Thorax 1985;40:613-617

Contribution of the rib cage to breathing intetraplegiaMDL MORGAN, AR GOURLAY, JR SILVER, SJ WILLIAMS, DM DENISON

From the Lung Function Department, Brompton Hospital, London; UK Scientific Centre, IBM, Winchester;and the National Spinal Injuries Centre, Stoke Mandeville

ABSTRACT In tetraplegia there is often paradoxical inward motion of the rib cage during inspira-tion. The volume of this negative contribution is difficult to estimate but can be obtained byoptical mapping. The partitioning of ventilation between the rib cage and abdomen in six normalsubjects, 10 stable tetraplegic patients, and one tetraplegic patient at intervals during rehabilita-tion has been studied by this technique. In normal subjects the tidal volume and the vital capacitywere the sum of positive contributions from the rib cage and abdomen. In stable tetraplegicsubjects with similar neurological levels, the rib cage contribution varied widely but the totalchest wall displacement could not be predicted from the vital capacity. In the patient studiedsequentially rib cage paradox reversed with time after injury, and this was associated with anabsolute increase in vital capacity and an improvement in the action of the diaphragm.

Several authors have drawn attention to the func-tional importance of paradoxical motion of the ribcage in tetraplegia.'-4 This is believed to account inpart for the very low vital capacity that may be seenafter injury. A reduction in paradoxical motion isoften associated with an improvement in vital capac-ity that occurs with time, even in the apparentabsence of neuromuscular recovery. It has not pre-viously been possible to make a volumetric estimateof this motion. This paper describes a method ofdoing so, by means of a previously described techni-que of optical mapping.5

Methods

In this study we examined six normal men (aged21-51 years) and 10 tetraplegic men (aged 16-71years). All were studied in the same way, lyingsupine and breathing quietly or making slow vitalcapacity manoeuvres. The excursions of thethoracoabdominal wall were recorded by opticalmapping. Briefly, the subject was photographedfrom above while a line pattern was projected on tohis body from either side. The distortion of the linepattern by the surface of the body produces contourlines when viewed from an angle other than that of

Address for reprint requests: Dr MDL Morgan, Chest MedicineDepartment, East Birmingham Hospital, Birmingham B9 5ST.

Accepted 19 February 1985

projection. Because the camera-projector relation-ships were known, the three dimensional coordi-nates of the body surface could be extracted fromthe photograph. Some 500-1000 coordinates of thetrunk surface were needed to generate adequatecross sections or compute the volume of those partsvisible to the camera. Serial photographs were usedto measure chest wall motion and respired volume.A continuous record of thoracoabdominal motionwas often obtained at the same time with a videocamera. In this case one typical quiet breath and onetypical vital capacity measurement were chosen foranalysis from the continuous record. The photo-graphic records of these breaths were digitised man-ually, a process that takes 30-40 minutes, so thatthey could be examined further.To determine the abdominal and rib cage compo-

nents of a breath the costal margin must be visible.Usually it could be seen with ease. When it couldnot, its end inspiratory and end expiratory positionswere marked on the skin. It is important to markboth because there may be considerable sliding ofthe skin over the rib cage in deep breathing (fig 1).The computer program for this study performs

four principal steps: (1) The spatial (x, y, z) coordi-nates of the 500-1000 points on the trunk surfaceare used to construct a digital image of the surfacerelative to a horizontal (that is, coronal) referenceplane close to the bed. (2) The position of the costalmargin on that surface is identified. (3) A vertical

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Fig 1 Torso with contour lines definng its shape; the three dimensional coordinates can be extracted to measure volume(left-inspiration; right-expiration). The costal margin can usually be identified easily on thin subjects, but if it cannotbe seen the boundary must be marked with a felt pen.

boundary is dropped from that margin to divide thetrunk image into rib cage and abdominal portions.(4) The instantaneous volumes and a selection ofcross sectional (that is, transverse) profiles are gen-erated for each portion.

SUBJECTSThe tidal volumes and vital capacity manoeuvreswere photographed in runs of three breaths and thetiming of the exposure was judged by eye. Thebreaths chosen for analysis were judged to be rep-resentative of the manoeuvre by observing the pat-tern change by eye on the still photographs and thevideo. After digitisation of the films from theselected breaths, the tidal volume and the vitalcapacity were calculated from the differences intrunk volume between inspiration and expiration.The measurement of respired volume in this way has

previously been shown to give acceptable accuracyin both normal and tetraplegic subjects.5

Photographs of six normal male subjects weretaken at the extremes of tidal breathing and of slowvital capacity manoeuvres. The distribution of venti-lation was also determined in 10 patients with com-plete traumatic tetraplegia. Their level of injury wasC5 or C6 as determined by clinical examination, andthe duration of injury ranged from two weeks to 25years. None of the patients had any respiratorycomplications at the time of study. In addition, onepatient was studied on several occasions to recordthe change in pattern of ventilation with duration ofinjury. He was 18 years old at the time of his acci-dent, when he sustained a transection of the spinalcord at the level of C6. There were no other injuries,the chest radiograph on admission was normal, andhe had no subsequent respiration complications. Hewas studied on six occasions, 6, 13, 27, 41, 75, and272 days after injury.

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Contribution of the rib cage to breathing in tetraplegia

ResultsNORMAL SUBJECTSThe findings for a typical quiet breath and a typicalvital capacity manoeuvre in normal subjects aresummarised in figure 2, in which the respiratoryexcursions are expressed as a percentage of eachsubject's predicted vital capacity.6 In all six subjectsthe abdominal and rib cage excursions wereoutward-that is, positive-so that the total breathis the sum of the two components. The rib cagecomponent varied from 5% to 56% (mean (SD)35% (17%)) during quiet breathing and from 21%to 68% (mean (SD) 40% (15%)) over the vitalcapacity.TETRAPLEGIC SUBJECTSThe findings in the 10 patients with tetraplegia areshown in figure 3 and follow the same convention.

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The vital capacities range from 18% to 67% of pre-dicted values for healthy people of same age, height,and sex. During quiet breathing the abdominalexcursions were positive in all 10 subjects. The ribcage components were paradoxical (ingoing or nega-tive) in six of the 10. In two patients ( 1 and 5) the ribcage contribution to tidal breathing predominated.Interestingly, both of these patients had abnor-malities of the bony rib cage (severe pectusexcavatum and ankylosing spondylitis). In the vitalcapacity manoeuvres the rib cage componentsbecame positive in three of the patients with para-dox during tidal breathing but it remained negativein the other three.The series of measurements made in one patient

over the first nine months after injury are shown infigure 4. In tidal breathing the paradoxical rib cagemotion diminished and then reversed with time, andduring the vital capacity manoeuvre rib cage motionwas consistently orthodox and increased with time

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Fig 2 Tidal volume (VT) and vital capacity (VC) ofall thenormal subjects, each expressed as percentage ofpredictedVC. The unshaded bars represent vital capacity or tidalvolume and the shaded and black bars alongside show theabdominal and rib cage components ofthe excursion, whichwere in all cases positive. The abdominal contributionpredominated in this position, accounting for 65% and60% in the respective breaths.

Fig 3 Partitioning oftidal breathing and vital capacitybetween the rib cage and the abdomen in 10 tetraplegicsubjects. During tidal breathing (VT) there was a negativerib cage contribution in six subjects. The largest volumes ofparadox were seen in the two patients with the shortest andlongest duration ofinjury. During the vital capacity (VC)manoeuvre many patients were able to reverse the negativerib cage contribution, but the two with the most severe

degrees oftidal paradox were unable to do so.

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after the injury. Over this pertribution of the abdomen to tUthan doubled (715 to 1778 ml

Discussion

Previous methods of determintributions of the rib cage andtypes: one is partial plethysmolBergofsky, where the lowerenclosed in a tank and the abdcseparated by a rubber seal ar(gin.' This method measures truis open to error because the pcchange during a breath andcaudocranial movements of thtype of method uses measureence,8 anteroposterior diametearea'0 to derive volume chantthe derivation depends on a:the measured variable and thewhich volume-motion coefficieFor this the subject usually hastion manoeuvre, which may

posture. These methods also

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Fig 4 Results obtained in a singlestudied on six occasion after injuryparadox during tidal breathing gra4time and then reversed. During thethere was no rib cage paradox and Iabdominal contrbution increased i

individual there was improvement iwithout obvious neuromuscular ret

iod the absolute con- dimension always implies a particular rib cage orle vital capacity more abdominal volume when the airway is closed. Opti-1). cal mapping makes no assumptions about shape and

does not need to be calibrated for the individual.The partitioning is performed after the breath hasbeen taken and along a boundary that can be clearly

ing the volume con- defined. Although the diaphragm itself is not visibleabdomen are of two the abdominal contents can be considered to begraphy, developed by incompressible and therefore caudal displacementpart of the body is of the diaphragm will produce abdominal expansion)men and rib cage are of the anterior wall that is visible to the camera.ound the costal mar- Thus the increase in abdominal volume that isie volume change but observed represents the volume displaced by the4sition of the seal will descent of the diaphragm.cannot account for The results of partitioning of ventilation in normal

e rib cage. The other supine subjects by optical mapping are similar tosments of circumfer- those achieved by other methods." The rib cage andXr,9 or cross sectional abdomen normally operate in parallel and the sumge. In these methods of their individual volume displacements makes uprelationship between the total volume change of the respiratory system. Involume change, from the normal subject these contributions are alwaysnts can be calculated. positive.,to perform a calibra- Fugl-Meyer and Grimby'2 attempted to partitiononly be valid in one ventilation in tetraplegia by using the method ofassume that a given Konno and Mead. They failed because the instabil-

ity of the rib cage in tetraplegia invalidated themethod. They did, however, report partial success inquiet breathing, where they described abdominalpredominance. Earlier Bergofsky, using trunkplethysmography, which was much criticised at thetime, obtained similar results to those describedhere.'3 He found that abdominal expansionaccounted for the major part of both tidal andexaggerated breathing and that in some patientsthere was rib cage paradox. In some of his patientsthe paradox was corrected on deep inspiration,while in others it increased. The results for patients1 and 2 (see bottom of fig 3) illustrate an importantpoint. They show that patients with very similar vitalcapacities and identical levels of injury may have afourfold difference in displacement of the total chestwall. This in turn suggests that monitoring a tetra-plegic patient's respiratory ability on the basis of

R vital capacity alone may be misleading.The degree of motion of the rib cage in tetraplegic

41 75 22l patients with similar levels of injury shows consider-

41 75 272 able individual variation. The ability of the rib cageto withstand the tendency to paradox appears to bedetermined by the degree of stiffness of the bony rib

tetraplegic pabtient cage and possibly by the action of the neck accessorythe diinitiaercage muscles.' The duration of injury and the presence

dually diminished withvital capacity manoeuvre of intercostal muscle spasticity are not importantboth the rib cage and the factors in explaining the differences in rib cagewith time. In this motion between patients. In the patient who wasin lung function with time studied sequentially after injury, however, there wascovery. an improvement in tidal volume and vital capacity

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Contribution of the rib cage to breathing in tetraplegia

that was not accompanied by any other clinical evi-dence of neuromuscular recovery. One obviousexplanation for this would be progressive improve-ment in diaphragmatic function after the resolutionof oedema of the cord soon after injury. While this isknown to occur in some cases, this patient wasscreened fluoroscopically one week after injury,when the diaphragm appeared to move well. Theincrease in the abdominal component may thereforehave a different explanation-for example, stiffen-ing of the rib cage through joint stiffness, or perhapseven intercostal spasticity, and atrophy of theabdominal wall allowing the diaphragm to movemore effectively than before.

Within individuals therefore function appears toimprove with time after injury. Thus rib cage para-dox may be only a temporary phenomenon in somepatients while in others it may improve but neverresolve.

References

1 Mortola JP, Sant'Ambrogio G. Motion of the rib cageand the abdomen in tetraplegic subjects. Clin Sci MolMed 1978;54:25-32.

2 Fugl-Meyer AR, Grimby G. Ventilatory function intetraplegic patients. Scand J Rehabil Med 1971;3:151-60.

3 Moulton A, Silver JR. Chest movements in patientswith traumatic injuries of the cervical cord. Clin Sci1970;39:407-22.

6174 Ledsome JR, Sharp JM. Pulmonary function in acute

cervical cord injury. Am Rev Respir Dis 1981;124:41-4.

5 Morgan MDL, Gourlay AR, Denison DM. An opticalmethod of studying the shape and movement of thethoracoabdominal wall in recumbent patients. Thorax1984;39: 101-6.

6 Cotes JE. Lung function: principles and application inmedicine. 3rd ed. Oxford: Blackwell Scientific Publica-tions, 1975.

7 Bergofsky EH. Relative contributions of the rib cageand diaphragm to ventilation in man. J Appl Physiol1964; 19: 698-706.

8 Agostoni E, Mognoni P, Torri G, Saracino F. Relationbetween changes of rib cage circumference and lungvolume. J Appl Physiol 1965; 20: 1179-86.

9 Konno K, Mead J. Measurement of separate volumechanges of rib cage and abdomen during breathing. JAppl Physiol 1967; 22:407-22.

10 Sackner JD, Nixon AJ, Davis B, Atkins N, SacknerMA. Non-invasive measurement of ventilation duringexercise using a respiratory inductive plethysmograph.Am Rev Respir Dis 1980; 122:867-71.

11 Sharp JT, Goldberg NB, Druz WS, Danon J. Relativecontributions of ribcage and abdomen to breathing innormal subjects. J Appl Physiol 1975;39:608-18.

12 Fugl-Meyer A, Grimby G. Rib cage and abdominalvolume ventilation partitioning in tetraplegic patients.Scand J Rehabil Med 1972;4: 161-7.

13 Bergofsky EH. Mechanism for respiratory insufficiencyafter cervical cord injury. Ann Intern Med1964;61:435-47.

14 Morgan MDL, De Troyer A. The individuality of chestwall motion in tetraplegia. Clin Respir Physiol1984;20:547-52.

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