Thorax 1994;49:557-561

Regional lung clearance during cough and forcedexpiration technique (FET): effects of flow andviscoelasticity

A Hasani, D Pavia*, J E Agnew, S W Clarke

Department ofThoracic MedicineA HasaniD PaviaS W Clarke

Department ofMedical PhysicsJ E Agnew

Royal Free Hospitaland School ofMedicine, LondonNW3 2QG

Reprint requests to:Dr A Hasani.* Present address:Boehringer Ingelheim (UK)Ltd, Bracknell, BerkshireRG12 8YS, UK.

Received 14 July 1993Returned to authors8 December 1993Revised version received14 February 1994Accepted for publication17 February 1994

AbstractBackground - In vitro studies have sug-gested that both the viscoelastic proper-ties of lung secretions and the peak flowattained during simulated cough influ-ence clearance. This study examines thepossible association of the viscoelasticproperties of sputum and maximumexpiratory flow with measured effective-ness of mucus clearance induced byinstructed cough and by forced expi-ration technique (FET) in patients withairways obstruction.Methods - Nineteen patients (11 men andeight women) of mean (SE) age, % pre-dicted FEV1, and daily sputum wet weightof 64 (2) years, 52 (6)%, and 37 5 (7 9) grespectively participated in the study.Mucus movement from proximal andperipheral lung regions was measured byan objective non-invasive radioaerosoltechnique. Each patient underwent threeassessments: control, cough, and FET.During cough and FET, maximum expir-atory flow was measured at the mouthlevel. Apparent viscosity and elasticity ofthe expectorated sputum samples weremeasured with a viscometer.Results - Compared with the control run(mean (SE) clearance: 16 (3)%) there wasan increase in clearance from the wholelung during cough (44 (5)%) and FET (42(5)%), and also an enhanced clearance ofinhaled, deposited radioaerosol from thetrachea, inner and intermediate regionsof the lungs, but not from the outer re-gion. There were, however, no differencesin regional clearance between cough andFET. Neither regional nor total clearancecorrelated with maximum expiratoryflow, apparent viscosity, elasticity, ordaily sputum wet weight.Conclusions - These results confirm thatcough and FET both promote effectiveclearance but suggest that, unlike in vitrostudies, sputum production and visco-elasticity, as well as maximum expira-tory flow, provide no guide to clearanceefficacy in humans.

(Thorax 1994;49:557-561)

Cough is a reserve defence mechanism forremoval of lung secretions.' It is particularlyimportant as a back-up mechanism in airway

diseases where mucociliary transport - theprimary host defence mechanism for mucusclearance - is often compromised.23 In health,cough comes into action during emergencysituations such as following the inhalation of aforeign body.

Several studies have addressed the questionof the efficacy of cough in clearing inhaled,deposited radioaerosols from the lungs ofhealthy non-smokers,s6 asymptomaticsmokers,7 and patients with lung disease.4514Only four of these studies examined the effec-tiveness of cough in clearing lung secretions ona regional basis from the lungs.8 1014 The otherstudies considered effectiveness only for mu-cus clearance from the lungs as a whole. Theregional clearance studies have given conflict-ing evidence as to the effectiveness of cough inperipheral regions of the lungs.The forced expiratory technique (FET) or

"huffing" was introduced by physiotherapistsas an alternative to coughing for the removal ofexcess lung secretions.'5 Its introduction wasbased on the claim that it reduces transpul-monary pressure compared with cough,thereby resulting in less airway compressionand closure.'6 Its effect on mucus clearancefrom the lungs as a whole using radioaerosolshas been studied in patients with hypersecre-tion."We now report a study on the effect of cough

and FET on regional mucus clearance in agroup of patients with airways disease andvarying amounts of daily sputum production.This study also examined the possible associ-ation between cough/FET and the maximumexpiratory flow attained during thesemanoeuvres, the viscoelasticity of the expect-orated secretions, and a measure of hyper-secretion in these patients.

MethodsPATIENTSNineteen patients (1 1 men, eight women) witha mean (SE) age of 64 (2) years participated inthe study. Twelve patients (six women) hadchronic obstructive pulmonary disease(COPD) and seven (two women) had bron-chiectasis. Fifteen patients were on inhaledbronchodilators of whom eight were also tak-ing oral bronchodilator therapy, and 12 weremaintained with inhaled corticosteroid ther-apy (one of them was also taking oral cortico-steroids). One patient was on home nebuliserbronchodilator therapy and four patients (two

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COPD and two bronchiectasis) were on nomedication. The mean (range) increase inFEV, following the administration of twopuffs (100pg each) of salbutamol was 9 (0-40)%. The group comprised four non-smokerswith bronchiectasis, two current smokers withCOPD (46 and 68 pack-years), and 13 ex-smokers with a mean (SE) of 31 (4) pack-years.The mean (SE) daily sputum wet weight pro-duction for the group was 37 5 (7 9) g.

STUDY DESIGNThe study was designed in a randomised, threeway, crossover (within patients) manner. Eachpatient attended our laboratories on threeoccasions separated by at least three days.During each visit the patient underwent anidentical experimental procedure but per-formed one of three treatment manoeuvres.These manoeuvres were cough, FET, andcontrol which were all carried out with thepatient sitting in the upright position. Duringthe cough manoeuvre the patient wasinstructed to perform six coughs (each coughafter full inspiration) per minute, repeated fivetimes, with a rest period of one minutebetween each series of six coughs. During theFET manoeuvre the patient was instructed toperform six forced expirations per minute withthe glottis open, starting from approximatelymid lung volume and ending the exhalationclose to residual volume, for five minutes withone minute rest period after every six forcedexpirations. During the control manoeuvre thepatient just rested with no coughs or forcedexpirations.Maximum expiratory flow during the cough

and FET manoeuvres was measured at themouth using a Vitalograph Compact spiro-meter which employed a Fleisch type pneumo-tachograph. The mean value of the maximumexpiratory flows measured for the 30 coughs orFETs was calculated for each patient.The patients were asked to refrain from

taking any inhaled bronchodilators for at leasttwo hours before each visit to the laboratories.

Informed written consent was obtainedfrom all the patients and the study wasapproved by the hospital's Ethical PracticesSubcommittee.

RADIOAEROSOL TECHNIQUEAn objective radioaerosol technique, whichhas previously been described in detail, wasused to assess movement of mucus within thepatients' lungs.7 18 Polystyrene particles (5 ,umin diameter) labelled'9 with technetium-99mwere inhaled under controlled conditionsthrough the mouth. Each patient, while seatedand wearing a nose clip, inhaled discretebreaths (0 45 litre) from the resting level of thelungs followed by a three second breath holdpause in order to enhance deposition of theradioaerosol in the peripheral airways of thelungs.20 The patient gargled and drank somewater after inhaling the radioaerosol to clearany deposited particles from the oropharynx

and oesophagus. Two axially opposed, colli-mated scintillation detectors located antero-posteriorly to the chest were used to ascertainthe radioactivity present in the lungs immedi-ately after inhaling the radioaerosol and 24hours later. The 24 hour particle retention wasexpressed as a percentage of the initial valueafter being corrected for background radiationand physical decay of the radionuclide and wastaken to represent "alveolar deposition"within the lungs.2'

REGIONAL CLEARANCEA large field-of-view gamma camera (OhioNuclear-110) linked to a computer (NuclearDiagnostics) was used to assess the initialtopographical distribution and subsequentclearance of the radioaerosol particles from thelungs. The initial distribution of the particleswas expressed quantitatively as a penetrationindex which is the ratio of the amount ofradioaerosol in an outer to inner region of thelungs divided by the same ratio for krypton-81m gas.22 The measurement of the radioaero-sol clearance was based on dividing the gammacamera images (64 x 64 format) of the lung intofour arbitrary regions (fig 1). The four regionswere a tracheal region which comprised mainlythe trachea, an inner region which comprisedmainly large airways, and intermediate andouter regions which comprised mainly smallairways. A posterior 8'mKr ventilation imagewas taken for each patient to assess the outeredges of the lungs (15% and 30% contours),and was adjusted to align with the aerosolimages. A 5 x 8 matrix was fitted as closely aspossible to the outer contours of the 8lmKrimage to define the four regions of the lung.23The regional clearance of the radioaerosol par-ticles was corrected for alveolar deposition andinter-regional movement.

Images of the distribution of the radioaero-sol particles within the lungs were taken im-mediately before and after each of the threetreatment manoeuvres which were com-menced within 10-15 minutes after theradioaerosol inhalation.

RHEOLOGICAL PROPERTIES OF SPUTUMThe patients were provided with containersand instructed to collect all sputum producedover a 24 hour period before each visit. Thedaily sputum production for each patient wasdescribed by the mean wet weight for the threesputum collections. All sputum samplesexpectorated during the cough and FET ma-noeuvres were collected and the wet weightwas ascertained.The viscoelastic properties - that is, appar-

ent viscosity (rj) in mPa-s and elasticity (G') inmPa - were measured only in sputum samplescollected during the cough and FET ma-noeuvres. A Contraves Low Shear 30 Sinusviscometer was used,24 and measurements weretaken at a frequency of 0-325 Hz and a temper-ature of 37'C. Whenever possible, threesamples of 1 ml in volume were tested withinone hour of production for each patient andthe results were expressed as the mean.

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Effect offlow rate and viscoelasticity on cough/FET

Figure 1 Definition offour regions relative to contours (15% and 30%) of 81"Krventilation image.

PULMONARY FUNCTIONForced expiratory volume in one second(FEV,), forced vital capacity (FVC), and max-imum mid expiratory flow rate (MMF25-75)were measured with a Vitalograph spirometerfor each patient. A Wright peak flow meter wasused to measure peak expiratory flow rate(PEF). Flow rates at 25% and 50% of vitalcapacity (Vmax25, Vmax50) were measured withan Ohio 840 spirometer. For each of the pul-monary function indices the best of three tech-nically acceptable measurements was recordedand expressed as % predicted value based onthe subject's sex, age, and height.25 26 Thepulmonary function tests were carried out oneach of the three visits after the radioaerosolassessments were completed in order not todisturb the lung secretions.

DATA ANALYSISThe data were analysed using the non-para-metric paired Wilcoxon and Spearman rankcorrelation tests.27 The level of significancewas taken at p < 0Q05.

ResultsThe mean (SE) pulmonary function indices forthe patients during the three visits are given intable 1. Pulmonary function remainedunchanged between the visits.The initial topographical distribution of the

radioaerosol within the lungs was similar

Table 1 Mean (SE) % predicted pulmonary functionindices for the patients during the three study visits

Pulmonary function indices Control Cough FET

FEVI 50 (5) 53 (5) 52 (6)FVC 69 (5) 73 (4) 71 (5)PEF 50 (5) 53 (5) 52 (5)MMF2575 28 (5) 29 (6) 28 (5)YMaX50 22 (4) 21 (4) 23 (4)Vmax25 24 (5) 24 (4) 25 (4)

FEV, = forced expiratory volume in one second; FVC = forcedvital capacity; PEF =peak expiratory flow rate; MMF25-75 =maximum mid expiratory flow rate; Vmax50 and Vmax25 = flowrates at 50% and 25% of vital capacity.

between the three runs. Mean (SE) alveolardeposition was 24 (2)%, 25 (2)%, and 24 (2)%,and penetration index was 0-38 (0 05), 0 39(0 05), and 0 39 (0 04) for the control, cough,and FET runs respectively. Figure 2 shows thepercentage of initial tracheobronchial deposi-tion of the radioaerosol in the four regions ofinterest of the lungs for the three runs. Thedistribution for any one region between thethree runs was similar.

Tracheobronchial clearance from the lungsas a whole measured with the scintillationdetectors showed that clearance was signific-antly enhanced (p <0-01) following cough (44(5)%) and FET (42 (5)%) compared withcontrol during which the patients did notcough (16 (3)%). Following the pulmonaryfunction tests (which themselves involved nineforceful expiratory manoeuvres) tracheobron-chial clearance was significantly faster(p<0 05) for the control run (22 (4)%) com-pared with both cough (10 (1)%) and FET (9(2)%).

Figure 3 illustrates the regional tracheo-bronchial clearance for the manoeuvres.Cough and FET significantly enhanced clear-ance of radioaerosol from the trachea, inner,and middle regions of interest of the lungs, butnot from the outer region. There were, how-

S 50 S Cough

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Figure 3 Mean (SE) tracheobronchial clearance of theradioaerosol from the four regions of the lungs during thethree manoeuvres.

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ever, no differences in regional clearancebetween cough and FET.The mean (SE) maximum expiratory flow

recorded during cough (288 (29)1/min) wassignificantly (p < 0 01) higher than that duringFET (203 (25) 1/min). The higher flowsmeasured during cough may be attributed tothe higher lung volumes from which this ma-noeuvre commenced compared with the FETmanoeuvre. The amount of sputum producedunder instruction was identical between thecough and FET (3 4 (0 5) g) runs. Four of the19 patients produced small amounts of sputumduring the cough and FET manoeuvres whichwere insufficient for assessment of their visco-elastic properties. The apparent viscosityvalues for the sputum samples produced dur-ing the cough (693 (78) mPa-s) compared withFET (684 (106) mPas) runs were similar, aswere the elasticity values (2979 (503) mPa v3054 (560) mPa respectively).There was no correlation between regional

clearance and any of the following: maximumexpiratory flow attained during the ma-noeuvres, the apparent viscosity and elasticityof sputum (fig 4), the amount of sputum expec-torated during the manoeuvres, and the dailysputum production of the patients before thestudy. Table 2 gives the correlation coeffi-cients for the comparison between clearancefrom the four regions of interest of the lungsand apparent viscosity and elasticity of sputumand maximum expiratory flow.

DiscussionOur observations of an enhancement ofwhole lung radioaerosol clearance followinginstructed cough confirm previous observa-tions reported by other workers on smallernumbers of patients.451 Furthermore, the en-hancement of whole lung radioaerosol clear-ance following FET is in keeping with theobservations of Sutton and coworkers."On theoretical grounds and using Weibel's

model of the human lung Leith28 postulatedthat cough may be effective in clearing secre-tions from the trachea down to the seventh oreighth airway generation. Scherer,29 however,using an in vitro model, suggested that coughin the presence of hypersecretion may be effec-tive in clearing secretions from airways as faras the respiratory bronchioles. Our data onregional clearance show that cough is effectivein clearing secretions from the inner and inter-mediate regions, in keeping with observationsfrom other published data. However, clearanceof secretions from the outer region due tocough failed to attain statistical significance.

Table 2 Spearman correlation coefficients (rs) for comparison between clearance(%) from the four regions of the lungs and apparent viscosity and elasticity of sputumand maximum expiratory flow during cough and FET

Tracheal Inner Intermediate Outer(Cough/FET) (Cough/FET) (Cough/FET) (Cough/FET)

Viscosity (q) -0 24/- 0-34 -0-05/-0-19 0 27/-0 11 -0 01/-0-14Elasticity (G') - 009/-0-31 0 004/- 0-25 0-40/-0-01 0 10/- 025Maximum flow -0 18/0 01 -0-01/0 07 -0-26/0-21 -0-28/0-18

p not significant for all regions.

This is in agreement with a much earlier coughstudy from our laboratory,8 but contrasts withthose reported by Oldenburg et a19 and Ross-man et al.'0 The apparent discrepancy mayhave arisen because of differences in the selec-tion of regions of interest between those stud-ies, and because more of the radiotracer (20%approximately) was deposited in the outer re-gion in the studies from our laboratory than inthe other two studies (12 5% approximately).The present study shows that FET on its

own is effective in clearing secretions from theinner and intermediate regions of the lungscompared with control runs. As such its role inphysiotherapy for the clearance of lung secre-tions with reduced peak flows must be advo-cated as an alternative to cough.30

Early studies have indicated that, for coughto be effective in clearing inhaled radioaerosolfrom the lungs, the presence of hypersecretionis essential.45 More recently Bennett et al haveshown a small improvement in whole lungclearance following 60 controlled coughs overa one hour period in healthy subjects,6 but notin a group of asymptomatic smokers.7 Thenumber of coughs used by Bennett et al werefar in excess of those used by other investig-

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Figure 4 Enhancement of inner region clearancefollowing cough and FET over control for the studygroup compared with (A) apparent viscosity and(B) elasticity of sputum expectorated during thesemanoeuvres.

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Effect offlow rate and viscoelasticity on cough/FET

ators. Mucus clearance by cough and FET inour study was not correlated with the amountof sputum produced during the forceful expir-atory manoeuvres, nor with the daily sputumproduction of the patients which was taken tobe a rough guide of their hypersecretory state.

The enhanced clearance during the pulmon-ary function testing (which required nineforceful expiratory manoeuvres) in the controlrun compared with the other two runs was

predictable. These exhalatory manoeuvres

enhanced the clearance of the excess secretionswhich were still present in the airways duringthe control run, whereas in the other two runs

instructed cough and FET had already helpedto expel the excess secretions.

It is acknowledged that sputum may not berepresentative of the quality and quantity ofmucus in the airways. Nevertheless, it serves

as an acceptable surrogate. Alternative means

of accessing secretions from the airways are

invasive and, as such, may in themselves alterthe properties of the secretions.

In vitro studies"-" using simulated mucus

with apparent viscosity in the range of 1-77Pa s have suggested that cough is more effec-tive in less viscous material. The lack of a

correlation between mucus clearance by coughor FET and viscoelasticity of expectoratedsecretions in our study may possibly beexplained by the fact that the viscosity of thesputum samples ranged over a much narrower

"window" (0 3-1 7 Pa s). The in vitro studiesmay therefore wrongly predict what actuallyhappens in vivo. The lack of a correlationbetween mucus clearance by cough or FETand elasticity of expectorated secretions in thisstudy also contrasts with published in vitrostudies3132 which suggest that elastic forces inthe mucus gel impede cough clearance. Clear-ance stimulated by cough has been reported to

be impaired by increases in spinnability andadhesivity of mucus simulants."Again in vitro studies3' 32 using mucus simu-

lants have indicated that cough clearance issignificantly enhanced with increases in peakflow rate. Our studies in patients do not con-

firm this and, indeed, show that FET andcough result in similar radioaerosol clearancesfrom the lungs despite a statistically significantreduction (mean 30%) in maximum expiratoryflow during the former manoeuvre. A possibleexplanation for this might be that although themaximum flow rates during FET are lowerthan those attained during cough, theirduration could be substantially longer thanthose for cough and thus make them equallyeffective in clearing lung secretions.

In conclusion, our study confirms in a sub-stantial number of patients that cough andFET are equally effective in clearing lungsecretions, although the latter can be achievedwith less effort on the part of the patient.Furthermore, our study indicates the possiblerisks in extrapolating data from in vitro stud-ies"'"33 to what actually happens in clinicalpractice.

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