Annals of the Rheumatic Diseases 1995; 54: 815-819

Use of high resolution computed tomography ofthe lungs in patients with rheumatoid arthritis

Bernard Cortet, Rene-Marc Flipo, Martine Remy-Jardin, Pascal Coquerelle,Bernard Duquesnoy, Jacques Remy, Bernard Delcambre

AbstractObjective-To assess the usefulness ofhigh resolution computed tomography(HRCT) of the lungs in patients withrheumatoid arthritis (RA) with and with-out respiratory symptoms.Patients and methods-Eighty eight RApatients with a mean duration of disease12 (SD 8) years were evaluated. Elevenpatients were excluded because of pre-vious exposure to silica. The 77 remainingpatients formed two groups accordingto the absence (group I, n = 38) or thepresence (group II, n = 39) of chronicrespiratory symptoms. A control groupconsisted of 51 non-smoking, healthypatients.Results-The most frequent abnormalitiesobserved in the 77 RA patients werebronchiectasis or bronchiolectasis (n = 23,30%), pulmonary nodules (n = 17, 22%),subpleural micronodules or pseudoplaques(n = 13, 17%/), ground glass opacities(n =11, 14%), and honeycombing (n = 8,10%). Bronchiectasis or bronchiolectasis(p = 0-012), rounded opacities (p = 0'016),ground glass attenuation (p = 0.004), andhoneycombing (p = 0.002) were found moreoften in RA group II (with respiratorysymptoms) than in group I (no respiratorysymptoms). Non-linear septal opacitieswere more frequent in group I than in thecontrol group, but other HRCT findingsdid not differ statistically significantlybetween group I and the control group.Conclusion-Bronchiectasis may be acharacteristic lung change in RA patients.Abnormalities on HRCT are less fre-quently observed in the absence of respir-atory symptoms than in the presence ofsuch symptoms (29% versus 69%).

(Ann Rheum Dis 1995; 54: 815-819)

Rheumatoid arthritis (RA) is a commonchronic inflammatory disease affecting about1% of the white population. Extra-articularmanifestations may involve, in particular, theskin (rheumatoid nodules), eyes, heart, andlungs. Since the first description oflung diseaseassociated with RA by Ellman and Ball in1948,1 several forms ofpleuropulmonary diseasehave been established in RA: pleural effusion/pleuritis, rheumatoid lung nodules, Caplan'ssyndrome, fibrosing alveolitis, lymphoid hyper-plasia with germinal centres, pulmonaryhypertension, constrictive bronchiolitis, and

bronchiectasis.2The prevalence of lung mani-festations in RA is not known with accuracy,and varies according to the method of diag-nosis. The chest radiograph, for example, maybe abnormal in 2-5% of patients with RA,2 butplain chest radiography is not sensitive enoughfor the diagnosis of lung involvement. Highresolution computed tomography (HRCT) is anon-invasive method of assessing interstitiallung disease (ILD), in particular, which hasrecently been shown to be useful in systemicsclerosis.3" The use of HRCT in RA is poorlydocumented, but the technique appears to beuseful when there is suspected clinical andradiological ILD.5 6 The aim of the presentstudy was to assess the usefulness of HRCT inRA patients with and without respiratorysymptoms, compared with a control group ofnon-smoking volunteers.

Patients and methodsPATIENTS

Eighty eight patients fulfilling the revisedcriteria for RA of the American RheumatismAssociation were reviewed.7 All had undergoneHRCT examination of the thorax between1987 and 1993. Among them, 11 patients whohad been exposed to silica were excludedbecause of possible confusion between rheu-matoid and pneumoconiotic lung lesions.HRCT had been performed in the remaining77 patients because of suspicion of associatedpulmonary disease, on the grounds of pul-monary symptoms or systematic evaluation oflung changes. In the latter case, the patientswere selected consecutively from one depart-ment ofrheumatology, the systematic evaluationof their lung changes was approved by theHospital Ethics Committee, and all patientsgave written informed consent to participate.The 77 patients comprised 51 women and 26men, mean age 57 (SD 10) years (range 36-79).Seventy one were non-smokers who had neversmoked and six were current smokers, meancigarette consumption 24 (20) packs/year(range 1-60 packs). The mean duration ofRAat the time of chest HRCT was 12 (8) years.Subcutaneous rheumatoid nodules were notedin 17 patients (22%) and rheumatoid factor in44 (57%). Nine patients (12%) were sufferingfrom Sjogren's syndrome (presence of siccasyndrome and positive labial salivary glandbiopsy (focus score> 1, stage III or IV onChisolm's classification8)). Functional capacitywas evaluated by Steinbrocker classification:912 were class I, 28 class II, and 37 class III.At the time of the HRCT examination, 63 of

Department ofRheumatology,CHRU Lille,H6pital B,2 Avenue OscarLambret,59037, Lille Cedex,FranceB CortetR-M FlipoP CoquerelleB DuquesnoyB DelcambreDepartment ofRadiology,CHRU Lille,Hopital Calmette,Boulevard JulesLeclerc,59037, Lille Cedex,FranceM Remy-JardinJ RemyCorrespondence to:Bernard Cortet,Department ofRheumatology,CHRU Lille, H6pital B,2 Avenue Oscar Lambret,59037, bille Cedex,France.

Accepted for publication26 June 1995

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the 77 patients were receiving corticosteroidsor second line drugs: glucocorticoids (n = 49);methotrexate (n = 24); tiopronine (n= 10);sodium aurothiomalate (n = 7); sulphasalazine(n = 7); hydroxychloroquine (n = 1). The patientswere allocated to two groups according tothe absence (group I, n = 38) or presence(group II, n = 39) of respiratory symptomssuch as cough (in the morning or all day),sputum production (in the morning or all day),or dyspnoea.A control group comprised 51 healthy

subjects who had never smoked and whowere previously enrolled in a prospective studyassessing HRCT of the lungs in healthy adultvolunteers.'0 There were 34 women and 17men (mean age 33 (8) years), all urbandwellers and recruited from workers in ourhospital. None had a past history of lungdisease and, in particular, none had previouslyundergone chest surgery or suffered from arespiratory illness such as bronchiolitis of anyorigin in previous years or in infancy. Somecontrol patients had respiratory symptoms:cough (n = 4; morning, n = 3; all day, n = 1),sputum production in the morning (n = 2), anddyspnoea occurring after strenuous activitysuch as climbing three flights of stairs, heavyhousework, or walking more than one mile onlevel ground (n = 8).

METHODS

HRCT of the thorax was performed with eitheran Elscint 2400 (Hackensak, NJ) or a SiemensSomatom Plus (Erlangen, Germany). Serialslices were taken through the chest, each 1 mmin width and 10 mm apart. Technical factorswere 130 kV and 420 mA (Elscint CT unit) or137 kV and 255 mA (Siemens CT unit).Images were reconstructed using a high spatialfrequency algorithm for parenchymal analysisand a standard algorithm for mediastinalevaluation. HRCT studies were performed atsuspended end inspiratory volume with onesecond (Siemens) or two seconds (Elscint)scan time with patients in the supine position.In cases of limited joint mobility, especiallyinvolving the shoulders, HRCT scan was per-formed with the patient's arms positionedalongside the body, without any effect on theimage quality. The HRCT examinations wereinterpreted by two radiologists blind to theclinical history, who reached a concensus

High resolution computed tomography (HRCT) findings in patients with rheumatoidarthritis (RA) without (group I) and with (group II) respiratory symptoms

HRCTfinding Group I Group II Control group(n = 38) (n = 39) (n = 51)

Bronchial wall thickening 2 (5) 11 (28) 9 (18)Bronchiectasis or bronchiolectasis 3 (8) 20 (51)* 0Rounded opacities 4 (11) 13 (33)* 11(22)Septal lines 0 0 4 (8)Non-septal linear opacities 5 (13) 9 (23) 0*Ground glass attenuation 1 (3) 10 (26)** 0Honeycombing 0 8 (23)** 0Dependant areas of attenuation 1 (3) 4 (10) 6 (12)Distortion 1 (3) 4 (10) 0Emphysema 2 (5) 2 (5) 0Enlarged lymph nodes 2 (5) 5 (13) 0Enlarged pulmonary arteries 0 1 (3) 0Pleural abnormalities 3 (8) 9 (23) 0

n = Number of patients with HRCT findings. Number in parentheses are percentage. *p < 0-05,**p < 0-01 compared with group I.

decision. Multiple radiological criteria for thediagnosis of lung involvement were assessed,including site and severity. The major abnor-malities screened for were: rounded opacities(parenchymal micronodules = rounded lesionsless than 3 mm in diameter; nodules = roundedlesions greater than 3 mm in diameter;subpleural micronodules = areas of hyper-attenuation less than 3 mm in diameter);ground glass attenuation (bronchi and vesselsvisible); dependent areas of attenuation(bronchial walls and vessels obscured); septallines and non-septal lines; honeycombing(areas of cystic spaces with thickened walls);bronchiectasis (abnormal visualisation ofproximal airways); bronchiolectasis (abnormalvisualisation of airways in peripheral locations:dilated bronchiolar division visualised alongtheir length when horizontal, or peripheralsignet ring signs when coursing in a verticaldirection; architectural distortion; emphysemacharacterised by areas of decreased attenuationand disruption of the vascular pattern.

Statistical comparisons between the differentgroups of patients were made using the x2 testwith Yates' correction if necessary. Correlationcoefficients were calculated by linear regressionanalysis.

ResultsThe table summarises the results.

HRCT IN RA PATIENTS

HRCT was abnormal in 38 (49%) of the 77 RApatients- 1 from group I (29%) (no respir-atory symptoms) and 27 from group II (69%)(with respiratory symptoms) (p < 0 001).The most frequent abnormality on HRCT of

the lungs was bronchiectasis or bronchiolectasis(figure), observed in 23 patients (30%)-threepatients in group I (8%), and 20 patients ingroup II (51%) (p = 0 0 12)-and consisted ofhoneycombing in seven ofthem. Among the 16with bronchiectasis or bronchiolectasis but nohoneycombing, 14 patients were non-smokerswho had never smoked. Specific evaluationof these 14 non-smoking patients showedbronchiectasis or bronchiolectasis associatedwith diffuse bronchial thickening in all butone; in four, airway changes were the soleabnormality on HRCT examination, and in10 the airway changes were associated withparenchymal micronodules (n = 6), dependentareas of attenuation (n = 4), subpleural micro-nodules or pseudoplaques (n = 4) and emphy-sema (n = 2).Rounded opacities were observed in 17 patients

(22%). Three types were identified accordingto their size and location: parenchymal micro-nodules (n = 6), nodules (n = 3), and subpleuralmicronodules or pseudoplaques (n = 13).

In the absence of respiratory symptoms(group I), rounded opacities were observed infour patients (111%), peripheral parenchymalmicronodules in two, and subpleural micro-nodules in two. In group II (with respiratorysymptoms), 13 patients (33%) had roundedopacities: parenchymal micronodules in four,

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High resolution computed tomography of the lungs in patients with RA

HRCT IN THE CONTROL GROUPAbnormalities were evident on HRCT in 22control patients (43%). The most frequentabnormality was subpleural micronodules(n = 11, 22%); others were: bronchial wallthickening without any other bronchialabnormality (n 9, 18%), dependent areas ofattenuation (n =6, 12%) and septal lines(n = 4, 8%). A significant correlation betweeneach respiratory symptom and HRCT findingswas found only for bronchial wall thickening

- ~ (p -

0 009).C5ti-n:

11 63C

Bronchiectasis: cylindral dilatation ofperipheral bronchi in the lower lobes and in tilingula, with mild bronchial wall thickening in the posterior segment of the right k

parenchymal nodules in three, and sutmicronodules in 11. This difference betwgroups was statistically significant (p = (

Non-septal linear opacities were obse14 patients (18%) and were always locperipheral lung tissue. Such abnornwere the sole HRCT findings in six Iand were associated with honeycomleight; they were exclusively or predomin the lower lung zones in all cases.

Five patients (13%) had non-septaopacities in the absence of respiratorytoms (group I) and nine (23%) wifeature had respiratory symptoms (gr(difference between groups not significaGround glass attenuation representin

active alveolitis was found in 11 patients-one in group I (3%) and 10 in gi(10%) (p = 0 004). It was usually bilatesymmetrical.Honeycombing highly suggestive ofpui

fibrosis was detected in eight patientsand comprised a microcystic pattern (na combination of microcystic and maci

honeycombing (n = 3). Honeycombiralways bilateral and asymmetrical, ai

associated with bronchiectasis or br(lectasis in seven patients, groundattenuation in seven, non-septalopacities in all cases, and pleural thickepleural effusion in five. Evidence ofcombing was always associated with pof respiratory symptoms (significant difbetween groups (p = 0.002)).The presence of respiratory symptoms

dyspnoea or sputum production) was

cantly correlated with the followingfindings: rounded opacities (p =ground glass attenuation (p = 0 004),combing (p = 0-002), and bronchiectbronchiolectasis (p < 0-001).

COMPARISON OF HRCT IN RA PATIENTS AND

CONTROLS

Bronchiectasis or bronchiolectasis (p < 000 1),septal lines (p = 0 05), non-septal linear opacities(p < 0 01), ground glass attenuation (p < 0 01),honeycombing (p < 0-05), and pleural abnor-malities (p < 0O01) occurred more frequently inRA patients than in the control group.Non-septal linear opacities was the sole abnor-mality observed more frequently on HRCT in

i RA patients without respiratory symptomshe (group I) than in control patients (p < 00 1).9wer lobe.

Discussion)pleural The most frequent abnormality depicted on

teen the HCRT in our study was bronchiectasis or

D-016). bronchiolectasis-found in 23 patients (30%).rved in While seven of these patients had lung changes:ated in (honeycombing) considered as indirect signs ofmalities pulmonary fibrosis, the remaining 16 RApatients patients with abnormalities in the absence ofbing in features of lung fibrosis included 14 non-

linantly smokers who had never smoked. This stronglysuggests that neither smoking nor an increased

1 linear susceptibility to its effects were the mainsymp- causes for the development of bronchiectasis

ith this or bronchiolectasis. In addition, we failedoup II) to observe bronchiectasis/bronchiolectasis innt). our control group of non-smokers, among.g early whom bronchial abnormalities consisteds (14%) solely of bronchial wall thickening which couldroup II be explained by occupational exposure to~ral and pollutants or other environmental factors

(urban dwellers). An association betweenImonary bronchiectasis and RA is well known," but it(10%) remains unclear if bronchiectasis occurs in= 5), or severe RA and if it is accompanied by otherrocystic extra-articular manifestations.'2 13 McDonagh,ng was et al, using HCRT, found bronchiectasis innd was four of 20 RA patients (20%), but none wasonchio- suffering from clinical symptoms of respiratory1 glass disease.6 In the same study, the authorslinear observed bronchiectasis in 30% of the patients

ning or with interstitial lung disease. On the basis ofhoney- pulmonary function tests, it has been shownIresence that airway disease may be the commonestEference form of RA lung involvement;'4 in other RA

patients, low values of forced expiratory(cough, volume in one second (FEVI), forced vitalsignifi- capacity (FVC), FEV1/FVC, and a significantHRCT high prevalence of bronchial reactivity to0-016), inhaled methacholine have been reported. 15honey- The most common explanation is that:asis or bronchiectasis in RA patients results from

frequent respiratory tract infections.'6 The

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predominant location of bronchiectasis orbronchiolectasis in the lower zones of the lungssupports this hypothesis. In addition, alpha-1antitrypsin deficiency has been suggested toincrease the risk of lung involvement in RA.'7Rounded opacities, found in 22% of our

patients, were the second most frequentlyobserved abnormality. Their location and sizewere consistent with the characteristic sub-pleural location of rheumatoid nodules.'8Pulmonary nodules are usually symptomless,or contribute little to pulmonary dysfunction;however, they can grow in size and tend torupture into the pleura causing pneumo-thorax, hydropneumothorax, or even pyo-pneumothorax, as observed in one of ourpatients.19 20 The frequency of parenchymalnodules in our patients (three in 77-4%) waslower than that reported from pathologicalstudies18 and on previous HRCT scan studies,6even though HRCT is able to demonstratelung nodules in the rheumatoid populationmore frequently than plain radiographs(fewer than 1% of rheumatoid nodules areestimated to be radiographically detectable21 ).We observed subpleural micronodules in 17%of our RA patients; although subpleural micro-nodules were identified in 22% of our controlgroup, several CT findings suggest theirpossible relationship with rheumatoid lungdisease. Subpleural lesions in RA patients areobserved in the upper, mid and lower lungzones, whereas in healthy adults subpleuralmicronodules are exclusively located in theupper part of the lungs."'Ground glass opacification representing an

early stage of active alveolitis was the fourthmost frequent HCRT abnormality we detected(14%). Discovery of such an abnormality onHRCT could indicate early aggressive treat-ment to prevent irreversible fibrosis.Honeycombing was present in eight patients

(10%), always bilateral and asymmetrical,with a predominant peripheral and inferiordistribution. These morphological features arein agreement with those previously reported inthe literature,22 23 and are indistinguishablefrom pulmonary fibrosis caused by otherconnective tissue diseases.24 Although inter-stitial lung disease is a well known extra-articular manifestation of RA, its prevalence isclosely related to the diagnostic tool used forits recognition. Pathological studies haveshown interstitial lung disease in up to 80% ofpatients,18 25 whereas interstitial lesions areradiographically identified in fewer than 5%.26Although the aim of this study was not tocompare chest radiography with lung HRCT,we are able to confirm the lack of sensitivity ofplain chest radiography, as 90% of our patientssuffering from lung fibrosis had a normal chestradiograph.Emphysema was seen in 5% of our RA

patients, whereas McDonagh et a76 found itin 20%. Tobacco smoking may explain thisdifference, as 80% of their patients werecurrent smokers, whereas 90% of those in ourstudy were non-smokers and had never smoked.The prevalence of HRCT findings accordingto the absence or presence of respiratory symp-

toms likewise differed between these studies.Among our 38 patients with respiratory symp-toms, abnormalities on HRCT were observedin 29 (69%), while only 11 (29%) of our 39patients without respiratory symptoms hadHRCT abnormalities. In contrast, McDonaghet al observed on HRCT a prevalence of lunginvolvement in up to 75% of asymptomaticrheumatoid patients.6 However, most of thesepatients were current smokers and the HRCTabnormalities probably reflected a greaterinfluence of tobacco than of RA. The signifi-cance of the abnormalities we demonstratedin the absence of respiratory symptoms isunknown, as we did not perform pulmonaryfunction tests. While McDonagh's group didnot find any significant difference on pul-monary function testing between RA patientswith clinical evidence of interstitial lung diseaseand control RA patients, when the pulmonaryfunction of the group of 20 patients with ILDwas compared with that of 10 patients withnormal HRCT, or nodules or pleural diseasealone, reductions in FEV, and lung carbonmonoxide transfer factor became significant.6Apart from the non-septal linear opacitieswhich were more frequent in our RA patientswithout respiratory symptoms (group I) than incontrol patients, the frequency of HRCTabnormalities was similar in these two groups.However, the fact that these groups were notage matched should be taken into accountwhen interpreting this result. Finally, in theabsence of respiratory symptoms, slight groundglass opacification representative of activealveolitis was demonstrated in only onepatient, and the honeycombing considered toindicate lung fibrosis was not observed.

In summary, HRCT is a useful diagnostictool in the assessment of lung involvement inpatients with respiratory symptoms and offersinformation not readily obtained from plainchest radiography. The significance of theseveral abnormalities which were observed inthe absence of respiratory symptoms remainsunclear and requires subsequent longitudinalstudies.

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