Nocturnal hypoxaemia in severe scoliosis

Br. J. Dis. Chest (1988) 82, 226

NOCTURNAL

B. MIDGREN*, *Department $Department

HYPOXAEMIA scoLIosIs

IN SEVERE

K. PETERSSON*, L. HANSSON*, L. ERIKSSON?, P. AIRIKKALAS AND D. ELMQVISTS

of Lung Medicine, fDepartment of Clinical Physiology and of Clinical Neurophysiology, University Hospital, S-221 85 Lund,

Sweden

Summary

The relationship between spirometry and daytime blood gases on the one hand and hypoxaemia during sleep on the other was studied in 13 patients with severe thoracic scoliosis. Eight patients had hypoxaemia (mean Sao,
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in identifying patients with nocturnal hypoxaemia (3). We also tested the hypothesis that desaturation during sleep is associated with more severe functional impairment (4) or a history of right ventricular failure (RVF) (3). Patients and Methods Patients Thirteen patients with severe thoracic scoliosis(Cobb’s angle 80”or more) were investigated. Six had idiopathic scoliosis (the exact age of onset was seldom obtainable from the patients) and seven had paralytic scoliosis (poliomyelitis in childhood or adolescence). The six idiopathic and two paralytic scoliotics (numbers 1-8) were referred to the Department of Lung Medicine for evaluation of their respiratory function with special reference to the severity of hypoxaemia during sleep. Five of the paralytic scoliotics (numbers 9-13) were recruited from a survey of respiratory function in patients with poliomyelitis sequelae where patients with VC
Pulmonary function tests (VCsi, {VC in sitting position}, VC,,, {VC in supine position} and FEV1) were performed on a flow integrating pneumotachograph (Siemens Siregnost FD 40 S). Pi,., (maximal inspiratory pressure) and P,,,, (maximal expiratory pressure) were determined from end expiration and end inspiration respectively. Figures for VC and FEV, are given as per cent of predicted based on age and height (14). For analysis of blood gases, pH and BE, 2 ml of blood were drawn from the radial artery of the sitting patient and analysed on a IL 413 blood gas analyser (Instrumentation Laboratories). The A-a O2gradient was calculated from the idealized alveolar gas equation (15), assuming a normal barometric pressure. In vivo oxygen saturation (SaoJ was measured with an ear oximeter (Hewlett Packard HP 47201A or, in three instances, a BTI BIOX III) (16-18). The values obtained with the BIOX 111were adjusted according to Chapman (17) to be comparable with the values obtained with the Hewlett Packard oximeter. Saol during daytime wakefulness was recorded during 50-60 minutes (without supplemental oxygen) with the patient resting in a chair. Whole night sleep recordings of electroencephalogram, electro-oculogram, submental electromyogram, electrocardiogram, respiratory movements of thorax and abdomen, and oronasal airflow were performed as previously described (3). All variables were recorded simultaneously on a 16-channel ink jet recorder. The continuous sleep records were scored for levels of sleep (1,2,3+4 and REM) using scoring epochs of 30 seconds (19). Oxygen saturation during sleep was measured by the same ear oximeter as during wakefulness; transcutaneous Pco, (PtccoJ was measured with a capnometer (Hewlett Packard 47210A option AlO) (20,21). The signals from the oximeter and the capnometer were recorded on a Tarkan W+ W 600 two-channel strip chart recorder, manually synchronized with the EEG recorder. The recordings were then digitized with 30-second sampling intervals (together with data on sleep stage) on a plotter

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(Hewlett Packard 7475A) connected to a microcomputer (IBM PC). Mean Saoz was calculated separately for nocturnal wakefulness, non-REM and REM sleep. The sleep-induced fall in Saozwas defined as the difference between mean Sao, during nocturnal wakefulness and sleep (average for all stages). To test the reproducibility of the 30-second sampling method for Sao2,we selected five Sao2 recordings. Segments of 5,15 and 45 minutes’ duration with large and rapid variations in Sao, were digitized, five times each. Reproducibility was tested with two-way analysis of variance. Since the slow response characteristics of the capnometer make determinations of mean Ptcco, during different sleep stages uncertain, the difference between highest and lowest Ptcco2 during the night was used as an approximate measure of sleep-induced change in ventilation. Because of the non-normal distribution of many of our data, statistical analysis was made by the Mann-Whitney U-test and Spearman’s rank correlation test, unless otherwise stated. P-values< 0.05 were considered significant. RESULTS Wakefulness data

Table I shows the pulmonary function data for all patients. Their ventilatory impairment was purely restrictive with a normal or elevated FEVJVC ratio and no effect of bronchodilators on VC or FEV,. Blood gases during daytime showed an elevated A-a 0, gradient and, in most cases, an increased Pace,. There was a hypoventilation pattern with a strong inverse relationship between Pao, and Pace, (~~‘-0.89, P~O.002). Sao, during daytime and nocturnal wakefulness were closely interrelated

(r,=O.99, P
Table I. Functional and anthropometric data during wakefulness Age

Paral

Sex

RVF

Paq (kPa)

Pace, (kPa)

A-Do,

Diff

dwSao,

(kPa)

@Pa)

(%I

4.5 3.5 8 4.5

5.2 5.3 1.3 7.9 7.5 9.2 7.2 8.6

8.4 7.6 8.8 7.6 7.5 6.5 7.3 6.5

4.7 5.6 2.1 3.0 3.5 3.0 4.0 3.6

-3.2 -2.3 -1.5 0.3 0.0 2.7

72.5 77.2 82.9 90.1 90.3 90.7

-0.1 2.1

92.8

30.8

8.5

7.3

7.5

3.7

-0.25

85.2

22 0 4.8 0 8.7

3s 40 83 67 56

5 0 4 2

8.6 9.5 11.6 12.7 12 .5

6.6 5.2 4.4 5.1 5.4

3.5 4.3 3.1 1.2

1.0

2.0 4.3 7.2 7.6 7.1

93.2 94.4 96.5 97.4 98.0

50.1

7.1

56.1

1.9

11.0

5.3

2.6

5.6

95.9

0.0067

0.028

0.0052

0.016

0.0067

0.0082

0.24

0.0084

0.0045

VC,,,

VCl.,,

FEV,

BE

(% pred)

(mmol/l) 14 13

21

30 35 26 30 30 30 31 34

26

(% pred) Patients with nocturnal 1 60 N 2 50 N 3 54 N 4 56 N 5 49 Y 6 39 N I 55 Y 8 60 N Mean

52.9

Patients without 9

10 11 12 13 Mean

59 58

60 54 31 53.6

P-value NH vs. non-NH

hypoxaemia F Y M Y F Y F Y M N M N M Y M N

33 36 25 32

30 21 29 29 30.2

nocturnal hypoxaemia Y F N 33 Y F N 41 Y F N 68 Y F N 65 Y M N 44

29 20 25 46 15

11 10

-1.5

Statistical analysis is made with the Mann-Whitney U-test. Paral, paralytic scoliosis; RVF, right ventricular failure; VC,,,, vital capacity in sitting position; VC,,,, fall in VC from sitting to supine posture, in % of VC,,,; FEV,, forced expiratory volume in one second; A-aDo,, alveobarterial oxygen gradient; Diff, Pao,-Pace,; dw.Sao,, oxygen saturation during diurnal wakefulness.

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Sleep data Mean sleeping time was 211 minutes (range 119-375) (Table II) with a shorter than expected percentage of REM sleep (22). Since patients 1 and 2 slept with supplemental oxygen, they were excluded from the quantitative analyses of Sao, during sleep. The interrupted sleeping pattern in patient 3 (119 minutes divided into 33 periods of sleep) made it impossible for the cutaneous capnometer to reflect accurately the changes in Pace, with transitions between wakefulness and sleep; we therefore excluded her from the analysis of changes in Ptcco,. The test for reproducibility of the sampling method for Sao, showed that the difference between repeated analyses (typically less than 1% Sao,) was not significant. F4,16for 5, 1.5, and 45 minutes’ sampling were 1.37,2.57, and 0.45 respectively (critical value at the 95% level is 3.01). Table II. Total sleeping time and distribution of sleep stages TST

Stage I

Stage 2

Stage 3+4

Stage REM

(min)

(%)

(%I

(%)

(%I

216 +86

20.0 +13.0

43.6 +-8.3

26.1 k17.6

5.6 +8.4

203 +101

17.6 +11.6

56.4 f10.5

15.6 26.3

10.0 +10.8

Ns

NS

P-CO.02

NS

NS

NH group

Mean SD

Non-NH group

Mean SD

Significance of difference

(Mann-Whitney) 100,

Nocturnal waket,lness

Non-REM sleep

REM sleep

Fig. 1. Sao, during wakefulness and sleep for all patients. The broken lines denote the patients who

received oxygen during the study

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Sao, invariably fell during non-REM sleep with, in most cases, a further fall during REM sleep (Fig. 1). Mean Sao, during sleep was strongly related to Sao, during wakefulness (r,=O.99) (Fig. 2) but also to Pao,, Pace, and difference Pao,-Pace, (Table III). Moreover, it was related to VC, FEV, and to the fall in VC with change of posture. The sleep-induced fall in Sao, was significantly related to nocturnal increase in Ptcco, (Fig. 3). Eight patients had NH, defined as mean Sao,<90% during sleep. They differed significantly from the other five patients with respect to blood gases during daytime (all were hypercapnic) and to VC,,,, VC,,r, fall in VC with posture, and FEV, (Table I). They did not, however, differ regarding Pi,,, or Pe,,., although the values were abnormally low (23) in the group as a whole (average PimaX=- and P,,,,=74 cmH,O). Right ventricular failure (clinical diagnosis based on the appearance of peripheral oedema and jugular venous distension) had been present in five out of the eight NH patients but in none of the five non-NH patients. Seven of the NH patients, but none of the non-NH patients, had been hospitalized due to respiratory disease. Both group differences are statistically significant (P
In patient 1, the increase in oxygen flow from 1.5 to 2 litres/min increased her calculated Pao, (24) from 6.8 to 8.7 kPa during sleep with a concomitant rise in calculated peak Pace, (20) from 11.5 to 12.2 kPa. This hypercapnia was associated with unpleasant symptoms in the morning. In patient 2, the increase in oxygen flow from 0.9 to 1.5 litres/min caused a rise in calculated Pao, during sleep from 5.9 to only 6.3 kPa but the calculated peak Pace, during sleep rose from 10.0 to 12.8 kPa. The increase in calculated Pao, from 3.9 to 5 .O kPa IOOY=-17.9 r= 0.996

90 -

+1.17x

P
60 -

50

60 310,

70 during

nocturnal

80 wakefulness

90 (%)

Fig. 2. Relationship between Sao2 during wakefulness and sleep. r- and P-values refer to linear

regression analysis. The filled symbols denote the patients who received oxygen, they are not included in the regression analysis. The broken line is the line of identity

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(mmHg)

r ~0.65 PCO.05 Y=-0.13-0.25X

Fig. 3. Relationship between decrease in Saozand increase in Ptccozwith sleep. r- and P-values refer to linear regression analysis. The filled symbols denote the patients who received oxygen, they are not included in the regression analysis

Table III. Correlations between mean oxygen saturation during sleep and other variables

Mean Saoz during sleep (n=ll)

vcsiL

vcsup

VC,,,,

0.76 *

0.80 **

-0.74 *

FEI/,

0.83 **

BE -0.80 **

Paoz Paco2 Diff

dwSaoz nwSaoz

0.86 ***

0.98 ***

-0.87 ***

0.86 ***

0.99 ***

*p
during oxygen breathing in patient 3 was accompanied by an increase in calculated peak Pace, during sleep from 10.1 to 11.9 kPa. Since the ear oximeter overestimates Sao, in the low range (25), her arterial PO, was probably even lower than the calculated values, Thus, oxygen therapy was considered inadequate to treat nocturnal hypoxaemia in these three patients. They now use a respirator during sleep and are doing well with a considerable improvement

of blood gases during spontaneous breathing without supplemental

oxygen

during the daytime. Supplemental oxygen elevated the calculated Pao, to acceptable levels during sleep in patients 5,6 and 8. This was accompanied by a modest hypercapnia (range 8.3-8.8 kPa). Two of them are currently using oxygen at home.

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I

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Fig. 4. Calculated Pao, during supplemental oxygen breathing in six patients with scoliosis. Patients 1 and 2 were investigated on two different oxygen flows, the others on air and on oxygen. Patient 3 had no REM sleep

DISCUSSION The pulmonary artery pressure in patients with chronic obstructive pulmonary disease is related to mean Sao, during sleep, rather than to the number or depth of desaturation episodes (26). ‘Baseline’ (=daytime) Sao, is more important than episodic desaturations for the development of right heart failure in patients with sleep apnoea syndrome (27). Therefore, we used mean Sao, levels rather than episodic desaturations during sleep for the analyses. Since a Sao, below 90% invariably leads to an increased pulmonary artery pressure (28), we defined nocturnal hypoxaemia as mean Sao,<90% during sleep (all stages). The sleep pattern of our patients (Table II) cannot be taken as a true measure of sleep quality in scoliotics as the recording conditions were not designed for this purpose. We recorded only one night, so the ‘first night effect’, with short total sleeping time, many awakenings and low percentage of REM, could not be avoided. The low percentage of REM sleep in the group as a whole leads to an underestimation of the degree of nocturnal hypoxaemia, since REM sleep is associated with lower Sao, than non-REM sleep. Since the NH patients had a lower percentage of REM sleep than the non-NH patients, the difference in nocturnal oxygenation between the two groups is underestimated rather than overestimated. Daytime findings in NH patients

Daytime hypoxaemia and hypercapnia were the most constant findings in our scoliotics with NH. This resembles the situation in lung disease (l-3,29). One could expect the base excess to reveal hypoventilation more reliably than a single determination of Pace,, which

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may be falsely low due to the painful stimulus of the arterial puncture. However, in our study base excess did not provide more information than Pace,. The difference Pao,-Pace, could not separate NH patients from non-NH patients better than either Pao, or Pace, alone. This is probably due to the fact that Pao, and Pace, were closely interrelated (which should be the case if alveolar hypoventilation is the main determinator of daytime hypoxaemia); thus the difference Pao,-Pace, yields essentially the same information as Pao, or Pace, alone. We could confirm the observation of Mezon et al. (4) that nocturnal hypoxaemia in scoliotics is well related to a poor clinical condition. Five of our eight NH patients had suffered from RVF at least once and seven had been hospitalized because of respiratory problems. In our material, the paralytic scoliotics generally had less severe NH than the non-paralytic scoliotics. This is probably due to differences in the severity of scoliosis in our material (reflected in the difference in VC) but there may also be a ‘survival of the fittest’ effect in the post-polio patients. Mechanisms behind nocturnal hypoxaemia

Daytime hypoxaemia in scoliotics has been attributed to both diminished alveolar ventilation with hypercapnia and to gas exchange disturbances with an increased A-a 0, gradient (30,31). Our data are consistent with both mechanisms but favour the first. Hypoxaemia during sleep in severe lung disease has also been attributed to hypoventilation (1) as well as to an increased A-a gradient due to a decrease in FRC (32). The significant association between the fall in Sao, and rise in Ptcco, in our study suggests hypoventilation as the most important mechanism behind sleep-induced hypoxaemia in scoliotics. It should also be noted that several of our patients were better oxygenated sitting than supine. Changes in Sao, with posture can thus contribute to nocturnal hypoxaemia. Hypoventilation may be due to a primary defect in the respiratory regulation or to impaired ventilatory mechanics. All our patients had a regular breathing pattern during non-REM sleep. This makes a defective respiratory regulation unlikely. Impaired ventilatory mechanics seems more likely since the VC was lower and the fall in VC with posture was larger in NH patients than in non-NH patients. The fall in VC may be related to a partial diaphragmatic paralysis (33). Since we did not measure transdiaphragmatic pressure, we cannot quantify specifically the strength of the diaphragm. We found, however, no difference between paralytic and non-paralytic scoliotics. An impaired inspiratory muscle function in scoliotics independent of primary neurological disease has been shown by Lisboa et al. (34) The improvement of daytime blood gases from nocturnal respirator treatment in patients 2 and 3 is in accordance with previous experiences (35) and may be due to the fact that the respiratory muscles are allowed to rest (36) or to a ‘resetting’ of the chemoreceptors in the medulla at a lower Pace, level (37). Oxygen should be used with caution since there is a considerable risk of inducing severe hypercapnia during sleep. We did not find any patient with a pathological number of sleep apnoeas. This contrasts to the findings of Guilleminault et al. (5). The reason for this discrepancy is presumably that three of their five patients were specifically referred to their group because of sleeping complaints. In our experience, sleep apnoeas in patients with scoliosis is the exception rather than the rule. We suggest that the term ‘Quasimodo syndrome’, introduced by Guilleminault et al. to characterize scoliotic patients with hypoxaemia during sleep, should not be used. The

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hunchback of Notre Dame, as Victor Hugo (38) described him, was a young man (about 20 years) of great strength, active throughout the day and night, with no evidence of breathlessness or daytime hypersomnolence. This contrasts to the clinical picture of our middle-aged patients, suffering from muscle weakness, exertional dyspnoea and in some cases abnormal daytime sleepiness due to hypercapnia. CONCLUSION We conclude that nocturnal hypoxaemia in patients with scoliosis is usually not due to sleep apnoeas or primary defects in the regulation of breathing but to impaired ventilatory mechanics leading to hypoventilation. The patients are in most cases hypoxaemic already during the daytime. In borderline cases, nocturnal hypoxaemia should be suspected if there is daytime hypercapnia and if there is a fall in vital capacity with the supine posture. Nocturnal hypoxaemia should also be strongly suspected in patients with a previous history of right ventricular failure.

ACKNOWLEDGEMENTS We are thankful for financial support from Swedish National Association against Heart and Chest Diseases, The Swedish Association of Persons Disabled by Traffic Accidents and Polio, the Swedish Society of Medical Sciences, the Swedish Medical Association and the Swedish Medical Research Council (grant no. B86-04X-00084-22B). Laboratory technicians Giiran Randwall and Jeanette Persson and registered nurse Irmelin AndrCn have provided excellent technical help during the investigations. REFERENCES 1. Hudgel DW, Martin RJ, Capehart M, Johnson B, Hill P. Contribution of hypoventilation to sleep oxygen desaturation in chronic obstructive pulmonary disease. J Appf Physiol 1983;55:669-77. 2. Stradling JR, Lane DJ. Nocturnal hypoxaemia in chronic obstructive pulmonary disease. Cfin. Sci. 1983;64:213-22. 3. Midgren B, White T, Petersson K, Bryhn M, Airikkala P, Elmqvist D. Nocturnal hypoxemia and car pulmonale in severe chronic lung disease. Bull Eur Physiopath Resp 1985;21:527-33. 4. Mezon BL, West P, Israels J, Kryger M. Sleep breathing abnormalities in kyphoscoliosis. Am Rev Resp Dis 1980;122:617-21.

5. Guilleminault C, Kurland G, Winkle R, Miles LE. Severe kyphoscoliosis, breathing and sleep. The ‘Quasimodo’ syndrome during sleep. Chest 1981;79:626-30. 6. Catterall JR, Douglas NJ, Calverley PMA, et al. Transient hypoxemia during sleep in chronic obstructive pulmonary disease is not a sleep apnoea syndrome. Am Rev Resp Dis 1983;128:24-9. 7. Guilleminault C, Motta J. Sleep apnea syndrome as a long-term sequela of poliomyelitis. In: Guilleminault C, Dement, eds. Sleep apnea syndromes, New York: Liss Inc, 1978:309-U. 8. Hill R, Robbins AW, Messing R, Arora NS. Sleep apnea syndrome after poliomyelitis. Am Rev Resp Dis 1983;127: 129-31.

9. Linderholm H, Werneman H. On respiratory regulation in poliomyelitis convalescents. Acta Med Scand 1956;316(suppl.):135-57.

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10. Plum F, Swanson AG. Abnormalities in central regulation of respiration in acute and convalescent poliomyelitis. AMA Arch Neurol Psychiat 1958;80:267-85. 11. Hamilton EA, Nichols PJR, Tait GBW. Late onset of respiratory insufficiency after poliomyelitis. Ann Phys Med 1970;10:223-9. 12. Lane DJ, Hazleman B, Nichols PJR. Late onset respiratory failure in patients with previous poliomyelitis. Q J Med 1974;172:551-68. 13. Solliday NH, Gaensler EA, Schwaber JR, Parker TF. Impaired central chemoreceptor function and chronic hypoventilation many years following poliomyelitis. Case report. Respiration 1974;31: 177-92. 14. Berglund E, Birath G, Bjure J, et al. Spirometric studies in normal subjects. I: Forced expirograms in subjects between 7 and 70 years of age. Acta Med Stand 1963;173:185-92. 15. West JB. Ventilation/bloodflow and gas exchange, 3rd ed. Oxford: Blackwell Scientific Publications, 1977:103. 16. Douglas NJ, Brash HM, Wraith PK, et al. Accuracy, sensitivity to carboxyhaemoglobin and speed of response of the Hewlett-Packard 47201A ear oximeter. Am Rev Resp Dis 1979;119:311-13. 17. Chapman KR, D’Urzo A, Rebuck AS. The accuracy and response characteristics of a simplified ear oximeter. Chest 1983;83:860-4. 18. Tweedale PM, Douglas NJ. Evaluation of Biox IIA ear oximeter. Thorax 1985;40:825-7. 19. Rechtschaffen A, Kales A. A manual of standardized terminology, techniques and scoring systemsfor sleep stages. BIS/BRI Los Angeles: UCLA, 1968. 20. Stradling JR, Nicholl CG, Cover D, Highes JMB. Speed of response and accuracy of two transcutaneous carbon dioxide monitors. Bull Eur Physiopath Resp 1983;19:407-10. 21. Midgren B, Airikkala P, Ryding E, Elmqvist D. Transcutaneous COZ monitoring and disordered breathing during sleep. Eur J Resp Dis 1984;65:521-8. 22. Philipson L, Risberg AM, Ingvar DH. Normal sleep pattern analyzed statistically and studied by color ‘dormograms’. Sleep 1980;2:437-51. 23. Smyth RJ, Chapman KR, Rebuck AS. Maximal inspiratory and expiratory pressuresin adolescents. Normal values. Chest 1984;86:568-72. 24. Kelman GR, Nunn JF. Nomograms for correction of blood PO*, PCO*, pH, and base excessfor time and temperature. J Appl Physiol1966;21: 1484-90. 25. Chapman KR, Liu FLW, Watson RM, Rebuck AS. Range of accuracy of two wavelength oximetry. Chest 1986;89:540-2. 26. Sautegeau A, Hannhart B, Btgin P, Polu JM, Schrijen F. Pression artCrielle pulmonaire basale diurne et niveau nocturne d’oxygCnation chez les bronchitiques chroniques (Diurnal pulmonary artery pressure and nocturnal oxygenation level in chronic bronchitis). Bull Eur Physiopath Resp 1984;20:541-5. 27. Bradley TD, Rutherford R, Grossman RF, et al. Role of daytime hypoxemia in the pathogenesis of right heart failure in the obstructive sleep apnea syndrome. Am Rev Resp Dis 1985;131:835-9. 28. Ferrer MI. Management of patients with car pulmonale. Med Clins NAm 1979;63:251-65. 29. Conway W, Kryger M, Timms R, Williams G. Hypercarbia predicts nocturnal desaturation in COPD (abstract). Am Rev Resp Dis 1982;125(suppl.):lOO. 30. Kafer ER. Respiratory function in paralytic scoliosis. Am Rev Resp Dis 1974;110:450-7. 31. Kafer ER. Respiratory and cardiovascular functions in scoliosis. Bull Eur Physiopath Resp 1977;13:299-321. 32. Hudgel DW, Devadatta P. Decrease in functional residual capacity during sleep in normal humans. J Appl Physiol1984;57:1319-22. 33, Allen SM, Hunt B, Green M. Fall in vital capacity with posture. BrJ Dis Chest 1985;79:267-71.

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34. Lisboa C, Moreno R, Fava M, Ferretti R, Cruz E. Inspiratory muscle function in patients with severe kyphoscoliosis. Am Rev Resp Dis 1985;132:48-52. 35. Hoeppner VH, Cockcroft DW, Dosman JA, Cotton DJ. Nighttime ventilation improves respiratory failure in secondary kyphoscoliosis. Am Rev Resp Dis 1984;129:240-3. 36. Braun NMT, Faulkner J, Hughes RL, Roussos C, Sahgal V. When should respiratory muscles be exercised? Chest 1983;84:76-84. 37. Kinnear WJM, Shaw DG, Jones DK, Higenbottam T, Shneerson JM. The ventilatory response to carbon dioxide before and after assisted ventilation in patients with neuromuscular and skeletal chest wall disease (abstract). Proceedings of the SEPISEPCR, Paris 1986:1628. 38. Hugo V. Notre-Dame de Paris (Hunchback of Notre Dame), 1831.

Date accepted 22 June 1987