Severe Pleural Restriction: The Maximum Static Pulmonary Recoil Pressure as an Aid
in Diagnosis* Charlotte Colp, M.D., F.C.C.P.,"* Joseph Reiche2, M.D.,? and Sung Suh Park, M.D.?
Three patients with pleural restriction are presented in detail. One patient had had a right pneumonectomy and died of ventilatory failure due to left-sided restrictive pleurisy. The second patient had neoplastic pleural effusion and inactive tuberculosis. The third patient had systemic lupus erythematmus with bilateral restrictive pleurith The physiologic picture was similar in the three cases, with marked decrease of lung volumes, increase of the RV/TLC ratio, absence of airways obstruction, de-
crease of the Dco and decrease of dynamic lung compliance. In addition, each of these three patients and others with severe pleural restriction had a lower than normal maximum static pulmonary recoil pressure (Pmax). Since in pulmonary restrictive disease, the Pmax was found to be elevated, it was a useful test for distinguishing pulmonary restrictiw from pleural restriction.
enerally, pleural disease leads to restrictive venUatory impairment with moderate reduction of lung volumes. But in three patients we have found severely disabling respiratory restriction due primarily to pleural involvement; one of these patients developed ventilatory failure on this basis. In no case was ventilatory impairment due to uncomplicated unilateral pleural restriction. The first patient had had a right pneumonectomy; this patient died, and pathologic examination showed restrictive pleurisy on the left, with little disease of the underlying lung. The second patient had inactive tuberculosis, mainly on the left, then developed severe rightsided pleural thickening due to neoplastic effusion. The third patient had bilateral pleurisy due to systemic lupus erythematosis. A clue to the diagnosis of pleural restriction was noted which may most-useful in differentiating pleural restriction from restrictive disease of the lung: the static pulmonary recoil pressure on full inspiration (Pmax) was less than normal.
The Pmax is a measure of the elastic recoil force of the lung at total lung capacity. It is decreased in emphysema. Of those conditions which cause reduction of the total lung capacity (ie, restrictive diseases) parenchymal pulmonary fibrosis will increase Pmax, whereas extrapulmonary causes of restriction may reduce it. Our three patients had reduction of lung volume and Pmax on repeated evaluation. In the absence of other causes of extrapulmonary restriction such as chest wall deformity, severe obesity, or muscle weakness, pleural disease was felt to be the cause of the clinical disability and reduction of Pmax.
'From the Pulmonary Division, Department of Medicine, Albert Einstein College of Medicine and the Chest Service, Department of Medicine Bronx Municipal Hospital Center, ~ r k NY , "Associate Clinical Professor of Medicine. tAssociate Professor of Medicine. This study was supported in art by a Public Health Service Pulmonary Academic ~ w a r c f(no. 5 KO 7 HL 70,076 01 ) from the National Heart and Lung Institute and by Cardiopulmonary Renal Program HE 13979-01. ted September 30. Manuscript received July 22; revision a College oj Reprint requests: LIT. Reichel, ~ l b e r smtein ty Medicine Eastchester Road and Morris Park Aoenue, Bronx, New ~ o r k10461
658 COLP, REICHEL, PARK
Pulmonary function tests were performed by our usual methods. Predicted normal values for lung.volumes are taken from Bates and Christie.' For measurements of lung mechanics2 the patient swallows a 10 x 1 cm esophageal balloon into which is introduced 0.7 ml of air. The balloon is placed at the lower portion of the esophagus. The Pmax is the airway opening-esophageal pressure gradient recorded on a strain gauge during full inspiration with the glottis open. The airway opening pressure at end inspiration is atmospheric pressure. Normal prediction for Pmax is based on our own unpublished data obtained in 23 normal healthy subjects including men and women with ages varying from 18 to 64 years. It is independent of the height of the subjects but varies with age. The prediction formula is: Pmax = 32 - .22x age, - with a standard error of estimate = 3.0 crn H20. Adequate patient effort and full cooperation are essential in performing the test. Predicted lung compliance is based on data of Frank et al.3
CHEST, 67: 6, JUNE, 1975
Accordingly, the patient was admitted to the hospital for evaluation of her previously inactive tuberculosis. On physical examination, the patient was a slightly obese woman (162.5 cm,66.9 kg), dyspneic at rest. The trachea was deviated to the right. There was a right thoracotomy scar. Flatness to percussion and absent breath sounds were noted in the right hemithorax. There was some dullness and diminution of breath sounds at the left base. There was no edema, clubbing or neck vein distention. Chest x-ray 6lm examination showed opacification of the right hemithorax, with shift of the mediastinurn to the right. There was an opacity at the left base which was felt to represent either pleural disease or parenchymal infiltration or fibrosis. An ECG showed prominent P waves in leads 1,2 and aVF. Results of sputum examinations for tubercle bacilli were negative. The patient had chronic hypoventilation, with an arterial oxygen saturation of 87 percent and arterial carbon dioxide pressum ( PaCOz) of 60 mm Hg. Pulmonary function studies performed in September 1964 (Table 1 ) showed a marked reduction of lung volumes. The vital capacity was only 0.6 liters, and the total lung capacity (TLC) was 1.08 liters (predicted = 5.0 liters). The residual volume (RV) was reduced, but not as much as the TLC, so that the RV/TLC ratio was 44 percent. There was no evidence of airways obstruction. The dynamic compliance was markedly reduced. However, the maximum static pulmonary recoil pressure was less than predicted for the patient's age. The diagnosis of pulmonary fibrosis was made and the patient was treated with methylprednisolone (Medrol) and antituberculosistherapy. She was discharged for care at home in April, 1965. Repeated studies of pulmonary function in July, 1965 gave the same results. The diffusing capacity for carbon monoxide by the steady state method (Dco SS) was measured on this occasion and was markedly reduced. Evaluation of the maximid respiratory muscle force (maximal static inspiratory and expiratory mouth pressure) showed normal muscle strength, with values of 160-220 cm Hz0 during expiratory effort and -110 cm Hz0 during inspiratory effort. The patient's subsequent course was marked by progressive cardiorespiratory failure with asterixis, somnolence, signs of right-sided congestive heart failure, hypoxemia and hypercapnea and finally death on Feb 13,1966. An autopsy was performed. Gross examination of the respiratory system confirmed that the right lung was absent
FIGURE1. (case 1 ) Status after right pneumonedomy. Note hazy opacity at left base, due to pleural thickening. Serial chest x-rays films during patient's illness showed no change.
This 33-year-old nurse was admitted to the hospital initially in October, 1964 with progressive shortness of breath of 11 years' duration. The diagnosis of tuberculosis was made in 1950 at which time the patient was treated for three years with antituberculosis chemotherapy followed by a right phrenic crush and a segmental resection. Ultimately, a right pneumonedomy was performed, with clinical improvement. Between 1953 and 1964 there was progressive shortness of breath. One month prior to admission, a chest x-ray film (Fig 1 ) showed a ''hazy infiltrate" at the left base, which was not previously noted. Table 1-Pulmonary Case Na.
DL.gnmis
luaia Pcol Dab
mm Hg
Function Data o f Three Patienu with Semere Pleural Re~riction D m
Meri.l SB (1) 01 kt..% ml/mm/mi.
VC
TLC
RV
88 (2) Litera (3) Lib (4) Litas (6)
RV/TLC FEVI% MMF Cdyn % FVC (6) Litera/wc.(7) Litsn/cmH10(8)
Pmu
&(9)
1
Pneumnnectomy. d c t . pleurisy 2 Old TB. Mali&. pleural d e t . 3 SLE --
--
-
- ---
-
1 Carbon monoxide diffusing u p c i t y single bath m e t h o d - n d d u e hrd on au data. 2 Carbon monoxide diffusing capacity l t a d y state d - - a d valua.1 3 Vital capacity (litem) nwmal value.' 4 Total lung mpscity (litera) n d due.' S Residual vdume (litera) normal d u e . '
CHEST, 67: 6, JUNE, 1975
6 One k w o d timed riW apcity-nornrl>75
percent. 7 Muimum midexpintury Bor rite-nand >O.7 I vibl u p c i t y . 8 Dylumic lw c o m p l b n c e - n d dues.* 9 Muimum pllmmvy rscdl p m a m - n d d u e -.33 x ye
-
+3 2
SEVERE PLEURAL RESTRICTION 659
due to removal at operation. The left lung specimen weighed
550 gm and the left parietal pleura was extensively thick-
ened, greyish-white and opaque. In several areas, the pleura measured as much as 0.9 cm in thickness. Pleural adhesions were extensive and involved both the diaphragmatic, mediastinal and costal aspects of the lungs. The adhesions were fairly easily removable. However, a 3 x 5 cm area on the costal as@ of the left upper lobe was adherent to the underlying pleura and sharp dissection was required to remove it. There was no evidence of granulomatous disease in the pleura. The configurations of the upper and lower lobes of the left lung were normal, and the cross sections revealed remarkably well preserved parenchymal patterns with minimal dilatation of bronchi and bronchioles. Microscopic examination of the pleura showed hyalinized, laminated almost acellular fibrous tissue, with multiple foci of calcification. The cause of death was felt to be respiratory failure secondary to left-sided pleural restriction in a patient who had had a right pneumonectomy. Her clinical course during the two years prior to death was believed to be one of progressive ventilatory failure due to end-stage parenchymal restrictive lung disease. At autopsy, to our surprise, this clinical diagnosis was not verified. The patient's left lung was found to be free of fibrosis, and the major cause of ventilatory failure was pleural restriction. The fact that the patient's Pmax was not greater than normal, in the absence of thoracic muscle weakness, chest wall deformity or obesity, pointed to pleural restriction rather than parenchymal fibrosis as the cause of ventilatory failure.
FIGURE3. (case 2 ) Note large right pleural effusion (Feb. 3, 1972).
This patient is a 62-year-old white woman who had pulmonary tuberculosis in the 1930's. The tuberculosis became inactive on bedrest, and x-ray films of the chest taken from 1956 to 1966 showed a stable lesion, with some fibrosis of both upper lobes and the left lower lobe ( Fig 2 ) . The patient
had no respiratory disability and was able to carry out her household duties. In January, 1972, the patient became ill wi& severe dyspnea over a one-week period. Physical examination a t this time revealed marked dullness and diminished breath sounds over the right posterior side of the chest. A chest roentgenogram taken Feb 3, 1972 confirmed the suspicion of a large
FIGURE 2. (case 2 ) Inactive tuberculosis is obvious, more marked on left ( roentgenogram taken 1966 ) .
FIGURE 4. (case 2) Pleural thickening fs shown on right ( May 30,1972 ) .
880 CILP, REICHEL, PARK
CHEST, 67: 6, JUNE, 1975
right pleural effusion (Fig 3). Thoracentesis and pleural biopsy confirmed the diagnosis of adenocarcinoma. Them was no evidence of a primary tumor in the lung, and on pelvic examination a small mass was noted which was thought to represent a primary ovarian tumor. Following the first thoracente-sis, two additional thoracenteses were performed over a two-week period. Subsequently, although neither radiotherapy nor chemotherapy were given, fluid did not reaccumulate, and the patient was left with residual pleural thickening as manifested by unchanging findings on chest x-ray film (Fig 4 ) for many months. During the three months following hospitalization, the patient noted progressive exertional dyspnea. The dyspnea became progressively worse for approximately two months, thenceforth remaining stable. On physical examination there remained considerable decrease of breath sounds over the right lower hemithorax. As in the past, scattered rilles were heard over the left lower lobe, and were attributed to bronchiectasis following tuberculosis. Pulmonary function studies were performed for the first time in July. 1972 (Table 1). As in the first case, the studies showed impairment of restrictive type with vital capacity of 0.85 liters. Results of lung studies again showed a very low compliance, but the Pmax was definitely below the predicted normal level for the patient's age. A lung perfusion scan showed a moderate decrease in perfusion of the right lower lobe, the left lower lobe and the left upper lobe. This patient, whose health was previously unimpaired, developed severe respiratory disability following unilateral neoplastic pleural involvement. Presumably, the unilateral deural involvement caused severe functional im~airment because the other lung was involved to a major degree by previous tuberculosis. While lymphangitic spread of carcinoma was initially considered as a cause of the patient's severe dyspnea, this diagnosis seems unlikely because the patient's condition did not progress clinically nor did lymphangitic carcinoma become apparent radiologically after several months of observation. Further, ovarian carcinoma rarely causes pulmonary lymphangitic carcinomatosis.
The patient is a 28-year-old Negro woman who initially presented in March. 1971 with severe chest pain and shortness of breath. The patient had noted diffuse arthralgias for one year. There was redness and swelling of the right knee and elbow for several weeks. For three weeks, she had bilateral chest pain and dyspnea. These symptoms had become progmssively more severe until the time of admission to the hospital. On physical examination the patient was febrile (38.9 C) and had dullness and decreased breath sounds at both bases, with a pleuropericardial friction rub over the left anterior hemithorax. There was evidence of arthritis as noted above. Chest roentgenograms showed bilateral pleural reaction ( Fig 5 ), with linear streaking at both bases. The findings on e l d o g r a m were consistent with findings in pencarditis. The suspected diagnosis of lupus erythematosus was confirmed by a strongly positive lupus erythematosus test'and a positive fluorescent antinuclear antibody study. Pulmonary function studies (Table 1) showed again restrictive impairments similar to those seen in cases 1 and 2, with a vital capacity of 0.8 liters. Results of lung studies showed a marked reduction of compliance; however, the Pmax was distinctly below normal. The patient was treated with prednisone, beginning with a dose of 40 mg daily. There was rapid and marked improve-
CHEST, 67: 6, JUNE, 1975
FIGURE5. (case 3) Bilateral pleural disease is obvious. ment, with relief of chest pain, dyspnea and other symptoms. Followup chest roentgenograms showed clearing of the pleuritis and infiltrates. In spite of clearing, the lungs were persistently small roentgenographically. Comparison of differential lung function bilaterally by the densigraphic method showed that both diaphragms moved and the vital capacity was symmetrically reduced bilaterally. The patient has been observed for wer one year, with gradual tapering of the dosage of prednisone to one tablet daily. Her condition remains stable, with no evidence of relapse of the original inflammatory process. Followup pulmonary function studies showed improvement within one month of treatment, with little change since then. A representative study is listed in the Table. The vital capacity has more than doubled, but is still far from normal. The TLC and residual volume have also increased so that the RV/TLC ratio remains slightly elevated. The single breath diffusing -capacity is also reduced, but not as much as the TLC, so that the diffusion to volume ratio is actually higher than normal, suggesting that interstitial fibrosis is not the cause of the patient's marked impairment of Wusion. Finally. although lung compliance has increased somewhat, the Pmax remains quite reduced. On the basis of these findings, the patient is felt to be suffering from considerable residual pleural fibrosis due to lupus erythematosus. Decortication has not been recommended because of the bilateral nature of the Drocess and because of our uncertaintv concerning how a Gtient with lupus erythematosus w o i d tolerate such an operation.
All three patients had marked reduction of vital capacity and slight or moderate reduction of residual volume. Since the total lung capacities were all quite decreased, the RVITLC ratios were increased in all patients. The patient with one lung had more reduction of volumes than the other patients. A low maximal midexpiratory flow rate (MMF) SEVERE PLEURAL RESTRICTION 661
was found in our patients and is explained by reduction of the vital capacity, for the normal timed vital capacities indicate the absence of airways obstruction. The diffusing capacity (Dco) was markedly reduced in all three patients. Arterial blood gas analyses showed hyperventilation and maintenance of normal or fairly normal oxygenation in two of our patients. Patient No. 1, who had the most severe mechanical ventilatory defect, developed chronic hypoventilation and arterial desaturation prior to her death. Chest wall compliance was not measured, but lung compliance was markedly reduced in all three patients. Also, the maximum static pulmonary recoil pressure was slightly lower than predicted in all three patients. We have reviewed all the Pmax measurements performed in our laboratory on patients with pleural disease and, for comparison, on patients with interstitial lung disease ( including sarcoidosis) who had total lung capacities of less than 80 percent of predicted. There were only 7 cases of uncomplicated pleural disease, but there were 61 cases of interstitial disease. In the former group, the Pmax ranged from 7-23, in the latter from 12-62 crn HzO.
I
I
PULMONARY FIBROSIS
A OTHER
CURRENT)
PLEURAL DISEASE
% PREDICTED TLC
FIGURE 6.Graph of Pmax (as percent of predicted) vs TLC (percentage of predicted) in patients with pulmonary fibrosis and pleural disease. Solid and broken lines represent regression line and one tail 95 percent confidence limit, respectively, for group of patients with pulmonary fibrosis. Regression formula, correlation coefficient ( r ), and Pvalue are: log Prnax (percentage predicted) = 2.45 - 0.59 x TLC (percentage predicted ) r = .34 P = 0.01
662 COLP, REICHEL, PARK
The relationship between the Pmax and the total lung capacity in all of the patients is shown in Figure 6. There was a wide range of variation of the Pmax in relation to the TLC, and its distribution along the regression line was skewed. Semilogarithmic plotting normalized this distribution. In four of seven cases of pleural restriction, the Pmax was well below the 95 percent confidence limits for pulmonary fibrosis cases. In two other cases, the Pmax was at the 95 percent confidence limit. Only one patient with pleural disease had a Pmax within the range expected for patients with pulmonary fibrosis.
Results of pulmonary function studies were remarkably similar in the three patients reported here. All had marked decrease of lung volumes. The findings of increase of the RV/TLC ratio in these patients (who were free of airways obstructive disease) are in accord with the usual findings in pleural disease4 and in normal subjects following chest trapping,^ and this seems to be generally characteristic of chest wall restriction or muscle weakness in which the residual volume is minimally affected but there is marked inability to expand the chest. All three patients had marked reduction of the Dco, probably due mainly to the marked reduction of lung volumes. The second patient was known to have some fibrosis of the lung due to tuberculosis, probably accounting in part for her reduction of Dco. In the third patient, with systemic lupus erythernatosus, the single breath Dco, performed at the time of followup study when she had improved with therapy but was still severely restricted, was about one-half normal. This reduction of Dco was not as great as the reduction of the total lung capacity at the time. The Dco is volume dependent and Yoo4 found, in patients with pleural disease, reduction of approximately the same magnitude as the reduction of the total lung capacity. On the other hand, in patients with diffuse interstitial pulmonary fibrosis, the Dco is almost always more reduced than are the lung volume^.^ Therefore, in this patient with lupus erythematosus, the relatively well preserved Dco lends further support to the impression that she does not have d i k e interstitial fibrosis and that her restriction is due to chronic pleuritis. In keeping with this interpretation are the findings of Huang and Lyons7 who compared pulmonary function data in patients with systemic lupus erythematosus and sclerodenna. In systemic lupus erythematosus, particularly in patients with known pleural involvement, the lung volumes were relatively more CHEST, 67: 6, JUNE, 1975
affected than the Dco. In contrast, patients with scleroderma, in whom diffuse interstitial fibrosis of the lung is the usual pathology, had better preservation of lung volumes but more marked reduction of the Dco. Perhaps the most significant findings in our three patients with severe restrictive pleurisy are the measurements of lung mechanics, which revealed a reduction of the maximal static p u b n a r y recoil pressure in the presence of severe reduction of lung compliance. The Pmax is affected by the recoil properties and degree of expansion of the lung. Factors affecting the latter include muscle strength, cooperation and the presence or absence of diseases of the pleura and the chest wall. Extrapulmonary factors which limit expansion of the lung will result in a decreased maximum static pulmonary recoil pressure. For example, in three of four patients studied in our laboratory with severe restriction due to kyphoscoliosis, the Pmax was slightly less than normal. The Pmax was similarly reduced in 13 of 17 patients with severe obesity. Also, inspection of static pressurevolume graphs in obese patients studied by Naimark and Cherniack8 indicates maximum transpulmonary pressures lower than found in their normal controls. Although the reduction of Pmax in the presence of volume restriction may be considered characteristic of extrapulmonary restriction, the fact that the reduction of Pmax is less than that of lung volume and the reduction of lung compliance was out of proportion to the reduction of lung volumes re~uires explanation. Do the findings suggest the possibility that these patients have coexisting pulmonary fibrosis? The fact that mechanical alterations of similar type were documented in normal subjects who had a tight rubber binder acutely applied to the thorax5 tends to deny such a possibility. In these subjects the lung volumes were reduced. As in our patients with pleural disease, the reduction of lung compliance was even more marked than the reduction of lung volumes. The transpulmonary pressure at any given volume was greater than before chest binding, but the maximum transpulmonary pressure ( Pmax ) was a little lower than in the normal state. Presumably, the chest binding causes closure of terminal airspaces which tend to decrease the lung compliance, and increase the lung recoil for a given volume. Such changes of lung mechanics would be even more pronounced at the lower volume level of our patients, where a greater number of terminal lung units may remain closed. The Pmax under these conditions would be affected by two opposing influences. On the one hand, the restriction of maximal inflation tends to reduce the Pmax. On the other CHEST, 67: 6, JUNE, 1975
hand, the closure of terminal lung units tends to increase the Pmax. Because of the balance of these opposing influences, the reduction of Pmax will be relatively less than the reduction of lung volume and of compliance. Thus, the relatively moderate reduction of Pmax in the presence of marked reduction of lung compliance observed in our patients with pleural disease may be largely accounted for by the closure of terminal lung units due to severe volume restriction. Indeed, postmortem examination of the lung revealed no significant parenchymal fibrosis in the first case despite a marked decrease of dynamic lung compliance noted during life. On the other hand, in pulmonary fibrotic disease, elevation of the maximum transpulmonary pressure has been well is again c o n h e d here, and is do~umented,~.'~ presumably due to the increased recoil force of the lung. Of course, there may be artefacts in the Pmax measurement; esophageal balloon pressure may not necessarily reflect true pleural pressure when there is extensive pleural disease. The relation between esophageal pressure and the pleural pressure of each pleural cavity when there is unilateral pleural restriction is not known. The possible effect of lung resection, especially pneumonectomy, on the Pmax is uncertain.' Despite these possible artefacts, the slightly low Pmax of pleural disease when found in conjunction with severe volume restriction appeared useful in these cases as a diagnostic aid in differentiating pleural restriction from fibrosis of the lung itself. This is a distinction of great practical importance because, although not used in any of our patients, decortication has been documented to be of therapeutic value in restrictive p l e ~ r i t i s . ' ~ , ~ ~ It is of interest that ventilatory failure, which is rare in fibrosis of the lung, occurred in our patient (who had had a pneumonectomy) with the most severe pleural resthction. ventilatory failure has not been reported in pleural disease alone but is a well known occurrence in other forms of severe extrapulmonary restriction with low Pmax such as kyph~scoliosis,'~ muscle weakness and obesity.
1 Bates DV, Macklem PT,Christie RV: Respiratory Function in Disease ( chap 2 ) . Philadelphia, WB Saunders Co,
1971 2 Ting EY, Williams Jr MH: The mechanics of breathing in chronic obstructive pulmonary disease. Am Rev Resp Dis
*Review of all Pmax determinations available to us after pneumonectomy revealed hi er than normal values in five atients, three of whom c early had pulmonary fibrosis, an3 a low value in one atient thought to have emphysema. Data were available begre and after operation in only one patient with cancer of the lung; his Pmax after pneurnonectomy was higher than the value before operation.
t'
SEVERE PLEURAL RESTRICTION 663
88:791, 1963 3 Frank NR, Mead J, Siebans AA, et al: Measurement of pulmonary compliance in 70 healthy young adults. J Appl Physiol9:38, 1956 4 Yoo OH, Ting EY: The effects of pleural effusion on pulmonary function. Am Rev Resp Dis 89:55, 1964 5 Cam CG, Butler J, DuBois AB: Some effects of restriction of chest cage expansion on pulmonary function in man: An experimental study. J Clin Invest 39:573, 1960 6 Colp C, Riker J, Williams MH Jr: Serial changes in lung function in scleroderma and idiopathic interstitial lung disease.Arch Intern Med 132:506, 1973 7 Huang CX,Lyons HA: Comparison of pulmonary function in patients with systemic lupus erythematosus, scleroderma and rheumatoid arthritis. Am Rev Resp Dis 93:885, 1966 8 Naimark A, Cherniack RM: Compliance of respiratory
system and components in health and obesity. J Appl Physiol 15:377, 1960 9 Ting EY, Williams Jr MH: Mechanics of breathing in sarcoidosis of the lung. JAMA 192:123, 1985 10 Macklem PT, Becklake MR: The relationship between the mechanical and diffusing properties of the lung in health and disease. Am Rev Resp Dis. 87:47, 1963 11 Petty TL, Filley GF, Mitchell RS: Objective functional improvement by decortication after 20 years of artificial pneumothorax for pulmonary tuberculosis. Am Rev Resp Dis 84:572, 1981 12 Siebens AA, Storey CF, Newman MM, et al: The physiologic effects of fibrothorax and the functional results of surgical treatment. J Thorac Surg 32:53, 1956 13 Bergofsky EH, Turino GM, Fishrnan AP: Cardiorespiratory failure in kyphoscoliosis. Medicine 38:283, 1959
Giacomo Puccini (1858-1924) "Puccini looks to me more like the heir of Verdi than any of his rivals." That was the verdict of a young London music critic called Bernard Shaw in 1894-a verdict made, remarkably, on the evidence only of Puccini's first successful opera, Manon Lescaut (1893). Shaw pointed to Puccini's combination of symphonic style (that is, a style of continuously developing music, like Wagner's) with a vein of traditional Italian melody. Puccini thereafter turned out a chain of operatic successes unequaled since his day. He pursued and ex-
664 COLP, REICHEL, M R K
tended this symphonic method; he extended also his range of poignant and biting harmonies, learning from Debussy as well as Wagner. Dramatically he cared little for subtlety of character but much for the power of erotic and brutal impulses seen or suggested on the stageimpulses which are powerfully suggested in the high points of his music. Jacobs A and Sadie S: Opera-A Modem Guide. New York, Drake Publishers, 1972
CHEST, 67: 6, JUNE, 1975
in Diagnosis* Charlotte Colp, M.D., F.C.C.P.,"* Joseph Reiche2, M.D.,? and Sung Suh Park, M.D.?
Three patients with pleural restriction are presented in detail. One patient had had a right pneumonectomy and died of ventilatory failure due to left-sided restrictive pleurisy. The second patient had neoplastic pleural effusion and inactive tuberculosis. The third patient had systemic lupus erythematmus with bilateral restrictive pleurith The physiologic picture was similar in the three cases, with marked decrease of lung volumes, increase of the RV/TLC ratio, absence of airways obstruction, de-
crease of the Dco and decrease of dynamic lung compliance. In addition, each of these three patients and others with severe pleural restriction had a lower than normal maximum static pulmonary recoil pressure (Pmax). Since in pulmonary restrictive disease, the Pmax was found to be elevated, it was a useful test for distinguishing pulmonary restrictiw from pleural restriction.
enerally, pleural disease leads to restrictive venUatory impairment with moderate reduction of lung volumes. But in three patients we have found severely disabling respiratory restriction due primarily to pleural involvement; one of these patients developed ventilatory failure on this basis. In no case was ventilatory impairment due to uncomplicated unilateral pleural restriction. The first patient had had a right pneumonectomy; this patient died, and pathologic examination showed restrictive pleurisy on the left, with little disease of the underlying lung. The second patient had inactive tuberculosis, mainly on the left, then developed severe rightsided pleural thickening due to neoplastic effusion. The third patient had bilateral pleurisy due to systemic lupus erythematosis. A clue to the diagnosis of pleural restriction was noted which may most-useful in differentiating pleural restriction from restrictive disease of the lung: the static pulmonary recoil pressure on full inspiration (Pmax) was less than normal.
The Pmax is a measure of the elastic recoil force of the lung at total lung capacity. It is decreased in emphysema. Of those conditions which cause reduction of the total lung capacity (ie, restrictive diseases) parenchymal pulmonary fibrosis will increase Pmax, whereas extrapulmonary causes of restriction may reduce it. Our three patients had reduction of lung volume and Pmax on repeated evaluation. In the absence of other causes of extrapulmonary restriction such as chest wall deformity, severe obesity, or muscle weakness, pleural disease was felt to be the cause of the clinical disability and reduction of Pmax.
'From the Pulmonary Division, Department of Medicine, Albert Einstein College of Medicine and the Chest Service, Department of Medicine Bronx Municipal Hospital Center, ~ r k NY , "Associate Clinical Professor of Medicine. tAssociate Professor of Medicine. This study was supported in art by a Public Health Service Pulmonary Academic ~ w a r c f(no. 5 KO 7 HL 70,076 01 ) from the National Heart and Lung Institute and by Cardiopulmonary Renal Program HE 13979-01. ted September 30. Manuscript received July 22; revision a College oj Reprint requests: LIT. Reichel, ~ l b e r smtein ty Medicine Eastchester Road and Morris Park Aoenue, Bronx, New ~ o r k10461
658 COLP, REICHEL, PARK
Pulmonary function tests were performed by our usual methods. Predicted normal values for lung.volumes are taken from Bates and Christie.' For measurements of lung mechanics2 the patient swallows a 10 x 1 cm esophageal balloon into which is introduced 0.7 ml of air. The balloon is placed at the lower portion of the esophagus. The Pmax is the airway opening-esophageal pressure gradient recorded on a strain gauge during full inspiration with the glottis open. The airway opening pressure at end inspiration is atmospheric pressure. Normal prediction for Pmax is based on our own unpublished data obtained in 23 normal healthy subjects including men and women with ages varying from 18 to 64 years. It is independent of the height of the subjects but varies with age. The prediction formula is: Pmax = 32 - .22x age, - with a standard error of estimate = 3.0 crn H20. Adequate patient effort and full cooperation are essential in performing the test. Predicted lung compliance is based on data of Frank et al.3
CHEST, 67: 6, JUNE, 1975
Accordingly, the patient was admitted to the hospital for evaluation of her previously inactive tuberculosis. On physical examination, the patient was a slightly obese woman (162.5 cm,66.9 kg), dyspneic at rest. The trachea was deviated to the right. There was a right thoracotomy scar. Flatness to percussion and absent breath sounds were noted in the right hemithorax. There was some dullness and diminution of breath sounds at the left base. There was no edema, clubbing or neck vein distention. Chest x-ray 6lm examination showed opacification of the right hemithorax, with shift of the mediastinurn to the right. There was an opacity at the left base which was felt to represent either pleural disease or parenchymal infiltration or fibrosis. An ECG showed prominent P waves in leads 1,2 and aVF. Results of sputum examinations for tubercle bacilli were negative. The patient had chronic hypoventilation, with an arterial oxygen saturation of 87 percent and arterial carbon dioxide pressum ( PaCOz) of 60 mm Hg. Pulmonary function studies performed in September 1964 (Table 1 ) showed a marked reduction of lung volumes. The vital capacity was only 0.6 liters, and the total lung capacity (TLC) was 1.08 liters (predicted = 5.0 liters). The residual volume (RV) was reduced, but not as much as the TLC, so that the RV/TLC ratio was 44 percent. There was no evidence of airways obstruction. The dynamic compliance was markedly reduced. However, the maximum static pulmonary recoil pressure was less than predicted for the patient's age. The diagnosis of pulmonary fibrosis was made and the patient was treated with methylprednisolone (Medrol) and antituberculosistherapy. She was discharged for care at home in April, 1965. Repeated studies of pulmonary function in July, 1965 gave the same results. The diffusing capacity for carbon monoxide by the steady state method (Dco SS) was measured on this occasion and was markedly reduced. Evaluation of the maximid respiratory muscle force (maximal static inspiratory and expiratory mouth pressure) showed normal muscle strength, with values of 160-220 cm Hz0 during expiratory effort and -110 cm Hz0 during inspiratory effort. The patient's subsequent course was marked by progressive cardiorespiratory failure with asterixis, somnolence, signs of right-sided congestive heart failure, hypoxemia and hypercapnea and finally death on Feb 13,1966. An autopsy was performed. Gross examination of the respiratory system confirmed that the right lung was absent
FIGURE1. (case 1 ) Status after right pneumonedomy. Note hazy opacity at left base, due to pleural thickening. Serial chest x-rays films during patient's illness showed no change.
This 33-year-old nurse was admitted to the hospital initially in October, 1964 with progressive shortness of breath of 11 years' duration. The diagnosis of tuberculosis was made in 1950 at which time the patient was treated for three years with antituberculosis chemotherapy followed by a right phrenic crush and a segmental resection. Ultimately, a right pneumonedomy was performed, with clinical improvement. Between 1953 and 1964 there was progressive shortness of breath. One month prior to admission, a chest x-ray film (Fig 1 ) showed a ''hazy infiltrate" at the left base, which was not previously noted. Table 1-Pulmonary Case Na.
DL.gnmis
luaia Pcol Dab
mm Hg
Function Data o f Three Patienu with Semere Pleural Re~riction D m
Meri.l SB (1) 01 kt..% ml/mm/mi.
VC
TLC
RV
88 (2) Litera (3) Lib (4) Litas (6)
RV/TLC FEVI% MMF Cdyn % FVC (6) Litera/wc.(7) Litsn/cmH10(8)
Pmu
&(9)
1
Pneumnnectomy. d c t . pleurisy 2 Old TB. Mali&. pleural d e t . 3 SLE --
--
-
- ---
-
1 Carbon monoxide diffusing u p c i t y single bath m e t h o d - n d d u e hrd on au data. 2 Carbon monoxide diffusing capacity l t a d y state d - - a d valua.1 3 Vital capacity (litem) nwmal value.' 4 Total lung mpscity (litera) n d due.' S Residual vdume (litera) normal d u e . '
CHEST, 67: 6, JUNE, 1975
6 One k w o d timed riW apcity-nornrl>75
percent. 7 Muimum midexpintury Bor rite-nand >O.7 I vibl u p c i t y . 8 Dylumic lw c o m p l b n c e - n d dues.* 9 Muimum pllmmvy rscdl p m a m - n d d u e -.33 x ye
-
+3 2
SEVERE PLEURAL RESTRICTION 659
due to removal at operation. The left lung specimen weighed
550 gm and the left parietal pleura was extensively thick-
ened, greyish-white and opaque. In several areas, the pleura measured as much as 0.9 cm in thickness. Pleural adhesions were extensive and involved both the diaphragmatic, mediastinal and costal aspects of the lungs. The adhesions were fairly easily removable. However, a 3 x 5 cm area on the costal as@ of the left upper lobe was adherent to the underlying pleura and sharp dissection was required to remove it. There was no evidence of granulomatous disease in the pleura. The configurations of the upper and lower lobes of the left lung were normal, and the cross sections revealed remarkably well preserved parenchymal patterns with minimal dilatation of bronchi and bronchioles. Microscopic examination of the pleura showed hyalinized, laminated almost acellular fibrous tissue, with multiple foci of calcification. The cause of death was felt to be respiratory failure secondary to left-sided pleural restriction in a patient who had had a right pneumonectomy. Her clinical course during the two years prior to death was believed to be one of progressive ventilatory failure due to end-stage parenchymal restrictive lung disease. At autopsy, to our surprise, this clinical diagnosis was not verified. The patient's left lung was found to be free of fibrosis, and the major cause of ventilatory failure was pleural restriction. The fact that the patient's Pmax was not greater than normal, in the absence of thoracic muscle weakness, chest wall deformity or obesity, pointed to pleural restriction rather than parenchymal fibrosis as the cause of ventilatory failure.
FIGURE3. (case 2 ) Note large right pleural effusion (Feb. 3, 1972).
This patient is a 62-year-old white woman who had pulmonary tuberculosis in the 1930's. The tuberculosis became inactive on bedrest, and x-ray films of the chest taken from 1956 to 1966 showed a stable lesion, with some fibrosis of both upper lobes and the left lower lobe ( Fig 2 ) . The patient
had no respiratory disability and was able to carry out her household duties. In January, 1972, the patient became ill wi& severe dyspnea over a one-week period. Physical examination a t this time revealed marked dullness and diminished breath sounds over the right posterior side of the chest. A chest roentgenogram taken Feb 3, 1972 confirmed the suspicion of a large
FIGURE 2. (case 2 ) Inactive tuberculosis is obvious, more marked on left ( roentgenogram taken 1966 ) .
FIGURE 4. (case 2) Pleural thickening fs shown on right ( May 30,1972 ) .
880 CILP, REICHEL, PARK
CHEST, 67: 6, JUNE, 1975
right pleural effusion (Fig 3). Thoracentesis and pleural biopsy confirmed the diagnosis of adenocarcinoma. Them was no evidence of a primary tumor in the lung, and on pelvic examination a small mass was noted which was thought to represent a primary ovarian tumor. Following the first thoracente-sis, two additional thoracenteses were performed over a two-week period. Subsequently, although neither radiotherapy nor chemotherapy were given, fluid did not reaccumulate, and the patient was left with residual pleural thickening as manifested by unchanging findings on chest x-ray film (Fig 4 ) for many months. During the three months following hospitalization, the patient noted progressive exertional dyspnea. The dyspnea became progressively worse for approximately two months, thenceforth remaining stable. On physical examination there remained considerable decrease of breath sounds over the right lower hemithorax. As in the past, scattered rilles were heard over the left lower lobe, and were attributed to bronchiectasis following tuberculosis. Pulmonary function studies were performed for the first time in July. 1972 (Table 1). As in the first case, the studies showed impairment of restrictive type with vital capacity of 0.85 liters. Results of lung studies again showed a very low compliance, but the Pmax was definitely below the predicted normal level for the patient's age. A lung perfusion scan showed a moderate decrease in perfusion of the right lower lobe, the left lower lobe and the left upper lobe. This patient, whose health was previously unimpaired, developed severe respiratory disability following unilateral neoplastic pleural involvement. Presumably, the unilateral deural involvement caused severe functional im~airment because the other lung was involved to a major degree by previous tuberculosis. While lymphangitic spread of carcinoma was initially considered as a cause of the patient's severe dyspnea, this diagnosis seems unlikely because the patient's condition did not progress clinically nor did lymphangitic carcinoma become apparent radiologically after several months of observation. Further, ovarian carcinoma rarely causes pulmonary lymphangitic carcinomatosis.
The patient is a 28-year-old Negro woman who initially presented in March. 1971 with severe chest pain and shortness of breath. The patient had noted diffuse arthralgias for one year. There was redness and swelling of the right knee and elbow for several weeks. For three weeks, she had bilateral chest pain and dyspnea. These symptoms had become progmssively more severe until the time of admission to the hospital. On physical examination the patient was febrile (38.9 C) and had dullness and decreased breath sounds at both bases, with a pleuropericardial friction rub over the left anterior hemithorax. There was evidence of arthritis as noted above. Chest roentgenograms showed bilateral pleural reaction ( Fig 5 ), with linear streaking at both bases. The findings on e l d o g r a m were consistent with findings in pencarditis. The suspected diagnosis of lupus erythematosus was confirmed by a strongly positive lupus erythematosus test'and a positive fluorescent antinuclear antibody study. Pulmonary function studies (Table 1) showed again restrictive impairments similar to those seen in cases 1 and 2, with a vital capacity of 0.8 liters. Results of lung studies showed a marked reduction of compliance; however, the Pmax was distinctly below normal. The patient was treated with prednisone, beginning with a dose of 40 mg daily. There was rapid and marked improve-
CHEST, 67: 6, JUNE, 1975
FIGURE5. (case 3) Bilateral pleural disease is obvious. ment, with relief of chest pain, dyspnea and other symptoms. Followup chest roentgenograms showed clearing of the pleuritis and infiltrates. In spite of clearing, the lungs were persistently small roentgenographically. Comparison of differential lung function bilaterally by the densigraphic method showed that both diaphragms moved and the vital capacity was symmetrically reduced bilaterally. The patient has been observed for wer one year, with gradual tapering of the dosage of prednisone to one tablet daily. Her condition remains stable, with no evidence of relapse of the original inflammatory process. Followup pulmonary function studies showed improvement within one month of treatment, with little change since then. A representative study is listed in the Table. The vital capacity has more than doubled, but is still far from normal. The TLC and residual volume have also increased so that the RV/TLC ratio remains slightly elevated. The single breath diffusing -capacity is also reduced, but not as much as the TLC, so that the diffusion to volume ratio is actually higher than normal, suggesting that interstitial fibrosis is not the cause of the patient's marked impairment of Wusion. Finally. although lung compliance has increased somewhat, the Pmax remains quite reduced. On the basis of these findings, the patient is felt to be suffering from considerable residual pleural fibrosis due to lupus erythematosus. Decortication has not been recommended because of the bilateral nature of the Drocess and because of our uncertaintv concerning how a Gtient with lupus erythematosus w o i d tolerate such an operation.
All three patients had marked reduction of vital capacity and slight or moderate reduction of residual volume. Since the total lung capacities were all quite decreased, the RVITLC ratios were increased in all patients. The patient with one lung had more reduction of volumes than the other patients. A low maximal midexpiratory flow rate (MMF) SEVERE PLEURAL RESTRICTION 661
was found in our patients and is explained by reduction of the vital capacity, for the normal timed vital capacities indicate the absence of airways obstruction. The diffusing capacity (Dco) was markedly reduced in all three patients. Arterial blood gas analyses showed hyperventilation and maintenance of normal or fairly normal oxygenation in two of our patients. Patient No. 1, who had the most severe mechanical ventilatory defect, developed chronic hypoventilation and arterial desaturation prior to her death. Chest wall compliance was not measured, but lung compliance was markedly reduced in all three patients. Also, the maximum static pulmonary recoil pressure was slightly lower than predicted in all three patients. We have reviewed all the Pmax measurements performed in our laboratory on patients with pleural disease and, for comparison, on patients with interstitial lung disease ( including sarcoidosis) who had total lung capacities of less than 80 percent of predicted. There were only 7 cases of uncomplicated pleural disease, but there were 61 cases of interstitial disease. In the former group, the Pmax ranged from 7-23, in the latter from 12-62 crn HzO.
I
I
PULMONARY FIBROSIS
A OTHER
CURRENT)
PLEURAL DISEASE
% PREDICTED TLC
FIGURE 6.Graph of Pmax (as percent of predicted) vs TLC (percentage of predicted) in patients with pulmonary fibrosis and pleural disease. Solid and broken lines represent regression line and one tail 95 percent confidence limit, respectively, for group of patients with pulmonary fibrosis. Regression formula, correlation coefficient ( r ), and Pvalue are: log Prnax (percentage predicted) = 2.45 - 0.59 x TLC (percentage predicted ) r = .34 P = 0.01
662 COLP, REICHEL, PARK
The relationship between the Pmax and the total lung capacity in all of the patients is shown in Figure 6. There was a wide range of variation of the Pmax in relation to the TLC, and its distribution along the regression line was skewed. Semilogarithmic plotting normalized this distribution. In four of seven cases of pleural restriction, the Pmax was well below the 95 percent confidence limits for pulmonary fibrosis cases. In two other cases, the Pmax was at the 95 percent confidence limit. Only one patient with pleural disease had a Pmax within the range expected for patients with pulmonary fibrosis.
Results of pulmonary function studies were remarkably similar in the three patients reported here. All had marked decrease of lung volumes. The findings of increase of the RV/TLC ratio in these patients (who were free of airways obstructive disease) are in accord with the usual findings in pleural disease4 and in normal subjects following chest trapping,^ and this seems to be generally characteristic of chest wall restriction or muscle weakness in which the residual volume is minimally affected but there is marked inability to expand the chest. All three patients had marked reduction of the Dco, probably due mainly to the marked reduction of lung volumes. The second patient was known to have some fibrosis of the lung due to tuberculosis, probably accounting in part for her reduction of Dco. In the third patient, with systemic lupus erythernatosus, the single breath Dco, performed at the time of followup study when she had improved with therapy but was still severely restricted, was about one-half normal. This reduction of Dco was not as great as the reduction of the total lung capacity at the time. The Dco is volume dependent and Yoo4 found, in patients with pleural disease, reduction of approximately the same magnitude as the reduction of the total lung capacity. On the other hand, in patients with diffuse interstitial pulmonary fibrosis, the Dco is almost always more reduced than are the lung volume^.^ Therefore, in this patient with lupus erythematosus, the relatively well preserved Dco lends further support to the impression that she does not have d i k e interstitial fibrosis and that her restriction is due to chronic pleuritis. In keeping with this interpretation are the findings of Huang and Lyons7 who compared pulmonary function data in patients with systemic lupus erythematosus and sclerodenna. In systemic lupus erythematosus, particularly in patients with known pleural involvement, the lung volumes were relatively more CHEST, 67: 6, JUNE, 1975
affected than the Dco. In contrast, patients with scleroderma, in whom diffuse interstitial fibrosis of the lung is the usual pathology, had better preservation of lung volumes but more marked reduction of the Dco. Perhaps the most significant findings in our three patients with severe restrictive pleurisy are the measurements of lung mechanics, which revealed a reduction of the maximal static p u b n a r y recoil pressure in the presence of severe reduction of lung compliance. The Pmax is affected by the recoil properties and degree of expansion of the lung. Factors affecting the latter include muscle strength, cooperation and the presence or absence of diseases of the pleura and the chest wall. Extrapulmonary factors which limit expansion of the lung will result in a decreased maximum static pulmonary recoil pressure. For example, in three of four patients studied in our laboratory with severe restriction due to kyphoscoliosis, the Pmax was slightly less than normal. The Pmax was similarly reduced in 13 of 17 patients with severe obesity. Also, inspection of static pressurevolume graphs in obese patients studied by Naimark and Cherniack8 indicates maximum transpulmonary pressures lower than found in their normal controls. Although the reduction of Pmax in the presence of volume restriction may be considered characteristic of extrapulmonary restriction, the fact that the reduction of Pmax is less than that of lung volume and the reduction of lung compliance was out of proportion to the reduction of lung volumes re~uires explanation. Do the findings suggest the possibility that these patients have coexisting pulmonary fibrosis? The fact that mechanical alterations of similar type were documented in normal subjects who had a tight rubber binder acutely applied to the thorax5 tends to deny such a possibility. In these subjects the lung volumes were reduced. As in our patients with pleural disease, the reduction of lung compliance was even more marked than the reduction of lung volumes. The transpulmonary pressure at any given volume was greater than before chest binding, but the maximum transpulmonary pressure ( Pmax ) was a little lower than in the normal state. Presumably, the chest binding causes closure of terminal airspaces which tend to decrease the lung compliance, and increase the lung recoil for a given volume. Such changes of lung mechanics would be even more pronounced at the lower volume level of our patients, where a greater number of terminal lung units may remain closed. The Pmax under these conditions would be affected by two opposing influences. On the one hand, the restriction of maximal inflation tends to reduce the Pmax. On the other CHEST, 67: 6, JUNE, 1975
hand, the closure of terminal lung units tends to increase the Pmax. Because of the balance of these opposing influences, the reduction of Pmax will be relatively less than the reduction of lung volume and of compliance. Thus, the relatively moderate reduction of Pmax in the presence of marked reduction of lung compliance observed in our patients with pleural disease may be largely accounted for by the closure of terminal lung units due to severe volume restriction. Indeed, postmortem examination of the lung revealed no significant parenchymal fibrosis in the first case despite a marked decrease of dynamic lung compliance noted during life. On the other hand, in pulmonary fibrotic disease, elevation of the maximum transpulmonary pressure has been well is again c o n h e d here, and is do~umented,~.'~ presumably due to the increased recoil force of the lung. Of course, there may be artefacts in the Pmax measurement; esophageal balloon pressure may not necessarily reflect true pleural pressure when there is extensive pleural disease. The relation between esophageal pressure and the pleural pressure of each pleural cavity when there is unilateral pleural restriction is not known. The possible effect of lung resection, especially pneumonectomy, on the Pmax is uncertain.' Despite these possible artefacts, the slightly low Pmax of pleural disease when found in conjunction with severe volume restriction appeared useful in these cases as a diagnostic aid in differentiating pleural restriction from fibrosis of the lung itself. This is a distinction of great practical importance because, although not used in any of our patients, decortication has been documented to be of therapeutic value in restrictive p l e ~ r i t i s . ' ~ , ~ ~ It is of interest that ventilatory failure, which is rare in fibrosis of the lung, occurred in our patient (who had had a pneumonectomy) with the most severe pleural resthction. ventilatory failure has not been reported in pleural disease alone but is a well known occurrence in other forms of severe extrapulmonary restriction with low Pmax such as kyph~scoliosis,'~ muscle weakness and obesity.
1 Bates DV, Macklem PT,Christie RV: Respiratory Function in Disease ( chap 2 ) . Philadelphia, WB Saunders Co,
1971 2 Ting EY, Williams Jr MH: The mechanics of breathing in chronic obstructive pulmonary disease. Am Rev Resp Dis
*Review of all Pmax determinations available to us after pneumonectomy revealed hi er than normal values in five atients, three of whom c early had pulmonary fibrosis, an3 a low value in one atient thought to have emphysema. Data were available begre and after operation in only one patient with cancer of the lung; his Pmax after pneurnonectomy was higher than the value before operation.
t'
SEVERE PLEURAL RESTRICTION 663
88:791, 1963 3 Frank NR, Mead J, Siebans AA, et al: Measurement of pulmonary compliance in 70 healthy young adults. J Appl Physiol9:38, 1956 4 Yoo OH, Ting EY: The effects of pleural effusion on pulmonary function. Am Rev Resp Dis 89:55, 1964 5 Cam CG, Butler J, DuBois AB: Some effects of restriction of chest cage expansion on pulmonary function in man: An experimental study. J Clin Invest 39:573, 1960 6 Colp C, Riker J, Williams MH Jr: Serial changes in lung function in scleroderma and idiopathic interstitial lung disease.Arch Intern Med 132:506, 1973 7 Huang CX,Lyons HA: Comparison of pulmonary function in patients with systemic lupus erythematosus, scleroderma and rheumatoid arthritis. Am Rev Resp Dis 93:885, 1966 8 Naimark A, Cherniack RM: Compliance of respiratory
system and components in health and obesity. J Appl Physiol 15:377, 1960 9 Ting EY, Williams Jr MH: Mechanics of breathing in sarcoidosis of the lung. JAMA 192:123, 1985 10 Macklem PT, Becklake MR: The relationship between the mechanical and diffusing properties of the lung in health and disease. Am Rev Resp Dis. 87:47, 1963 11 Petty TL, Filley GF, Mitchell RS: Objective functional improvement by decortication after 20 years of artificial pneumothorax for pulmonary tuberculosis. Am Rev Resp Dis 84:572, 1981 12 Siebens AA, Storey CF, Newman MM, et al: The physiologic effects of fibrothorax and the functional results of surgical treatment. J Thorac Surg 32:53, 1956 13 Bergofsky EH, Turino GM, Fishrnan AP: Cardiorespiratory failure in kyphoscoliosis. Medicine 38:283, 1959
Giacomo Puccini (1858-1924) "Puccini looks to me more like the heir of Verdi than any of his rivals." That was the verdict of a young London music critic called Bernard Shaw in 1894-a verdict made, remarkably, on the evidence only of Puccini's first successful opera, Manon Lescaut (1893). Shaw pointed to Puccini's combination of symphonic style (that is, a style of continuously developing music, like Wagner's) with a vein of traditional Italian melody. Puccini thereafter turned out a chain of operatic successes unequaled since his day. He pursued and ex-
664 COLP, REICHEL, M R K
tended this symphonic method; he extended also his range of poignant and biting harmonies, learning from Debussy as well as Wagner. Dramatically he cared little for subtlety of character but much for the power of erotic and brutal impulses seen or suggested on the stageimpulses which are powerfully suggested in the high points of his music. Jacobs A and Sadie S: Opera-A Modem Guide. New York, Drake Publishers, 1972
CHEST, 67: 6, JUNE, 1975
