Albert L. Rafanan, MD; Joseph A. Golish, MD, FCCP; Dudley S. Dinner, MD; L. Kathleen Hague, RN; and Alejandro C. Arroliga, MD, FCCP

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1 Nocturnal Hypoxemia Is Common in Primary Pulmonary Hypertension* Albert L. Rafanan, MD; Joseph A. Golish, MD, FCCP; Dudley S. Dinner, MD; L. Kathleen Hague, RN; and Alejandro C. Arroliga, MD, FCCP Study objective: Unsuspected sleep-related respiratory events are common in patients with severe pulmonary disease. Sleep in patients with primary pulmonary hypertension (PPH) has not been studied (to our knowledge). The purpose of this study was to measure the prevalence of respiratory disturbances and nocturnal hypoxemia during the sleep of patients with PPH. Setting: Tertiary-care referral hospital. Design: Retrospective review. Patients: Thirteen patients with PPH. Measurements: All patients underwent a single-night comprehensive polysomnogram study. Patients who spent > 10% of the total sleep time with oxygen saturation by pulse oximetry (SpO 2 ) at < 90% or who needed oxygen to maintain their SpO 2 level at > 90% were classified as nocturnal desaturators. Analysis was performed to determine which clinical variables (ie, demographics, body mass index, spirometry, diffusion capacity, right heart catheterization pressures, 6-min walk test, arterial blood gas levels, resting and walking SpO 2 levels, and polysomnogram variables) would predict nocturnal desaturation. Statistical significance was considered when p values were < Results: Of the 13 patients in the study, 10 (77%) were nocturnal desaturators. All patients had normal apnea indexes, but two had mild elevations of the hypopnea index (< 15 episodes per hour). Nocturnal desaturations occurred independently of apneas or hypopneas. Six patients who did not have O 2 titration during sleep spent > 25% of sleep time with SpO 2 < 90%. The mean ( SD) variables that were significantly different between desaturators (10 patients) and nondesaturators (3 patients) were FEV 1 ( % predicted vs % predicted, respectively; p 0.002), resting PaO 2 ( vs mm Hg, respectively; p 0.001), alveolar-arterial oxygen pressure difference (P[A-a]O 2 ) ( vs mm Hg, respectively; p 0.048), resting SpO 2 ( % vs %, respectively; p 0.038), and walking SpO 2 ( % vs %, respectively; p 0.002). The mean hemoglobin level was higher in the group of nocturnal desaturators than in the group of nondesaturators ( vs g/dl, respectively; p < ). Conclusion: Seventy-seven percent of patients with PPH have significant nocturnal hypoxemia that is unrelated to apneas and hypopneas. Nocturnal desaturation occurs more frequently in patients with higher P(A-a)O 2 values and lower FEV 1 values, resting arterial PaO 2 and SpO 2 values, and walking SpO 2 values. (CHEST 2001; 120: ) Key words: nocturnal hypoventilation; obstructive sleep apnea; oxygen therapy; pulmonary hypertension; sleep Abbreviations: BMI body mass index; Dlco diffusing capacity of the lung for carbon monoxide; P(Aa)O 2 alveolar-arterial oxygen pressure difference; PPH primary pulmonary hypertension; REM rapid eye movement; Spo 2 oxygen saturation by pulse oximetry; TST total sleep time; TST-Spo 2 90% total sleep time with an oxygen saturation of 90% Primary pulmonary hypertension (PPH) is a rare disease that is more commonly seen in women and is characterized by a progressive increase in *From St. Vincent Mercy Medical Center Hospital and the Medical College of Ohio (Dr. Rafanan), Toledo, OH; and the Departments of Pulmonary and Critical Care Medicine (Drs. Golish and Arroliga, and Ms. Hague), and Neurology (Dr. Dinner), The Cleveland Clinic Foundation, Cleveland, OH. Manuscript received September 11, 2000; revision accepted April 23, Correspondence to: Alejandro C. Arroliga, MD, FCCP, Head, Section of Critical Care Medicine, Department of Pulmonary and Critical Care Medicine, The Cleveland Clinic Foundation, 9500 Euclid Ave, Cleveland, OH ; arrolia@ccf.org pulmonary arterial pressure and resistance in the absence of identifiable causes. 1 When untreated, patients with PPH have a very poor prognosis, with a 1-year survival rate of 68% and a 5-year survival rate of 34%. 2 Current treatments for PPH include vasodilators, anticoagulants, supplemental oxygen, and lung transplantation. 3 Sleep causes a profound effect in individuals with severe pulmonary disease, by its influence on the respiratory drive, airway stability, and ventilatory mechanics. 4 Reported sleep disturbances in patients with pulmonary disease include unsuspected ob- 894 Clinical Investigations

2 structive sleep apnea and a high prevalence of insomnia, excessive daytime sleepiness, and nightmares compared to the general population. In addition, patients with COPD, kyphoscoliosis, and neuromuscular disorders have been shown to frequently desaturate, especially during rapid eye movement (REM) sleep. 4 Nocturnal hypoxemia can lead to polycythemia, respiratory failure, and pulmonary hypertension. Hypoxemia causes pulmonary vasoconstriction and elevated pulmonary artery pressures. In patients with PPH, untreated and unsuspected nocturnal hypoxemia can have deleterious effects and may worsen the pulmonary hypertension. To our knowledge, the characteristics of sleep in patients with PPH have not been reported. The purpose of this study was to evaluate the prevalence of respiratory disturbances and nocturnal hypoxemia during the sleep of patients with PPH. Clinical variables that could predict nocturnal hypoxemia also were examined. Materials and Methods Patients with PPH who underwent a comprehensive polysomnogram study (polysomnography) in our institution were included in the study. Pulmonary hypertension was confirmed by right heart catheterization and was defined as a mean pulmonary artery pressure of 25 mm Hg at rest or 30 mm Hg during exercise. PPH was diagnosed according to the standard criteria provided by the National Registry of Primary Pulmonary Hypertension 1 in 30 patients evaluated by one of the authors (A.C.A.). In brief, secondary causes of pulmonary hypertension were ruled out in all patients by histories, results of physical examinations, pulmonary function studies, and an extensive workup that included chest radiographs, ventilation-perfusion scans, right and left heart catheterization, high-resolution CT scans, and transthoracic echocardiograms with bubble studies. Transesophageal echocardiograms, pulmonary angiograms, and open-lung biopsies were performed in selected patients if they were clinically indicated. 5 The standard initial evaluation before polysomnography included an interview of the patient about sleep symptoms and a calculation of body mass index (BMI). Pulmonary function studies (ie, measurements of FEV 1, FVC, and diffusing capacity of the lung for carbon monoxide [Dlco]) were performed (Jaeger Compactlabs; Millbery, OH) with the patient in the seated position according to approved standards. 6 Arterial blood gases were measured with patients seated and breathing room air. The alveolar Po 2 for the calculation of the alveolar-arterial oxygen pressure difference (P[A-a]O 2 ) was derived from the alveolar gas equation. 7 The level of hemoglobin and the hematocrit were measured in all patients. The 6-min walk test was performed with the patient walking for 6 min in a closed, level corridor according to a standardized protocol. 8 The distance walked was recorded. Oxygen saturation by pulse oximetry (Spo 2 ) was measured at rest and during ambulation. Oxygen titration was performed for all patients with oxygen desaturation, which was defined as Spo 2 90%. A single-night comprehensive polysomnography was performed according to established standards. 9 Multichannel recordings of the EEG, electro-oculogram, electromyogram, oronasal flow (by thermistor), respiratory effort (by abdominal and thoracic strain gauges), and oxygen saturation were recorded onto a computerized workstation (Vangard; Cleveland, OH). Sleep staging was performed by standard criteria. 10 An apnea was defined as the cessation of airflow with a duration of at least 10 s. An obstructive apnea was defined as an apnea in which there was evidence of persistent respiratory effort. A central apnea was defined as an apnea in which there was no evidence of respiratory effort. A hypopnea was defined as a reduction in airflow by 50%, with a duration of at least 10 s. The proportion of total sleep time (TST) spent with an Spo 2 of 90% (TST-Spo 2 90%) was derived from a cumulative frequency curve of arterial oxygen saturation. Oxygen titration was not routinely performed unless requested by the ordering physician. Patients who had spent 10% TST-Spo 2 90% or who needed oxygen to maintain Spo 2 at 90% were classified as nocturnal desaturators. Computerized polysomnography records were reviewed to determine the correlation of oxygen desaturation and respiratory events (ie, apneas and hypopneas). Data are presented as mean SD and were compared with Student s t test and Fisher s Exact Test. Statistical tests were two-tailed, and p values 0.05 were considered to be significant. Results We studied 13 patients with PPH (12 women and 1 man) with a mean age of years and a mean BMI of kg/m 2. Other characteristics are shown in Table 1. Three patients were receiving daytime resting oxygen supplementation, and six patients needed oxygen only when walking. Our patients slept an average of min, with REM sleep making up % of TST (Table 1). Snoring was noted in 85% of patients. All study patients had a normal apnea index (ie, 5 episodes per hour), and two patients had mild sleep hypopnea (hypopnea index, 5 to 15 episodes per hour). Ten patients (77%) were classified as nocturnal desaturators (Table 2). The oxygen desaturations Table 1 Characteristics of 13 Patients With PPH* Variables Values Demographics Age, yr Sex, % female 92 BMI, kg/m Right heart catheterization pressures Mean pulmonary artery pressure, mm Hg Right atrial pressure, mm Hg Cardiac index, L/min/m min walk distance, feet Pulmonary function testing, % predicted FEV FVC Dlco Polysomnogram variables TST, min REM sleep, % Sleep efficiency, % Respiratory disturbance index, apnea hypopnea index score *Values given as mean SD, unless otherwise indicated. CHEST / 120 / 3/ SEPTEMBER,

3 Table 2 Supplemental Oxygen Use and Sleep-Related Respiratory Events of Patients With PPH Patient Daytime Rest O 2 Use,* L Walk O 2 Use,* L Nocturnal O 2 Use,* L TST-Spo 2 90%, % Snoring Lowest O 2 Saturation, % Apnea Index Hypopnea Index Nocturnal desaturators who did not have O 2 titration Heavy None None None 52 Light None 1 None 84 Light Heavy None 6 None 65 Light None None None 26 Light Nocturnal desaturators who had O 2 titration 7 None None 2 1 None None Light None Light Heavy Nonnocturnal desaturators 11 None None None 1 Heavy None None None 0 None None None None 0 Light *Flow of oxygen via nasal cannula. occurred independently of apneas and hypopneas. Among the nocturnal desaturators, three patients were hypoxemic at rest, and seven experienced oxygen desaturation with exercise. Of the 10 patients who were classified as nocturnal desaturators, 6 did not have oxygen titration during sleep, and all 6 patients spent 25% TST- Spo 2 90%. The other four nocturnal desaturators underwent oxygen titration during sleep requiring 2 to3lo 2 above the resting settings. Two patients were kept on their resting O 2 setting during the polysomnography; they spent 65% of the sleep time with saturation 90% and had saturation nadirs of 69% and 78%. Two patients also had frequent premature ventricular contractions during sleep. All 13 patients had at least one sleep complaint (Table 3). Sleep symptoms and sleep parameters (ie, TST, sleep efficiency, percentage of sleep that was REM sleep, and apnea and hypopnea index) were not statistically different between groups (Table 4). Desaturators and nondesaturators had similar ages, Table 3 Frequencies of Sleep Symptoms in Nocturnal Desaturators and Nondesaturators Sleep Symptom Nondesaturators, %(n 3) Desaturators, %(n 10) Excessive daytime sleepiness 0 30 Witnessed apneas 0 30 Insomnia Morning headaches Frequent nocturnal awakenings BMIs, 6-min walk distances, and right heart catheterization pressures (data not shown). Variables that were significantly different between desaturators and nondesaturators were FEV 1 ( % predicted vs % predicted; p 0.002), resting Pao 2 ( vs mm Hg; p 0.001), P(Aa)O 2 ( vs mm Hg; p 0.048), resting Spo 2 ( % vs %; p 0.038), and walking Spo 2 ( % vs %; p 0.002) (Fig 1). All patients had one or more transthoracic echocardiograms with contrast performed within 6 months of the polysomnography. Only 2 of the 13 patients (15.3%) had evidence of a patent foramen ovale. The two patients were from the nocturnal desaturators group. The mean hemoglobin level for the three patients who did not desaturate was g/dl, and Table 4 A Comparison of Sleep Variables Between Nocturnal Desaturators and Nondesaturators* Sleep Variable Nondesaturators (n 3) Desaturators (n 10) p Value TST, min Sleep efficiency, % REM sleep, % Apnea index, apneas/h Hypopnea index, hypopneas/h Apnea-hypopnea index, apneas and hypopneas/h *Values given as mean SD, unless otherwise indicated. 896 Clinical Investigations

4 Figure 1. Comparison of ventilatory mechanics and oxygen measurements between desaturators and nondesaturators. AaPO2 P(A-a)O 2. * p for the 10 patients who were nocturnal desaturators it was g/dl (p ). There was a statistically significant difference as well between the hematocrit level of patients who did not desaturate at night ( %) and that of the nocturnal desaturators ( %; p ). Discussion The most important finding of the study is that 77% of the patients with PPH had significant nocturnal hypoxemia. Severe oxygen desaturation occurred independently of the presence of apneas or hypopneas. This study is important as well because it suggests that monitoring nocturnal oxygen saturation might be beneficial for patients with PPH. Nocturnal hypoxemia occurred in 77% of our study population, and all nocturnal desaturators who did not undergo oxygen titration spent 25% TST- Spo 2 90%. Before the polysomnography study, only four patients (31%) received nocturnal O 2 supplementation, and in two of those patients the prescribed O 2 level was adequate. In patients who had oxygen titration during sleep, it appears that levels 2 to 3LO 2 above the resting O 2 requirements were adequate. In this study, nocturnal desaturation was significantly associated with baseline resting oxygen measurements (ie, Pao 2, P[A-a]O 2, and resting Spo 2 ), walking Spo 2, and FEV 1 percent predicted. Lower baseline resting oxygen measurements were associated with nocturnal hypoxemia. It is likely that in the group of nocturnal desaturators the small changes in Pao 2 that are frequently seen even in healthy subjects 11 will explain the significant drop in Spo 2 that was observed in these patients, because patients were already in the steeper part of the oxyhemoglobin dissociation curve. 11,12 Oxygen desaturation has been reported to occur in asymptomatic healthy subjects. 11,12 Block and colleagues 12 have reported that oxygen desaturation is more frequent in men than women and that the incidence of nocturnal oxygen desaturation correlates with increasing age and the presence of obesity. 12 Gries and Brooks, 11 in a study of 350 healthy subjects of whom 47% were women, reported a mean (SD) low oxygen saturation level of 90.4% (3.1%) and a median saturation of 96.5% (1.5%). Our patients were predominantly women, and the mean respiratory disturbance index was 5, which is similar to the index of the patients described by Gries and Brooks 11 ; however, the degree of desaturation was more severe in our patients. Walking Spo 2 seemed to be a better predictor of nocturnal hypoxemia because all patients who desaturated when walking were subsequently found to have nocturnal hypoxemia. This may be because Spo 2 reflects both the resting oxygen measurement and the cardiac reserve. However, it is not a perfect predictor as 20% of the nocturnal desaturators had normal walking Spo 2 level. The mildly decreased FEV 1 of the desaturators was also significantly different from that of nondesaturators ( % predicted vs 98 15% predicted; p 0.002). Reversible airway obstruction in patients with PPH has been reported. 13 This mild airway obstruction may lead to an increased ventilation-perfusion mismatch during sleep that further impairs the marginal oxygenation of patients with PPH. Other variables, such as age, BMI, pulmonary artery pressures, right atrial pressures, cardiac index, 6-min walk distance, and apnea-hypopnea index were not found to be significantly different. Hypoxemia is a potent pulmonary arterial bed vasoconstrictor. Daytime oxygen saturation is routinely checked, and supplemental oxygen is prescribed to patients who are hypoxemic at rest or during exercise. 14 Nocturnal oxygen saturation is not usually monitored unless obstructive sleep apnea is suspected. Untreated nocturnal hypoxemia will lead to increasing pulmonary artery pressures and progressive right ventricular dysfunction. Right ventricular failure accounts for 63% of deaths among patients with PPH. 14 Furthermore, untreated nocturnal hypoxemia can lead to impaired myocardial oxygenation, nocturnal arrhythmias, and, possibly, sudden death. It is interesting to note that the group of patients who experienced nocturnal desaturation in this study had a higher level of hemoglobin and a higher hematocrit when compared with the three patients who did not desaturate, suggesting a compensatory response to the presence of nocturnal hypoxemia. Alternatively, the data might suggest that CHEST / 120 / 3/ SEPTEMBER,

5 the patients who did not desaturate were anemic. A bigger study is needed to clarify this issue. Patients with obstructive and restrictive lung disease have been shown to have unsuspected nocturnal hypoxemia, despite normal baseline oxygen saturation levels The abnormality of PPH, however, involves the pulmonary vascular bed (ie, medial hypertrophy, intimal fibrosis, and plexogenic pulmonary arteriopathy) with a normal pulmonary parenchyma. 14 Pulmonary function studies most often show a mild restrictive defect without obstruction and a reduced Dlco. 1 In the absence of significant obstructive or restrictive lung disease and with adequate baseline oxygen saturation, the mechanism of nocturnal hypoxemia in PPH is unclear. However, we propose several possible explanations. Daytime hypoxemia in patient with PPH is due to the effect of a low mixed-venous oxygen saturation resulting from an inadequate cardiac output and to ventilation-perfusion mismatch. 18 Uncommonly, severe hypoxemia also can be seen in patients with right-to-left shunting from a patent foramen ovale. In this study, only two patients had a patent foramen ovale. Both of them were in the group that desaturated at night. Sleep causes several physiologic changes to respiration. Even in healthy individuals, sleep can cause breathing pattern instability, hypoventilation, upper airway obstruction, ventilationperfusion mismatch, and a decrease in both the hypoxic and hypercapnic ventilatory responses. 19,20 In healthy individuals, these physiologic changes of sleep seem to be of little consequence. In order to maintain a constant mixed-venous oxygen saturation, a 20-mm Hg fall in Pao 2 can be compensated for by an increase in the cardiac output by 50%. 21 However, in patients with severe PPH, cardiac output is already impaired and cannot be further increased. Moreover, the presence of hypoxemia will increase pulmonary artery pressures, further impairing cardiac function. The supine position during sleep may also play a role in producing nocturnal hypoxemia. In the awake state, the assumption of the supine from the sitting position has been described as worsening hypoxemia in patients with pulmonary hypertension from Eisenmenger s syndrome. 22 Sandoval and colleagues 22 suggested that an increased ventilation-perfusion mismatch and/or a diffusion limitation phenomenon were the possible mechanisms. This study is limited by its small sample size, which restricts the power of the study and the generalizability of the data to a larger population. Moreover, its retrospective nature may have created a selection bias, as patients with a higher likelihood of respiratory disturbances were probably more likely to have polysomnography. Nevertheless, this observational study has generated questions worthy of additional research, such as whether routinely monitoring nighttime oxygen saturation in PPH patients will improve their outcomes. Conclusion A high percentage of patients with PPH have significant nocturnal hypoxemia that is unrelated to apneas and hypopneas. Nocturnal desaturation occurs more frequently in patients with higher P(A-a)O 2 values and lower FEV 1, resting arterial Pao 2 and Spo 2, and walking Spo 2 values. References 1 Rich S, Dantzker DR, Ayres SM, et al. Primary pulmonary hypertension: a national prospective study. Ann Intern Med 1987; 107: D Alonzo GE, Barst RJ, Ayres SM, et al. Survival in patients with primary pulmonary hypertension: results from a national prospective registry. Ann Intern Med 1991; 115: Arroliga AC, Dweik RA, Kaneko FJT, et al. Primary pulmonary hypertension: update on pathogenesis and novel therapies. Cleve Clin J Med 2000; 67: Millman RP, Kramer NR. Sleep disorders and outpatient treatment of patients with pulmonary disease. Curr Opin Pulm Med 1996; 2: Kaneko FT, Arroliga AC, Dweik RA, et al. Biochemical reaction products of nitric oxide as quantitative markers of primary pulmonary hypertension. Am J Respir Crit Care Med 1998; 158: American Thoracic Society. Standardization of spirometry: update. Am J Respir Crit Care Med 1995; 102: Anthonisen NR, Fleetham JA. Ventilation: total, alveolar, and dead space. In: Farhi LE, Tenney SM, eds. Handbook of physiology (vol 4): the respiratory system. Bethesda, MD: American Physiological Society, 1987; Enright PL, Sherrill DL. Reference equations for the sixminute walk in healthy adults. Am J Respir Crit Care Med 1998; 158: American Thoracic Society. Indications and standards for cardiopulmonary sleep studies. Am Rev Respir Dis 1989; 139: Rechtschaffen A, Kales A, eds. A manual of standardized terminology: techniques and scoring system for sleep stages of human subjects. Los Angeles, CA: University of California at Los Angeles Brain Information Service/Brain Research Institute, Gries RE, Brooks LJ. Normal oxyhemoglobin saturation during sleep: how low does it go? Chest 1996; 110: Block AJ, Boysen PG, Wynne JW, et al. Sleep apnea, hypopnea and oxygen desaturation in normal subjects: a strong male predominance. N Engl J Med 1979; 300: O Hagan AR, Stillwell PC, Arroliga A. Airway responsiveness to inhaled albuterol in patients with pulmonary hypertension. Clin Pediatr 1999; 38: Rubin LJ. Primary pulmonary hypertension. Chest 1993; 104: Phillipson EA, Goldstein RS. Breathing during sleep in chronic obstructive pulmonary disease: state of the art. Chest 1984; 85(suppl):24S 30S 898 Clinical Investigations

6 16 Guilleminault C, Kurland G, Winkle R, et al. Severe kyphoscoliosis, breathing and sleep: the Quasimodo syndrome during sleep. Chest 1981; 79: Tatsumi K, Kimura H, Kunitomo F, et al. Arterial oxygen desaturation during sleep in interstitial pulmonary disease: correlation with chemical control of breathing during wakefulness. Chest 1989; 95: Walcott G, Burchell HB, Brown AL Jr. Primary pulmonary hypertension. Am J Med 1970; 49: Douglas NJ, White DP, Pickett CK, et al. Respiration during sleep in normal man. Thorax 1982; 37: Bradley TD, Phillipson EA. Sleep disorders. In: Murray JF, Nadel JA, Mason RJ, et al, eds. Textbook of respiratory medicine. Philadelphia, PA: WB Saunders, Catterall JR, Douglas NJ, Calverley PM, et al. Transient hypoxemia during sleep in chronic obstructive pulmonary disease is not a sleep apnea syndrome. Am Rev Respir Dis 1983; 128: Sandoval J, Alvarado P, Martinez-Guerra ML, et al. Effect of body position changes on pulmonary gas exchange in Eisenmenger s syndrome. Am J Respir Crit Care Med 1999; 159: CHEST / 120 / 3/ SEPTEMBER,

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