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IntroductionMalnutrition, detraining and disuse dueto prolonged bed rest, and increasedmuscular catabolism can all induce severeskeletal muscle dysfunction. Periods ofcontrolled mechanical ventilation forcepatients to undergo a period of bed rest and relative immobility. Combinedwith other factors (eg malnutrition, sepsis, pharmacological agents) this disuseleads to skeletal muscle atrophy. Therespiratory muscles are skeletal musclesand during periods of controlled mech-anical ventilation the diaphragm andother inspiratory muscles are movedpassively, so are theoretically prone tosuch disuse atrophy. Work on animals hassupported this theory (Anzueto et al,1997; Le Bourdelles et al, 1994). Anzuetoet al (1997) found significant impairmentin diaphragmatic strength and endurancein baboons that had been mechanicallyventilated for 11 days. The logical im-plication is that this could also occur inhumans, but no studies have demon-strated this.

Any abnormalities in muscle functionmay be exacerbated by reduced oxygensupply, metabolic acidosis, electrolyte orendocrine disorders. Thus, the inspiratorymuscles may already be weakened beforemechanical ventilation and are likely todeteriorate during the ventilation period.Although inspiratory muscle function isdifficult to measure, some studies havesuggested that the inspiratory muscles areseverely weakened in intubated patientsrecovering from critical illness (Kacmareket al, 1989; Sahn and Lakshminaryan,1973). Early studies suggested that a lowmaximal inspiratory pressure (MIP)signifying inspiratory weakness was animportant predictor of weaning failure(Sahn and Lakshminaryan, 1973).Subsequent studies, however, have failedto find significant differences in the MIP

Inspiratory MuscleDysfunction after ProlongedPeriods of MechanicalVentilation Two case studies

SummaryBackground and purpose Mechanical ventilationnecessitates periods of bed rest and relative immobility that,combined with other factors, lead to skeletal muscle atrophy.As the respiratory muscles are skeletal muscles, they aretheoretically prone to disuse atrophy. Sustained maximalinspiratory pressure (SMIP) measures are a new form ofassessment of inspiratory muscle function that may reflectinspiratory work capacity. The aim of this study was toestablish whether inspiratory or peripheral muscle function isabnormal after a period of prolonged mechanical ventilation,and whether any changes in function occur during aprolonged weaning programme.

Methods Two adult patients who had required mechanicalventilation on a general intensive care unit for more than 14 days consented to take part in the study. Baseline SMIP,standard maximal inspiratory pressure (MIP) and handgripstrength measures were performed when weaning began.Repeated SMIP, MIP and grip measures were taken twice aweek during the weaning programme until each patient wasable to breathe without support for 48 hours.

Findings Baseline SMIP and handgrip measures were foundto be abnormally low in both subjects. SMIP measuresincreased over a series of measurement sessions, in parallelwith increases in measures of handgrip and diminishing levelsof respiratory support. Standard MIP measures started from alevel that would generally indicate ability to breathe withoutsupport and showed little change over time.

Conclusions If SMIP is accepted as a reliable measure ofinspiratory muscle function, then these findings support thehypothesis that periods of mechanical ventilation have adetrimental effect on respiratory muscle function. Thesefindings also suggest that SMIP is responsive to changinginspiratory muscle function, but as they are fromuncontrolled studies, no firm conclusions can be drawn.

Key WordsMechanical ventilation,intensive care, respiratory muscle.

by Anne BrutonJoy H ConwayStephen T Holgate

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whether a weaning trial is successful orfails.

Sustained MIP (SMIP) is a relativelynew non-invasive measurement forassessing inspiratory muscle function. It isbased on the ability to sustain maximalinspiratory pressure during a dynamicmanoeuvre from residual volume (RV) tototal lung capacity (TLC). The reliabilityof this measure has been studied innormal subjects (Bruton et al, 1999) andin patients with respiratory pathology(Bruton et al, 2001).

The aims of this study were:

� To establish whether inspiratory musclefunction (assessed by SMIP measures)or peripheral muscle function(assessed by handgrip) is abnormalafter a period of prolonged mechanicalventilation.

� To establish whether any change ininspiratory or peripheral musclefunction occurs during a prolongedweaning programme.

MethodFull ethical approval was granted bySouthampton and South West HampshireJoint Research Ethics Committee beforethe study was undertaken.

EquipmentThe original equipment for measuringSMIP was designed for spontaneouslybreathing patients and consists of threeelements: a handset plus mouthpiece, abase unit, and a personal computer

Bruton, A, Conway, J H andHolgate, S T (2002).‘Inspiratory muscledysfunction afterprolonged periods ofmechanicalventilation: Two casestudies’, Physiotherapy,88, 3, 131-137.

Fig 1: Sample SMIP graphs from Kevin, first session

10

17 33 49 65 81 97 113 129 145 161 177

Time (16 units = 1 second)

Kevin: June 6, 2000

Insp

irat

ory

pre

ssu

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cm H

2O)

10

20

30

40

50

60

70

Fig 2: Sample SMIP graphs from Kevin, last session

10

17 33 49 65 81 97 113 129 145 161 177

Time (16 units = 1 second)

Kevin: July 4, 2000

Insp

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pre

ssu

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cm H

2O)

10

20

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70

Fig 3: Photograph of SMIP equipment

in situ with a ‘mock’ ICU patient

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running a software package that is knownas the TIRE (Test of IncrementalRespiratory Endurance). The equipmentwas adapted for intubated patients (byDeVilbiss UK Ltd) by uniting the com-ponents of the handset and base unit intoa single unit.

The TIRE software samples theinspiratory pressures at 16 Hz during asustained maximal inspiration andgenerates a graph of these inspiratorypressures over time (fig 1, 2). Thesoftware also indicates the peak maximalinspiratory pressure (peak MIP), ie thehighest pressure generated; and SMIP, ie the area under the curve produced by a sustained maximal inspiratorymanoeuvre. The TIRE software wasinitially designed for inspiratory muscletraining (Chatham et al, 1995), but hasalso been used as a measure of inspiratorymuscle function (Bruton et al, 1999, 2001;Ionescu et al, 1998). Grip strength waschosen as an indicator of peripheralskeletal muscle performance for thesestudies. The equipment used was anelectrical hand-held grip strength meter(MIE Medical Research Ltd) with a digitalliquid crystal display.

Subject Selection and RecruitmentAdult patients who had requiredprolonged periods of mechanicalventilation (more than two weeks) andwho were willing to participate wereeligible for inclusion in the study.Exclusion criteria were cardiovascularinstability, inability to communicate inEnglish, or inability to give informedconsent. The two patients who took partin the study were adults who had requiredlonger than average periods of mech-anical ventilation and were believed (by aconsultant) to be likely to require aprolonged phase of gradual weaning fromventilation. Each subject was approachedby the researcher and agreed to performrepeated measures of both SMIP andhandgrip strength during the weaningprocess. Initial measures were carried outonce the decision to start reducing thelevel of respiratory support had beentaken. Subsequent measures were takenonce or twice a week depending on eachindividual’s condition and co-operation.

Procedure for Measurement of SMIP

� Before performing SMIP tests subjectsinspired 100% oxygen for 1-2 minutesto prevent any possibility of hypoxiaduring the measurements.

� Subjects were placed in high sitting(roughly 45º at the hips) and a numberof baseline parameters recorded, ie respiratory rate, heart rate and blood pressure.

� The equipment was inserted into theventilator circuit with a three-way tappermitting the subjects to continuewith their current mode of assistedventilation until the moment ofmeasurement (fig 3).

� Subjects were then asked to exhale toresidual volume, the three-way tap wasturned, and then subjects were stronglyencouraged to make a single maximalinspiratory effort for as long aspossible.

� At the end of each measuredinspiration, the three-way tap wasreturned to its original position andsubjects were able to exhale normallyand resume their normal mode ofrespiration. The whole measurementprocedure took less than 30 seconds.

� After a rest period of at least oneminute the procedure was repeated.

� Practice attempts were made until theoperator was satisfied that the readingswere as technically acceptable aspossible. Technical acceptability wasdefined as no obvious air leak duringthe manoeuvre, maximal inspiratorypressure occurring within the firstsecond, a continuous inspiratory graphshowing a rapid rise to a peak, followedby a gradual decay towards zero with nosudden fall in pressure.

Procedure for Measurement ofHandgripThe protocol for grip strength meas-urement followed that of Balogun et al(1991a, b) and adapted for the setting.Measures were taken in the same positionas for SMIP measures. After familiar-isation with the technique, three maximalefforts were recorded for each hand witha minimum of 60 seconds rest betweeneach effort. The highest recorded valuewas used for data analysis. The reliabilityof these measures has been reportedelsewhere (Bruton et al, 1999, 2001).

Authors

Anne Bruton PhD MAMCSP and Joy HConway PhD MScMCSP are lecturers inphysiotherapy andStephen T HolgateMD DSc FRCP isMRC professor ofimmunopharmacologyat the University ofSouthampton.

This work forms partof a PhD undertakenby Anne Bruton and supervised by Dr Conway andProfessor Holgate. It was funded by theSouth East Researchand DevelopmentDirectorate.

This article wasreceived onDecember 1, 2000,and accepted onAugust 10, 2001.

Address forCorrespondence

Dr Anne Bruton,School of HealthProfessions andRehabilitationSciences, University of Southampton,Highfield,Southampton SO17 1BJ.

E-mailab7@soton.ac.uk

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Case Study 1A 68-year-old man ‘Julian’ with knownischaemic heart disease, peripheralvascular disease, emphysema and benignpleural asbestos disease presentedcomplaining of increasing shortness of breath on exertion. Subsequentinvestigations revealed two masses in theupper lobe of the right lung for which heunderwent a right upper lobectomy. Post-operatively Julian developed acuterespiratory failure requiring intubationand mechanical ventilation on theintensive care unit. He had two failedextubation attempts and then received apercutaneous tracheostomy.

Subsequently Julian had a number ofmedical and psychological problemsincluding a Pseudomonas aeruginosainfection, periods of atrial fibrillationrequiring cardio-conversion, and periodsof agitation, anxiety and depressionrequiring a referral to a psychoger-iatrician and medication (Lorazepam).During this period he was also deemed tohave nutritional problems includingweight loss and generalised oedema.

Four weeks later Julian’s condition had stabilised enough for the decision to be taken to initiate a weaning prog-ramme and he was deemed appropriatefor SMIP measurement by a consultantanaesthetist.

Two weeks after that ventilatory sup-port could be removed and Julian wasreturned to an ordinary ward.

Case Study 2A 19-year-old man ‘Kevin’ was admitted tohospital with a two-week history of aninfluenza-like illness, and a preliminarydiagnosis of community-acquiredpneumonia. On admission he neededimmediate intubation and mechanicalventilation for respiratory failure. Overthe following week his conditiondeteriorated with increasing expiratoryflow obstruction and a rising PaCO2,despite heavy sedation, full paralysis and trials of various ventilatory modesincluding prone lying.

Kevin was then transferred to theresearcher’s intensive care unit with aPaCO2 of 21 kPa (normal range 3.5 to6.5). He was ventilated using pressureregulated volume control on an osc-illating bed, paralysed with atracuriumand sedated with fentanyl and propofol. A diagnosis of Goodpasture’s syndrome

was made on the basis of glomerularbasement membrane (GBM) antibodyresults of > 100 (normal being < 2.5).Treatment for this consisted of dailyplasmapheresis and immunosuppres-sion using a combination of steroids(hydrocortisone) and a cytotoxic agent(cyclophosphamide).

Three days later Kevin’s trachealaspirate was noted to be multi-resistantStaphylococcus aureus (MRSA) positive (forwhich vancomycin was prescribed) andhis renal function began to deteriorate.Ten days later he received a percutaneoustracheostomy and his ventilation modewas changed to pressure support. Overthe next few days his sedation wasgradually reduced and attempts weremade to reduce the level of pressuresupport required.

The weaning process continued foranother three weeks, during which therewas a period when Kevin becamedepressed and was started on ami-triptyline and Prozac. At the end of thisweaning period he no longer requiredany ventilatory support, his tracheostomytube was removed and he was transferredto an ordinary ward.

MeasurementsThe serial measures taken from eachsubject are outlined in tables 1 and 2. Theaim was to take measures twice a week.However, the interval between measureswas not consistent as the subjectssometimes chose not to do them oncertain days.

Figures 1 and 2 give sample SMIPgraphs generated by Kevin at his first andlast measurement sessions respectively.SMIP measures are expressed in pressuretime units.

Published results from earlier studiesindicate that for normal men the meanSMIP is about 600 pressure time units(although with wide inter-subject var-iability), mean peak MIP about 110 cmH2O, and mean handgrip about 300Newtons. ‘Normal’ data for intensive carepatients are not currently available. It hasbeen suggested that a MIP of 30 cm H2Oor higher indicates readiness to beweaned from mechanical ventilation(Sahn and Lakshminarayan, 1973).

Baseline SMIP and handgrip measureswere abnormally low in both subjects and increased over time. Standard MIPmeasures, however, started from a level

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that would generally indicate ability tobreathe without support and showed littlechange over time.

DiscussionThese two patients illustrate a number ofthe environmental factors known to bedetrimental to general skeletal musclefunction. Malnutrition is known to havean adverse affect on muscle function(Epstein, 1994) and is a common prob-lem in critically ill patients (Cerra et al,1997). Both subjects lost weight duringtheir admission and thus reduced theirbody mass index. Formal assessment ofnutritional status in intensive care is acomplex issue and was not undertaken in this study, but it is likely that bothsubjects had sub-optimal nutritional statusduring their illness. Sepsis is also knownto have an adverse affect on musclefunction (Roussos and Macklem, 1982),and both subjects had infective episodesduring admission (one with Pseudomonasaeruginosa, one with MRSA). Suchinfective episodes are common incritically ill patients.

Pharmacological agents have also been associated with abnormal musclefunction, in particular corticosteroids(Decramer et al, 1994). Critical illnessmyopathy is being increasingly reportedin intensive care units (Hund, 1999).Although several factors may contrib-ute to the condition, the action of corticosteroids seems to predominate(Larsson et al, 2000) along with poten-tiation by neuromuscular blocking agents,immobility and possibly sepsis. Kevintherefore had all the factors believed tobe associated with critical illnessmyopathy, but no formal electrophys-iology tests were carried out.

The effect of psychological factors onskeletal muscle function has not beenclearly determined. It has been suggested,however, that psychological factors cancontribute to weaning failure (Marini,1995). Both men experienced periods ofdepression during their intensive careadmission.

The inspiratory muscles are subject toall the factors that affect skeletal muscles.The conventional measure of inspiratorymuscle strength in ventilated patients isthe MIP, but Moxham and Goldstone(1994) have described MIP measurementsin the ICU as ‘of limited value’. In boththese patients SMIP could be seen to

increase over a series of measurementsessions, in parallel with increases inmeasures of peripheral muscle strength(handgrip) and diminishing levels ofrespiratory support. The MIP measures,however, show less evidence of change ineither subject.

How much of the SMIP increases aredue to a learning effect and how muchthey reflect genuine change over time isopen to debate. At each measurementsession, the subjects were encouraged to per form to their maximum until either fatigue affected performance ormotivation ceased. Often several dayselapsed between sessions, and it isunlikely that any learning effect wouldhave been retained. Wen et al (1997)found that although there was an intra-sessional learning effect for MIPmanoeuvres, this was not retained fromweek to week.

The reliability of SMIP measures hasbeen examined in normal subjects andpatients with pathology (Bruton et al,1999, 2001). They were found to be as reliable as other effort-dependent

Table 2: Serial ventilation parameters and muscle functionmeasures taken from Kevin over five sessions

Session Ventilation parameters Muscle function measuresFIO2 PS VT RR Peak MIP SMIP Grip

(cm H2O) (ml) (cm H2O) (ptu) (N)

1 0.50 20 465 35 35 14 83

2 0.45 20 505 38 32 38 103

3 0.40 VS NR 34 47 119 142

4 0.35 12 520 28 47 158 159

5 0.35 0 NR 25 47 269 163

Key to tables

FIO2 = fraction of inspired oxygen concentrationPS = pressure support VT = tidal volume VS = volume supportRR = respiratory rate (breaths per minute)NR = not recordedptu = pressure time unitsN = newtons

Table 1: Serial ventilation parameters and muscle functionmeasures taken from Julian over four sessions

Session Ventilation parameters Muscle function measuresFIO2 PS VT RR Peak MIP SMIP Grip

(cm H2O) (ml) (cm H2O) (ptu) (N)

1 0.45 26 527 24 42 38 58

2 0.35 23 620 15 43 86 91

3 0.35 15 575 22 67 140 149

4 0.35 8 520 22 70 188 182

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measures of muscle strength, eg hand-grip. The reliability of effort-dependentmeasures in patients in intensive care ismore difficult to establish due to therapidity of change in their condition.

Measurement reliability is essentially anestimate of the degree of consistencybetween measures. In intensive carepatients it is difficult to know whether any inconsistency in measures is due tothe measure itself, or to genuine changein the underlying variable. Globalinspiratory muscle function is not a staticentity, but is dependent on all theelements in the chain of command forany muscular contraction, ie volition,neural pathways, neuromuscular junction,muscle architecture, etc. There is alsosome evidence that efficient ventilationcan occur only when the inspiratorymuscles contract in a sequential and co-ordinated manner (De Troyer andEstenne, 1984).

As SMIP is a new measurement, itssignificance remains open to interpre-tation. It is the product of time ofcontraction and pressure generation(Chatham et al, 1994) and may reflect acombination of work potential and forcegeneration capacity. Work of breathing is the product of pressure change and volume change and since time ofcontraction and volume change arerelated, this new measurement reflectsmaximal capacity for inspiratory work.

Skeletal muscle endurance can bevariously defined as the capacity toperform repeated contractions and/or tosustain a single contraction, over aprolonged period of time. During theSMIP manoeuvre, maximal inspiratoryeffort is maintained over time, so that theinspiratory effort occurs throughout thefunctional range of the inspiratorymuscles. It is thus a dynamic manoeuvre,whereas the standard MIP is a static orquasi-static manoeuvre. The functionaland clinical implications of an ability tosustain maximal contractions of theinspiratory muscles throughout theirrange are not yet clear. The ability togenerate adequate force may not beentirely related to muscle strength butmay also relate to the ability to co-ordinate contraction of the inspiratory

muscles effectively. It is acknowledgedthat SMIP manoeuvres are open to thecriticisms that can be levelled at all effort-dependent measures. In particular, thereis uncertainty as to whether a low valuereflects genuine weakness, or simply lack of effort from the subject (Moxhamand Goldstone, 1994). Julian and Kevinseemed to be well motivated and makinggenuinely maximal efforts.

Physiotherapists working with criticallyill patients are well aware of the det-rimental effect that periods of mechanicalventilation can have on skeletal musclefunction. They are also familiar with thecommon complications associated withmechanical ventilation, such as noso-comial pneumonia, and the majority oftheir workload in intensive care unitsrelates to respiratory therapy.

The effects of mechanical ventilation on the inspiratory muscles are less welldocumented, however, primarily becauseof the difficulties surrounding assessmentof inspiratory muscle function in thissetting. Animal research suggests thatcontrolled mechanical ventilation (inwhich the ventilator does all the work)adversely affects the inspiratory muscles(Anzueto et al, 1997). Current practice isto use assistive modes of ventilation (inwhich the patient performs some of thework) and it is not yet clear what effectthese modes have on the inspiratorymuscles. However, when treating patientswho have received prolonged periods ofmechanical ventilation and are provingdifficult to wean, it is worth consideringthe possibility of inspiratory muscledysfunction.

ConclusionThe main hypothesis underlying thisinvestigation is that periods of prolongedmechanical ventilation have a detrimentaleffect on skeletal muscle function andhence inspiratory muscle function. IfSMIP is accepted as a reliable measure ofinspiratory muscle function, then theresults from these investigations supportthis hypothesis. These results also suggestthat SMIP is responsive to changinginspiratory muscle function over time, butas they are from uncontrolled studies, nofirm conclusions can yet be drawn.

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Key Messages

� The respiratory muscles are skeletalmuscles and respond accordingly toenvironmental change.

� Prolonged periods of mechanicalventilation are detrimental to allskeletal muscles including therespiratory muscles.

� In intubated patients sustainedmaximal inspiratory pressuremeasures seem to reflect inspiratorywork capacity better than standardmaximal inspiratory pressuremeasures.

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