossRef46
Thomas E Vanhecke, Barry A Franklin, Steven C Ajluni, R Bart Sangal, Peter A McCullough. (2008) Cardiorespiratory fitness and sleep-related breathing disorders. Expert Review of Cardiovascular Therapy 6:5, 745-758
CrossRef47
Frédéric Roche, Delphine Maudoux, Yann Jamon, Jean-Claude Barthelemy. (2008) Monitoring of ventilation during the early part of cardiopulmonary exercise testing: The first step to detect central sleep apnoea in chronic heart failure. Sleep Medicine 9:4, 411-417
CrossRef48
Denham S. Ward, Jaideep J. Pandit. 2008. Airway Management and Physiologic Control of Ventilation. , 389-400.
CrossRef49
Julio A. Barcena, James C. Fang. (2007) Diagnosis and treatment of sleep apnea in heart disease. Current Treatment Options in Cardiovascular Medicine 9:6, 501-509
CrossRef50
Wilbert S. Aronow. (2007) Cardiovascular Manifestations Seen in Obstructive Sleep Apnea. Comprehensive Therapy 33:2, 82-86
CrossRef51
Mónica Llombart, Eusebi Chiner, Elia Gómez-Merino, Ada Luz Andreu, Esther Pastor, Ana Camarasa. (2007) Síndrome de apnea central de origen multifactorial tratado mediante soporte ventilatorio domiciliario. Archivos de Bronconeumología 43:8, 467-471
CrossRef52
Thierry Badoual, Luc Hittinger, Marie-Pia d'Ortho. (2007) Syndrome d'apnées du sommeil et insuffisance cardiaque. La Presse Médicale 36:6, 990-998
CrossRef53
Lyle J. Olson, Virend K. Somers. (2007) Sleep apnea: Implications for heart failure. Current Heart Failure Reports 4:2, 63-69
CrossRef54
Austin Chin Chwan Ng, Saul Benedict Freedman, Andrew Paul Sindone. (2007) Autonomic Abnormalities in Congestive Heart Failure Patients With Sleep-Disordered Breathing. Journal of Cardiac Failure 13:5, 395-400
CrossRef55
David Wang, Ronald R. Grunstein, Harry Teichtahl. (2007) Association between ventilatory response to hypercapnia and obstructive sleep apnea–hypopnea index in asymptomatic subjects. Sleep and Breathing 11:2, 103-108
CrossRef56
Timothy J. Barreiro, David J. Gemmel. (2007) Noninvasive Ventilation. Critical Care Clinics 23:2, 201-222
CrossRef57
Patrick Hanly. (2007) Sleep Disorders and End-Stage Renal Disease. Sleep Medicine Clinics 2:1, 59-66
CrossRef58
Zbigniew L. Topor, Konstantinon Vasilakos, Magdy Younes, John E. Remmers. (2007) Model based analysis of sleep disordered breathing in congestive heart failure. Respiratory Physiology & Neurobiology 155:1, 82-92
CrossRef59
2007. Respiratory Rate and Abnormal Breathing Patterns. , 187-202.
CrossRef60
Kentaro Meguro, Takuji Toyama, Hitoshi Adachi, Shigeru Ohshima, Koichi Taniguchi, Ryozo Nagai. (2007) Assessment of central chemosensitivity and cardiac sympathetic nerve activity using I-123 MIBG imaging in central sleep apnea syndrome in patients with dilated cardiomyopathy. Annals of Nuclear Medicine 21:1, 73-78
CrossRef61
R. TKACOVA, H. WANG, T. D. BRADLEY. (2006) Night-to-night alterations in sleep apnea type in patients with heart failure. Journal of Sleep Research 15:3, 321-328
CrossRef62
Rishi Sukhija, Wilbert S. Aronow, Rasham Sandhu, Priyanka Kakar, George P. Maguire, Chul Ahn, Stuart G. Lehrman. (2006) Prevalence of Left Ventricular Hypertrophy in Persons With and Without Obstructive Sleep Apnea. Cardiology in Review 14:4, 170-172
CrossRef63
GASPARD MONTANDON, AIDA BAIRAM, RICHARD KINKEAD. (2006) Long-Term Consequences of Neonatal Caffeine on Ventilation, Occurrence of Apneas, and Hypercapnic Chemoreflex in Male and Female Rats. Pediatric Research 59:4 Part 1, 519-524
CrossRef64
T. Aittokallio, M. Gyllenberg, O. Polo, J. Toivonen, A. Virkki. (2006) Model-Based Analysis of Mechanisms Responsible for Sleep-Induced Carbon Dioxide Differences. Bulletin of Mathematical Biology 68:2, 315-341
CrossRef65
Jean-Louis Pépin, Nathalie Chouri-Pontarollo, Renaud Tamisier, Patrick Lévy. (2006) Cheyne–Stokes respiration with central sleep apnoea in chronic heart failure: Proposals for a diagnostic and therapeutic strategy. Sleep Medicine Reviews 10:1, 33-47
CrossRef66
Kosuke Tsukamoto, Akitoshi Ohara. (2006) Temporal Worsening of Sleep-Disordered Breathing in the Acute Phase of Myocardial Infarction. Circulation Journal 70:12, 1553-1556
CrossRef67
Shigetake Sasayama, Toru Izumi, Yoshihiko Seino, Kenji Ueshima, Hidetsugu Asanoi, for The CHF-HOT Study Group. (2006) Effects of Nocturnal Oxygen Therapy on Outcome Measures in Patients With Chronic Heart Failure and Cheyne-Stokes Respiration. Circulation Journal 70:1, 1-7
CrossRef68
Keith R. BURGESS, Jacky COOPER, Anthony RICE, Keith WONG, Tahnee KINSMAN, Allan HAHN. (2006) Effect of simulated altitude during sleep on moderate-severity OSA. Respirology 11:1, 62-69
CrossRef69
Erik C. Skobel, Anil-Martin Sinha, Christine Norra, Winfried Randerath, Ole-Alexander Breithardt, Christian Breuer, Peter Hanrath, Christoph Stellbrink. (2005) Effect of cardiac resynchronization therapy on sleep quality, quality of life, and symptomatic depression in patients with chronic heart failure and Cheyne-Stokes respiration. Sleep and Breathing 9:4, 159-166
CrossRef70
Manuel Varela, Marta Calvo, Miriam Chana, Ivan Gomez-Mestre, Rosa Asensio, Pedro Galdos. (2005) Clinical implications of temperature curve complexity in critically ill patients. Critical Care Medicine 33:12, 2764-2771
CrossRef71
Jerry J. Batzel, Franz Kappel, Susanne Timischl-Teschl. (2005) A cardiovascular-respiratory control system model including state delay with application to congestive heart failure in humans. Journal of Mathematical Biology 50:3, 293-335
CrossRef72
Kentaro Meguro, Hitoshi Adachi, Shigeru Oshima, Koichi Taniguchi, Ryozo Nagai. (2005) Exercise Tolerance, Exercise Hyperpnea and Central Chemosensitivity to Carbon Dioxide in Sleep Apnea Syndrome in Heart Failure Patients. Circulation Journal 69:6, 695-699
CrossRef73
Neil J. Douglas. 2005. Respiratory Physiology: Control of Ventilation. , 224-231.
CrossRef74
Virend K. Somers, Shahrokh Javaheri. 2005. Cardiovascular Effects of Sleep-Related Breathing Disorders. , 1180-1191.
CrossRef75
Jasdeep Sidana, Wilbert S. Aronow, Gautham Ravipati, Brian Di Stante, John A. McClung, Robert N. Belkin, Stuart G. Lehrman. (2005) Prevalence of Moderate or Severe Left Ventricular Diastolic Dysfunction in Obese Persons with Obstructive Sleep Apnea. Cardiology 104:2, 107-109
CrossRef76
Shahrokh Javaheri. 2005. Heart Failure. , 1208-1217.
CrossRef77
David P. White. 2005. Central Sleep Apnea. , 969-982.
CrossRef78
Tadayoshi Miyamoto, Masashi Inagaki, Hiroshi Takaki, Toru Kawada, Yusuke Yanagiya, Masaru Sugimachi, Kenji Sunagawa. (2004) Integrated characterization of the human chemoreflex system controlling ventilation, using an equilibrium diagram. European Journal of Applied Physiology 93:3, 340-346
CrossRef79
Anil-Martin Sinha, Erik C Skobel, Ole-Alexander Breithardt, Christine Norra, Kai U Markus, Christian Breuer, Peter Hanrath, Christoph Stellbrink. (2004) Cardiac resynchronization therapy improves central sleep apnea and Cheyne-Stokes respiration in patients with chronic heart failure. Journal of the American College of Cardiology 44:1, 68-71
CrossRef80
Luc J. Teppema, Albert Dahan. (2004) Low-dose acetazolamide reduces the hypoxic ventilatory response in the anesthetized cat. Respiratory Physiology & Neurobiology 140:1, 43-51
CrossRef81
STEPHANE GARRIGUE, PHILIPPE BORDIER, S. SERGE BAROLD, JACQUES CLEMENTY. (2004) Sleep Apnea:. A New Indication for Cardiac Pacing?. Pacing and Clinical Electrophysiology 27:2, 204-211
CrossRef82
Aiko Ogawa, Takashi Iwase, Takanobu Yamamoto, Shinichirou Nishiyama, Koji Narui, Shinichi Momomura. (2004) Improvement of Cheyne-Stokes Respiration, Central Sleep Apnea and Congestive Heart Failure by Noninvasive Bilevel Positive Pressure and Medical Treatment. Circulation Journal 68:9, 878-882
CrossRef83
Katsuhisa Banno, Toshiaki Shiomi, Ryujiro Sasanabe, Kazuo Otake, Rika Hasegawa, Masato Maekawa, Takayuki Ito. (2004) Sleep-Disordered Breathing in Patients With Idiopathic Cardiomyopathy. Circulation Journal 68:4, 338-342
CrossRef84
S Garrigue, P Bordier, J Clémenty. (2003) Apnées du sommeil et stimulation cardiaque : mécanismes d’action et perspectives. Annales de Cardiologie et d'Angéiologie 52:4, 239-245
CrossRef85
Joao J. Leite, Alfredo J. Mansur, Humberto F.G. de Freitas, Paulo R. Chizola, Edimar A. Bocchi, Mario Terra-Filho, J.Alberto Neder, Geraldo Lorenzi-Filho. (2003) Periodic breathing during incremental exercise predicts mortality in patients with chronic heart failure evaluated for cardiac transplantation. Journal of the American College of Cardiology 41:12, 2175-2181
CrossRef86
J.o-Dee L Lattimore, David S Celermajer, Ian Wilcox. (2003) Obstructive sleep apnea and cardiovascular disease. Journal of the American College of Cardiology 41:9, 1429-1437
CrossRef87
M. J. Morrell. (2003) Sleep and Breathing in Congestive Heart Failure. Clinical Pulmonary Medicine 10:3, 170-176
CrossRef88
Kingman P. Strohl. (2003) Periodic breathing and genetics. Respiratory Physiology & Neurobiology 135:2-3, 179-185
CrossRef89
T. Kara, K. Narkiewicz, V. K. Somers. (2003) Chemoreflexes - physiology and clinical implications. Acta Physiologica Scandinavica 177:3, 377-384
CrossRef90
(2002) Obesity and the Risk of Heart Failure. New England Journal of Medicine 347:23, 1887-1889
Full Text91
Shinji Teramoto, Yuichi Inoue, Yasuyoshi Ouchi. (2002) Clinical significance of geriatric sleep apnea syndrome. Geriatrics and Gerontology International 2:4, 163-171
CrossRef92
Sevag Bananian, Stuart G. Lehrman, George P. Maguire. (2002) Cardiovascular Consequences of Sleep-related Breathing Disorders. Heart Disease 4:5, 296-305
CrossRef93
Laffey, John G., Kavanagh, Brian P., . (2002) Hypocapnia. New England Journal of Medicine 347:1, 43-53
Full Text94
Gilmar F Prado, Richard P Allen, Virgı́nia M.F Trevisani, Vanessa G Toscano, Christopher J Earley. (2002) Sleep disruption in systemic sclerosis (scleroderma) patients: clinical and polysomnographic findings. Sleep Medicine 3:4, 341-345
CrossRef95
Wilhelm Nolte, Carsten Radisch, Andrea Rodenbeck, Jens Wiltfang, Michael Hufner. (2002) Polysomnographic findings in five adult patients with pituitary insufficiency before and after cessation of human growth hormone replacement therapy. Clinical Endocrinology 56:6, 805-810
CrossRef96
Gary T. Midelton, William H. Frishman, Stanley S. Passo. (2002) Congestive Heart Failure and Continuous Positive Airway Pressure Therapy: Support of a New Modality for Improving the Prognosis and Survival of Patients With Advanced Congestive Heart Failure. Heart Disease102-109
CrossRef97
Stuart G. Lehrman, George P. Maguire. (2002) Positive Airway Pressure for the Failing Heart. Heart Disease61-62
CrossRef98
Shinji Teramoto, Takeo Ishii, Takeshi Matsuse. (2001) Central sleep apnoeas in patients with Charcot-Marie-Tooth disease. The Lancet 358:9275, 70
CrossRef99
Bernd M. Sanner, Martin Konermann, Claus Doberauer, Thomas Weiss, Walter Zidek. (2001) Sleep-disordered breathing in patients referred for angina evaluation-association with left ventricular dysfunction. Clinical Cardiology 24:2, 146-150
CrossRef100
(2000) Central Sleep Apnea and Heart Failure. New England Journal of Medicine 342:4, 293-294
Full Text101
Cherniack, Neil S., . (1999) Apnea and Periodic Breathing during Sleep. New England Journal of Medicine 341:13, 985-987
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