79horax 1993;48:698-701

Lung volume restriction in patients with chronicrespiratory muscle weakness: the role ofmicroatelectasis

M Estenne, P A Gevenois, W Kinnear, P Soudon, A Heilporn, A De Troyer

Chest ServiceM EstenneW KinnearA De TroyerDepartment ofRadiologyPA GevenoisErasme UniversityHospitalDe Bijtjes InstituteP SoudonRehabilitation Center,Brugmann HospitalA HeilpornBrussels, BelgiumReprint requests to:Dr Estenne, Chest Service,Erasme Hospital, Route deLennik 808, 1070 Brussels,BelgiumReceived 12 October 1992Returned to authors24 December 1992Revised version received17 March 1993Accepted 23 March 1993

AbstractBackground-It is well established thatpatients with longstanding weakness ofthe respiratory muscles have a reductionin lung distensibility. Although thisoccurs in most patients without anyradiographic changes suggestingparenchymal lung disease, it has beenattributed to the development ofmicroatelectasis.Methods-A high resolution computedtomographic (CT) scanner was used ineight patients with traumatic tetraplegiaand six patients with generalised neuro-muscular disorders to look for areas ofatelectasis. With the patient in the supineposture scans of 1 mm thickness wereobtained at total lung capacity at inter-vals of 1 cm from the apex to the base ofthe lung.Results-Vital capacity, total lung capac-ity, and inspiratory muscle strength werereduced to a mean of 59'5%, 7390/o, and511% of predicted values, respectively.Static expiratory lung compliance wasdecreased in 12 of the 14 patients andaveraged 69-1% of the predicted value.The CT scans revealed only small areasof atelectasis in one tetraplegic patientand in one patient with a generalisedneuromuscular disorder; no parenchy-mal abnormality was seen in the other 12patients.Conclusions-In many patients withchronic weakness of the respiratory mus-cles the reduced lung distensibility doesnot appear to be caused by microatelec-tasis. It might be related to alterations inelasticity ofthe lung tissue.

(Thorax 1993;48:698-701)

It is now clearly established that the loss oflung volume in patients with longstandingweakness of the respiratory muscles results, inpart, from a reduced distensibility of thelung.' This reduced lung distensibility hasbeen reported in patients who develop diseasein adult life, such as those with traumatictransection of the cervical cord or withpoliomyelitis, as well as in patients with mus-cular dystrophy who usually develop signsand symptoms of the disease in early child-hood.2-8 It is clear, therefore, that failure ofdevelopment of a normal complement of

alveoli is not the primary factor. On the otherhand, it is well known that lower lobe atelec-tasis is a frequent occurrence in patients withsevere diaphragmatic weakness.78 Patchyatelectasis has also been found at postmortem examination in many ventilatordependent patients with poliomyelitis.910Therefore, although in most patients thereduced lung distensibility is present withoutany radiographic changes suggestingparenchymal lung disease, this alteration hasbeen attributed to dispersed alveolarcollapse.'We have used a high resolution computed

tomographic (CT) scanner to test thishypothesis directly and have sought to answerthe following questions. (1) Do patients withchronic respiratory muscle weakness and nor-mal chest radiographs have areas of atelecta-sis? (2) If they do, what is the topographicaldistribution of these areas within the lungs?(3) Are these atelectatic areas large enough toaccount for the observed reduction in pul-monary compliance?

MethodsFourteen patients (seven men, seven women)of mean (SE) age 36-1 (41) years (range20-69) were studied. Descriptions of thepatients are given in table 1. Eight patients(cases 1-8) had suffered accidental fracturedislocation of the cervical spine between thefourth and seventh vertebrae. They werestudied six months to 13 years after injury ata time when they were all tetraplegic and con-fined to wheelchairs. The other six patients(cases 9-14) had various chronic neuromus-cular disorders involving the respiratory mus-cles. The diagnoses had been made 6-28years before the study and were based onclinical and appropriate laboratory examina-tions. None of the 14 patients had a history ofrespiratory disease although two (cases 1 and3) were smokers and one (case 14) had previ-ously undergone corrective surgery by theHarrington method for thoracic scoliosis.None of the patients was treated by assistednocturnal ventilation. At the time of the studyall patients were in a clinically stable state andfree from respiratory symptoms; none hadany evidence of parenchymal disease onanteroposterior chest radiographs.

All pulmonary function tests were carriedout with the patient in the sitting position.Total lung capacity (TLC), vital capacity

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Microatelectasis in patients with respiratory muscle weakness

Table 1 Details ofpatients with respiratory muscle weakness

Patient Age Height Weight Duration ofno. (Y) Sex (cm) (kg) Diagnosis disease (y)

1 25 M 187 85 C4-5 112 69 F 162 64 C5-6 133 47 F 163 44 C4-5 94 31 M 176 80 C5-6 65 23 M 175 80 C6-7 46 22 M 182 60 C6-7 57 26 M 187 80 C6-7 0-58 33 M 180 70 C6 0-5

9 35 M 184 66 Becker muscular dystrophy 2210 28 F 150 49 Limb girdle muscular dystrophy 1811 60 F 154 42 Mitochondrial myopathy 612 33 F 152 40 SMA type II 2813 53 F 160 53 FSH muscular dystrophy 1714 20 F 156 52 Congenital muscular dystrophy 16

SMA-spinal muscular atrophy; FSH-facioscapulohumeral.

(VC), functional residual capacity (FRC), three maximal efforts were obtained in eachand residual volume (RV) were determined in patient and the lowest value was used as anduplicate by the closed circuit helium dilution index of inspiratory muscle strength.technique (Sensormedics 2400, Sensor- Predicted values for lung volumes are frommedics, Anaheim, California). Pressure- the European Community for Coal andvolume (PV) curves of the lung were obtained Steel'3 and normal values for the lung PVby a quasi-static method with an oesophageal curves and PpLmin are derived from measure-latex balloon (length 10 cm)." The balloon ments performed in our laboratory in 120tip was placed in the mid oesophagus and healthy subjects." Comparisons between pre-filled with 0-4 ml of air. Recordings of the PV dicted and measured values were made with acurves were preceded by three full inflations univariate analysis of variance.to ensure a constant volume history. Several Arterial blood was sampled from the radialinspiratory and expiratory curves were per- artery while the patient was breathing roomformed in each patient and a line of best fit air in the seated position, and blood gas ten-was drawn by eye through at least three sets sions were measured with an ABL 500 bloodof PV data that agreed to ± 1 cm H,O. The gas analyser (Radiometer; Copenhagen). Thestatic recoil pressure of the lung (Pst(L)) was alveolar-arterial oxygen tension differencemeasured at fixed percentages of TLC. Static (A-aDo2) was estimated using the alveolar airexpiratory lung elastance was calculated equation assuming a respiratory exchangeabove FRC from the linear portion of the PV ratio of 0-8. Predicted values for Pao, andcurve by measuring the change in volume A-aDo are those calculated by Mellemgaard."4produced by a 5 cm H2O change in Pst(L). CT scans of the lungs were then obtainedThe mean value for lung elastance obtained with a high resolution scanner (Somatonfrom at least three PV curves was subse- Plus, Siemens AG, Erlangen, Germany).quently converted to its reciprocal to give sta- With the patient supine scans of 1 mm thick-tic lung compliance.'2 ness were obtained at TLC at intervals of

Minimal (inspiratory) pleural pressures 1 cm from the apex to the base of the lungs;(PpiLmin) were obtained during maximal sta- scan time was two seconds, tube current 220tic inspiratory efforts at FRC. Pressures sus- mA, and voltage 137 kV. The images weretained for one second were recorded. At least reconstructed using an ultra high resolution

Table 2 Static lung volumes, lung compliance, and inspiratory muscle strength

Patient VC FRC TLC RV CL PPLmin at FRCno. (% pred) (% pred) (% pred) (% pred) (/o pred) (%/o pred)

1 31 84 59 156 38 502 92 65 81 76 72 793 51 94 80 138 39 384 52 77 67 112 75 485 64 94 85 153 104 506 54 88 72 134 77 477 51 103 81 188 109 578 63 79 74 109 65 40

9 85 76 80 67 79 7610 58 80 75 114 66 5111 76 88 75 80 76 3312 50 82 77 137 63 5613 59 81 70 92 40 4714 47 57 58 84 64 43

Mean 59-5 82-0 73-9 117-1 69-1 51-1SE 4-3 3-1 2-2 9 5 5-7 3-5

VC-vital capacity; FRC-functional residual capacity; TLC-total lung capacity; RV-residual volume; CL-staticexpiratory lung compliance; PPLmin at FRC-minimal pleural pressure measured at FRC.

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Estenne, Gevenois, Kinnear, Soudon, Heilporn, De Troyer

Figure 1 Staticexpiratory pressure-volumecurve of the lung inpatients with chronicweakness of the respiratorymuscles (open circles);mean data in eight patientswith traumatic tetraplegiaand six patients withgeneralised neuromusculardisorders. Closed circlesrepresent meanpredicted values. Each barrepresents ±1 SE. Volumeis expressed as apercentage of the predictedtotal lung capacity. Notethat the curve in thepatients is reduced on itsvolume axis and issubstantially flattened.

-i6 1000

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a 0 60-C

Q)-=Ea 406

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F

F

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Lung recoil pressure (cm H20)40

algorithm with a matrix of 512 x 512 pixelsand scored for the presence of atelectasis by athoracic radiologist (PAG).

ResultsAll patients had a substantial reduction ininspiratory muscle strength and considerablerestrictive ventilatory impairment. As shownin table 2 mean PPLmin was 51 1% of thepredicted value (p < 00001), and VC andTLC were 59-5% and 73 9% of the predictedvalues, respectively (p < 00001). The FRCwas also reduced in most cases with a meanvalue of 82-0% of predicted (p = 0-0001). Incontrast, RV was increased in six of eightpatients with traumatic tetraplegia and in twoof six patients with generalised neuromuscu-lar disorders. For the patient group as awhole, RV was 1 17 1% of the predicted value(p > 005).The mean expiratory PV curve of the lung

obtained in the 14 patients is compared withthe predicted curve in fig 1 which clearlyshows that the PV curve of the patients wasreduced on its volume axis and that Pst(L)was decreased both at full inflation and atFRC. The slope of the PV curve was alsoreduced. The results in table 2 show that 12of the 14 patients had a reduced pulmonarycompliance giving a mean (SE) value for thegroup as a whole of 69-1 (5-7)% of the pre-dicted value (p < 0O001).

Table 3 Arterial blood gas data and CT studies.

Patient Pao2 Paco2 A-aDo2no. (kPa) (kPa) (kPa) Chest CT

1 11-55 5-68 1-24 Normal2 9.79* 5-31 3-48t Atelectasis3 12-45 5-57 0-08 Normal4 10-89 5-43 2-60 Normal5 11-36 5-28 2-09 Normal6 12-51 5-27 1P01 Normal7 13-24 5-01 0-85 Normal8 13-47 5-01 0-63 Normal9 9.73* 5 50 3-40t Normal10 13-33 4-84 0 47 Normal11 11-89 5-48 1-69 Normal12 12-71 5-35 0-27 Normal13 13-24 4-68 0 43 Atelectasis14 13-87 4-80 0 09 NormalMean 12-15 5-23 1-31SE 0-36 0-08 0-31

Pao,-arterial oxygen tension; Paco2-arterial carbondioxide tension; A-aDor-alveolar-arterial oxygen tensiondifference; CT-computed tomography.*Values smaller than 2 SD below the predicted ones;tvalues greater than 2 SD above the predicted ones.'4

Values of Pao2, Paco2, and A-aDo2obtained during room air breathing are givenfor each subject in table 3. One tetraplegicpatient (case 2) and one patient with a gener-alised neuromuscular disorder (case 9) hadlow values of Pao2 and a slight widening ofthe A-aDo2. In the other 12 patients, how-ever, these values were within normal limitswith a mean Pao2 for the group of 12-15 kPa(predicted value 12-60 kPa) and a meanA-aDo2 of 1-31 kPa (predicted value 1-33kPa).The CT scans revealed areas of platelike

atelectasis in only one tetraplegic patient(case 2) and in one patient with a generalisedneuromuscular disorder (case 13). Theseareas were located in the two lower lobes incase 2 and in the right lower lobe in case 13.As shown in fig 2, however, these areas weresmall. The other 12 patients studied did notshow any parenchymal abnormality.Clinically the two patients with areas ofatelectasis did not differ from the others and,in particular, they did not show any clinicalsign suggesting diaphragmatic paralysis.

Figure 2 CT scan images of the lungs obtained in (A) case 2 and (B) case 13. Areas ofplauand in the right lower lobe in case 13.

e atelectasis are observed in both lower lobes in case 2

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Microatelectasis in patients with respiratory muscle weakness

Their degree of inspiratory muscle weaknessand lung volume restriction was also nogreater than in the other patients. Althoughcase 2 had a low Pao2 and an increasedA-aDo2, these variables were within normallimits in case 13.

DiscussionThe alterations in respiratory mechanicsfound in the patients studied are comparablein all respects to those previously reported inpatients with traumatic tetraplegia-6 or gener-alised neuromuscular disorders.'278 Allpatients had a clear restrictive ventilatoryimpairment and most had a reduced FRCand a decreased static pulmonary compli-ance, confirming that the distensibility of thelungs themselves is reduced in such patients.The reduction in static pulmonary compli-

ance in the patients in this study amounted toa mean of 30%. If this reduction was pri-marily related to atelectasis about one third ofall terminal lung units should be collapsed.Since our patients had no evidence of pul-monary alterations on standard chest radio-graphs we suspected that this lung collapsewas patchy. We therefore used a CT scannerwith a particularly high resolution whichallows solid structures of 1 mm in diameter tobe visualised.'5 No alteration in lungparenchyma was seen in 12 of the 14patients. Furthermore, the areas of atelectasisseen in the two patients were small and didnot account for the measured reduction inpulmonary compliance. It appears, therefore,that dispersed alveolar collapse is not the pri-mary determinant of the reduced lung disten-sibility in many patients with longstandingweakness of the respiratory muscles.Two factors would theoretically be capable

of reducing lung distensibility in otherwisenormal lungs when weakness of the respira-tory muscles exists. One mechanism, as sug-gested by Young et al,'6 is a generalisedincrease in the surface tension of the alveolarlining layer as a result of breathing at a lowlung volume. There is ample physiologicalevidence from acute experiments, beginningwith the work in dogs by Mead and Collier,'7that breathing at a small, constant tidal vol-ume is associated with a decrease in the com-pliance of the lungs. This disturbance hasbeen well documented both in laboratory ani-mals and in human subjects.'820 However,while this alteration is rapidly corrected by afew deep breaths when produced experimen-tally, it has been shown that the decreasedpulmonary compliance of patients withchronic respiratory muscle weakness is notreversed by short periods of positive pressuremechanical hyperinflation of the lungs.2' 22 Itis unlikely, therefore, that the reduced lungdistensibility in these patients is caused byalterations in surface forces.The second possible mechanism is an

alteration in lung tissue elasticity. Since theelastic properties of a system are partly deter-mined by the stresses to which the system issubjected, the elastic properties of lung tissuemight change in patients with respiratory

muscle weakness because of their chronicallylimited range of activity. We are aware of nodata which show directly that such patientshave abnormal shortening and stiffening ofthe elastic fibres within their lungs. The lackof improvement after mechanical hyperinfla-tion of the lungs,2'22 the normal appearanceof the lung parenchyma on the CT scanner,and the preservation of normal gas exchangein most subjects (table 3), however, are allconsistent with this explanation. The chroni-cally limited range of activity of these patientshas also been suggested to explain theirreduced rib cage compliance.The authors are greatly indebted to the Fonds de laRecherche Scientifique Medicale (FRSM, Belgium) for thegrant support (3.4518.92), to C Melot for his constructivesuggestions, and to M Onrubia for secretarial assistance.

1 De Troyer A, Pride NB. The respiratory system in neuro-muscular disorders. In: Roussos C, MacKlem PT, eds.The thorax. Part B. New York: Marcel Dekker, 1985;1089-121.

2 Ferris BG, Mead J, Whittenberger JL, Saxton GA.Pulmonary function in convalescent poliomyeliticpatients. m. Compliance of the lungs and thorax. NEngl Med 1952;247:390-3.

3 De Troyer A, Heilporn A. Respiratory mechanics inquadriplegia. The respiratory function of the intercostalmuscles. Am Rev Respir Dis 1980;122:591-600.

4 Estenne M, Heilporn A, Delhez L, Yernault JC, DeTroyer A. Chest wall stiffness in patients with chronicrespiratory muscle weakness. Am Rev Respir Dis1983;128: 1002-7.

5 Estenne M, De Troyer A. The effects of tetraplegia onchest wall statics. Am Rev Respir Dis 1986;134:121-4.

6 Scanlon PD, Loring SH, Pichurko BOM, McCool FD,Slutsky AS, Sarkarati M, et al. Respiratory mechanics inacute quadriplegia. Lung and chest wall compliance anddimensional changes during respiratory maneuvers. AmRev Respir Dis 1989;139:615-20.

7 Gibson GJ, Pride NB, Newsom Davis J, Loh LC.Pulmonary mechanics in patients with respiratory mus-cle weakness. Am Rev Respir Dis 1977;115:389-95.

8 De Troyer A, Borenstein S, Cordier R. Analysis of lungvolume restriction in patients with respiratory muscleweakness. Thorax 1980;35:603-10.

9 Landon JF. Analysis of 88 cases of poliomyelitis treated inDrinker respirator, with control series of 68 cases: clini-cal studies in poliomyelitis. JPediatr 1934;5:1-18.

10 Blosson RA, Affeldt JE. Chronic poliomyelitic respiratordeath. AmJ Med 1956;20:77-87.

11 De Troyer A, Yernault JC. Inspiratory muscle force innormal subjects and patients with interstitial lung dis-ease. Thorax 1980;35:92-100.

12 Clement J, Van de Woestijne KP. Resistance or conduc-tance? Compliance or elastance? J Appl Physiol 1971;30:437-9.

13 Quanjer Ph, ed. Standardized lung function testing.Working party. European Community for Coal andSteel. Clin Respir Physiol 1983;19(Suppl 5):45-51.

14 Mellemgaard K. The alveolar-arterial oxygen difference:its size and components in normal man. Acta PhysiolScand 1966;67: 10-20.

15 Mayo JR, Webb WR, Gould R, Stein MG, Bass I, GamsuG, et al. High-resolution CT of the lungs: an optimalapproach. Radiology 1987;163:507-10.

16 Young SL, Tierney DF, Clements JA. Mechanism ofcompliance change in excised rat lungs at low transpul-monary pressure. JAppl Physiol 1970;29:780-5.

17 Mead J, Collier C. Relation of volume history of lungs torespiratory mechanics in anesthetized dogs. Jf ApplPhysiol 1959;14:669-78.

18 Ferris BG, Pollard DS. Effect of deep and quiet breathingon pulmonary compliance in man. Jf Clin Invest1960;39:143-9.

19 Egbert LD, Laver MB, Bendixen HH. Intermittent deepbreaths and compliance during anesthesia in man.Anesthesiology 1963;24:57-9.

20 Williams JV, Tiemey DF, Parker HR. Surface forces inthelung, atelectasis, and transpulmonary pressure. JAppl Physiol 1966;21:819-27.

21 De Troyer A, Deisser P. The effects of intermittent posi-tive pressure breathing on patients with respiratory mus-cle weakness. Am Rev RespirDis 1981;124:132-7.

22 McCool FD, Mayewski RF, Shayne DS, Gibson CJ,Griggs RC, Hyde RW. Intermittent positive pressurebreathing in patients with respiratory muscle weakness.Alterations in total respiratory system compliance. Chest1986;90:546-52.

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