Thorax 1994;49:793-797

Pulmonary sarcoidosis with a diffuse ground glasspattern on the chest radiograph

Abdellatif Tazi, Tsellina Desfemmes-Baleyte, Paul Soler, Dominique Valeyre,Allan J Hance, Jean-Paul Battesti

AbstractBackground- Several chest radiographicabnormalities have been described in pul-monary sarcoidosis, but a diffuse groundglass pattern is extremely rare.Methods-The chest radiographs of morethan 1600 patients with sarcoidosis eva-luated in our service between 1976 and1991 were reviewed to determine the pre-valence of this pattern on chest radio-graphy at presentation, and to assess theclinical characteristics of these patients.Results-Ten patients (0-6%) were identi-fied with diffuse ground glass abnormalit-ies on the chest radiograph (eight men);all had associated hilar or mediastinaladenopathy. All patients were white andnine were smokers or former smokers.Nine patients were symptomatic and sixhad inspiratory crackles on physical ex-amination. As a group these patients wereremarkable for the frequency and sever-ity of physiological abnormalities and thepresence of various findings typically as-sociated with "active" disease. Ninepatients were followed for more thanthree years. All were treated with oralcorticosteroids because of significantsymptoms or physiological abnormalit-ies, or both. Symptoms and radiologicalabnormalities disappeared or improvedin all patients, but recurred in a highproportion when steroids were tapered ordiscontinued. By December 1992 onlythree patients had been withdrawn fromtreatment.Conclusions-A diffuse ground glass pat-tern on the chest radiograph is unusual inpatients with sarcoidosis and may occurmore commonly in white subjects andcigarette smokers. Its presence suggeststhe existence of active disease of recentonset likely to require long term treat-ment with corticosteroids.

(Thorax 1994;49:793-797)

Sarcoidosis is a multisystem disorder ofunknown aetiology characterised by the pres-ence of non-caseating granulomas at sites ofinvolvement.lA Although most organs can beaffected by the disease, the lung and thoraciclymph nodes are the most common sites andapproximately 900o of patients with sarcoidosishave an abnormal chest radiograph.'"

Various radiographic patterns have been de-scribed in patients with pulmonary parenchy-mal involvement. In patients with parenchymalabnormalities a reticulonodular pattern is most

commonly observed,5 but other less commonpatterns have been reported.5 A diffuseground glass pattern - defined as a homo-geneous opacification in which normal anatomi-cal details of the lung are still visible but givinga hazy appearance to the lung fields8 - is mainlyobserved in hypersensitivity pneumonitis, par-ticularly in the acute form of farmer's lung,9 andhas also been described in some patients withearly stages of asbestosis and berylliosis.5 Adiffuse ground glass pattern on the standardchest radiograph is extremely rare in sarcoido-sis, although ground glass opacities (usuallylocalised) have been observed with high resolu-tion computed tomographic scanning of thelung.'101We have recently encountered a patient with

sarcoidosis who presented with a ground glasspattern on chest radiography. To further in-vestigate this association we have reviewedradiographs of more than 1600 patients withsarcoidosis evaluated at our unit to determinethe prevalence of a diffuse ground glass patternat the time of diagnosis and to better define theclinical characteristics and prognosis of thesepatients.

MethodsSTUDY POPULATIONSAll patients with pulmonary sarcoidosis eva-luated at H6pital Avicenne between January1976 and December 1991 were included. Thediagnosis of sarcoidosis was based on previouslydescribed criteria, including the presence ofnon-caseating granulomas in a biopsy specimenof involved tissue or the site of a Kveim-Siltzbach reaction.'2 Patients whose chest radio-graph taken at diagnosis demonstrated a diffuseground glass pattern - defined as a homo-geneous opacity affecting both lungs and inwhich normal anatomical details are still visible- were identified and their medical recordsreviewed. Epidemiological data (including age,sex, ethnic group, current and past smokinghabits) and clinical history were available for allpatients. Apart from routine biological tests,blood and urine calcium concentrations werealso noted. Serum angiotensin convertingenzyme activity was assayed with hippurylhistidine leucine as a substrate.'3

PULMONARY FUNCTION TESTSThe forced expiratory volume in one second(FEV1) and vital capacity (VC) were measuredwith a spirometer (Godart water sealed spir-ometer) and residual volume (RV) by multiplebreath helium dilution. Carbon monoxidetransfer factor (TLCO) was measured by the

Service dePneumologie,H6pital Avicenne,Bobigny, FranceA TaziT Desfemmes-BaleyteD ValeyreJ-P BattestiINSERM U 82,Faculte de MedecineXavier Bichat,75018 Paris, FranceA TaziP SolerD ValeyreA J Hance

Reprint requests to:Dr A J Hance.Received 5 August 1993Returned to authors26 October 1993Revised version received6 April 1994Accepted for publication18 April 1994

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single breath method and scaled for age andheight or alveolar volume (VA) as specified. Theresults were compared with previously pub-lished standards.'3

BRONCHOALVEOLAR LAVAGEAll patients who underwent bronchoalveolarlavage as part of the diagnostic evaluation gaveinformed consent before the procedure. Lavagewas performed as previously described usingfive aliquots (50 ml each) of sterile saline.'2 Thetotal number of cells recovered/ml lavage fluidwas determined by counting cells present in an

aliquot of the resuspended original fluid. Dif-ferential cell count was obtained on May-Grun-wald-Giemsa stained cytocentrifuged prepara-tions of the lavage fluid by counting at least 500cells.

STATISTICAL METHODSResults are expressed as mean (SD). Compari-sons of sequential data were made using apaired t test, a probability of < 0 05 beingconsidered significant.

ResultsCHARACTERISTICS OF PATIENTS WITHPULMONARY SARCOIDOSIS AND A DIFFUSEGROUND GLASS RADIOGRAPHIC PATTERN AT THETIME OF DIAGNOSISClinical, biological and radiological findingsBetween January 1976 and December 19911652 patients with sarcoidosis were evaluated atour unit. Ten patients (06%) had a diffuseground glass pattern in the lung fields on a chestradiograph performed at the time of diagnosis.In these individuals the diagnosis of sarcoidosiswas based on the presence of a compatibleclinical picture, no evidence of disease due toother agents known to produce granulomatouslung diseases, and the presence of typical non-caseating granulomas on tissue biopsy samples(skin (n = 1), bronchial mucosa (n = 4), lymph

Typical chest radiograph from a patient with sarcoidosiswith a diffuse ground glass pattern. Note the existence ofbilateral hilar and mediastinal adenopathy.

nodes (n = 3)), or at the site of a Kveim-Siltzbach reaction (n = 2). All patients hadcoexistent bilateral hilar or mediastinal adeno-pathy, or both. A typical chest radiograph ofone of these patients is shown in the figure.Previous chest radiographs were available forfour patients and all were normal two, six, nine,and twelve months respectively before presen-tation. Two patients underwent thoracic highresolution computed tomographic scanning as

part of the diagnostic evaluation and the pres-ence of ground glass al2normalities was con-firmed in both cases.The epidemiological and clinical findings of

the 10 patients are summarised in table 1. Nineof the patients were symptomatic at the time ofdiagnosis. Nine had smoked cigarettes; the sixwho were current smokers smoked more than20 cigarettes/day (mean (SD) 25 (8)). Sixpatients had bilateral inspiratory crackles pre-dominantly at the lung bases. Seven patientshad extrathoracic lesions at one or more sites(peripheral lymph nodes (n = 4), ocular(n = 2), skin (n = 1), liver and spleen (n = 1),parotids (n = 1), peripheral nerves (n = 1), andbone (n = 1)). Although no patient had hyper-calcaemia, an increase in the daily urinary cal-cium excretion (> 0.1 mmol/kg/day) was notedin five of eight cases studied at the time of initialevaluation. Serum levels of angiotensin con-verting enzyme were elevated for all patients,ranging from two to five times the maximalnormal value.

Pulmonary functionResults of pulmonary function tests were avail-able for eight patients at the time of diagnosis.Seven patients had a restrictive defect, definedby a TLC of < 80% predicted (67 8 (12 5)%).The TLCO adjusted for age and height wasconsiderably impaired in all cases (48 4 (13)%of predicted) and five of eight patients had a

TLCO/VA of < 80% predicted (71 (17 7)%).Arterial hypoxaemia (Pao2 < 10 6 kPa) waspresent at rest in five of eight patients.

Bronchoalveolar lavageSince patients evaluated as early as 1976 wereincluded in this study, lavage results were avail-

Table 1 Epidemiological and clinical features of patientswith sarcoidosis who presented with diffuse ground glassabnormalities on the chest radiograph

Clinical characteristics No. of patients(n= 10)

Epidemio.ogical featuresMean (SD) age (years) 38-5 (11 5)M:F 8:2Smoking history

Current 6Former 3None 1

RaceWhite 10

Clinical signs and symptomsCough 7Exertional dyspnoea 8Weight loss 5Inspiratory rales 6Extrathoracic localisation 7

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Table 2 Results of bronchoalveolar lavage in six patients with sarcoidosis who presented with a diffuse ground glasspattern on the chest radiograph

Smoking Total cells/ml Percentage of cellshistory (x 10-3)

Macrophages Lymphocytes Neutrophils Eosinophils Mast cells

NS 145 48 51 1 0 0FS 115 24 76 0 0 0S 395 45-5 53 0 0 1-5S 791 43 50 6 0 1S 645 78-5 18 2 1 0 5FS 150 52 48 0 0 0

NS = non-smoker; FS = former smoker; S = current smoker.

able for only six patients. The number of lym-phocytes/ml lavage fluid was increased in allpatients (table 2). The CD4/CD8 lymphocyteratio was evaluated in two smokers and was 4 2and 2-6 respectively. Increased numbers ofinflammatory cells were generally not presentalthough one patient, a current smoker, had amoderate increase in neutrophils in the lavagefluid. Three of the six patients evaluated had anincreased percentage of mast cells in the lavagefluid (>0-5%). 14

OUTCOMENine patients were followed for more than threeyears (mean (SD) 99 (38) months, range 36-146months). Because all these patients initially hadsignificant respiratory symptoms (dyspnoeaand/or cough) or severely impaired lung func-tion, or both, all received treatment with oralcorticosteroids (05 mg/kg/day prednisone).They all improved with treatment and inspirat-ory crackles disappeared in all cases withinthree months. Similarly, parenchymal abnor-malities on the chest radiographs disappearedwithin three months of the institution of cor-ticosteroids in seven of the nine patients andwere considerably improved in the remainingtwo. Lung function tests also improved withtreatment (table 3). For all patients studied(n = 7) TLC returned to within the predictedrange during treatment. In parallel, TLCOadjusted for age and height increased by > 10%in five of seven cases, although TLCO/VA wasnot significantly modified (table 3). Pao, at restreached normal values (> 10 6 kPa) in three ofthe five patients who were initially hypoxaemicand improved in two other cases.Although all patients showed initial improve-

ment six of the nine patients experienced recur-

Table 3 Sequential evaluation of mean (SD) results ofrespiratory function testing for seven patients withsarcoidosis who presented with a diffuse ground glasspattern at the time of diagnosis and after treatment withcorticosteroids

Physiological test Before treatment After treatment

TLC (% predicted) 66-8 (13-2) 89 (7-2)*FEV1/VC 78-0 (12 3) 77-4 (9-3)TLCO (% predicted) 49-1 (13-8) 66-8 (13-6)*TLCO/VA 72-5 (19-0) 73-5 (9-7)Pao2(kPa) 10-3(1-7) 11-5(1-2)** p <0-05 comparing results before and after treatment using apaired t test. The best lung function while the patient wasreceiving corticosteroids was chosen.

rent signs and symptoms of active sarcoidosiswhile their doses of prednisone were beingtapered or after interruption of treatment.Strikingly, during these recurrent episodes ofsarcoidosis the chest radiographs alwaysshowed a diffuse ground glass pattern. Fourpatients had multiple episodes of reculrent sar-coidosis. Overall the duration of treatmnent was96 (41) months (range 30-143 months), and bythe end of December 1992 only three patientshad been successfully withdrawn from treat-ment with corticosteroids after 30, 48, and 128months, respectively.

DiscussionA review of more than 1600 chest radiographsof patients with sarcoidosis evaluated at ourunit has shown that the presence of a diffuseground glass pattern on the chest radiograph isan uncommon finding at presentation, but isassociated with a distinct clinical profile. Thesepatients were all white and tended to be heavysmokers, they had sarcoidosis of recent onset,and were almost always symptomatic. The dis-ease was responsive to treatment with cortico-steroids but frequently relapsed when cortico-steroids were tapered or stopped, and severalrequired long term treatment.

Several epidemiological features are note-worthy in this form of sarcoidosis. Firstly, nineof the 10 patients had smoked, and six werecurrent heavy smokers. In two studies from ourgroup the overall prevalence of cigarette smok-ing among patients with pulmonary sarcoidosiswas 31%12 and 39% 13 and, among smokers,mean tobacco consumption was 10 cigarettes aday.13 In contrast, current smokers in the pre-sent study smoked more than 20 cigarettes aday. The high proportion of current and pastsmokers in this series may explain the observedmale predominance.The origin of ground glass abnormalities in

our patients and the reason for the associationof these abnormalities with cigarette smoking isunclear. Smoking is known to increase alveolarepithelial permeability which might promotealveolar filling. Because some of our patientswere non-smokers and others had stoppedsmoking alterations in pulmonary epithelialpermeability induced by smoking, which arerapidly reversible,'5 are not the sole factor re-sponsible for the ground glass abnormalities.Smoking is also known to modify the lungimmune responses and such changes mightpredispose to the development of ground glass

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abnormalities. Smoking is not thought tomodify the prognosis of sarcoidosis in un-selected patients,'3 however, suggesting thatsmoking in itself cannot explain the unfavour-able outcome of these patients.

It is also noteworthy that all patients, withoutexception, were white. Sarcoidosis is known tooccur more frequently among the black popula-tion and, in France, among immigrants fromthe Caribbean.'16 In our own series, however,the proportion of white patients with sarcoid-osis is approximately 85%. Thus, given thesmall number of patients identified with groundglass abnormalities, a very large case-controlstudy would be necessary to show that thisabnormality is truly more common in the whitepopulation.The presence of hilar or mediastinal adeno-

pathy on the radiograph of all 10 patients, andthe observation that chest radiographs taken inthe year before diagnosis (when available) werenormal, strongly suggest that pulmonary sar-coidosis presenting with a diffuse ground glassradiographic pattern is likely to represent dis-ease of recent onset.

Also striking are the clinical and functionalprofiles of these patients. Nine presented withsevere respiratory symptoms (dyspnoea andcough) and series in which large numbers ofunselected patients have been evaluated indic-ate that respiratory symptoms at presentationare less frequent, particularly in whitepatients. 216 Furthermore, six patients hadfine inspiratory crackles mainly in the lowerzones. It should be stressed that the presence ofinspiratory crackles in our patients was not dueto pulmonary fibrosis as they cleared with treat-ment. In unselected patients crackles areunusual, especially in patients with disease ofrecent onset who are unlikely to have extensivefibrotic changes. In a study which compares theprevalence of respiratory crackles in variousinterstitial lung disorders inspiratory crackleswere found in only 20% of patients withsarcoidosis.'8 In our series the prevalence ofcrackles in sarcoidosis of recent onset is lessthan 10%, and is essentially restricted to non-white patients in whom sarcoidosis is known tobe more severe.'9 Because crackles themselvessuggest the presence of extensive pulmonarydisease, it is difficult to determine whether thepresence of ground glass abnormalities addsadditional prognostic information or merelyindicates the presence of "severe" parenchymalinvolvement.Although a moderate restrictive pattern asso-

ciated with an abnormal diffusing capacity isfrequently noted in sarcoidosis,202' an import-ant decrease in TLC and TLCO, as observed inour patients, is unusual.2223 Furthermore, stud-ies on gas exchange have shown that hypox-aemia at rest, which was present in five of ourcases, is unusual.2123 Because of these func-tional abnormalities and the associated clinicalsymptoms, all patients needed treatment withoral corticosteroids. Although they respondedrapidly, long term oral corticosteroid therapywas required to maintain this improvement.This chronic evolution is also uncommon insarcoidosis of recent onset in white patients.'9

The activity of the disease at presentation inour patients was supported by the presence ofhigh serum levels of angiotensin convertingenzyme in all cases. Although cigarette smokinghas been shown to increase serum angiotensinconverting enzyme levels in patients with sar-coidosis,'3 the presence of respiratory symp-toms, extrathoracic disease, and hypercalciuriain most of the patients suggests that the elevatedlevels of serum angiotensin converting enzymereflect both the clinical activity of their diseaseand the presence of widespread granulomatouslesions.342425 The increased recovery of lym-phocytes and mast cells by bronchoalveolarlavage also supports the presence of active dis-ease. '4 Although the presence of an elevatednumber of lymphocytes has been reported to bea good prognostic indicator or to be associatedwith a good response to treatment, or both,2627the presence of mast cells is thought to beassociated with a poor prognosis. '4

Extensive use of thoracic high resolutioncomputed tomographic scanning has led to themore frequent identification of "ground glass"opacities. Focal ground glass abnormalitieshave been observed in a broad spectrum of lungdisorders including sarcoidosis of recentonset.'01'2829 In sarcoidosis these localisedabnormalities often occur preferentially aroundbronchovascular bundles and are associatedwith other lesions.'028 A predominant and dif-fuse ground glass pattern has also been identi-fied on lung high resolution computedtomography in other conditions,2830 and dis-seminated, although not diffuse, ground glassabnormalities have been described in sarcoid-osis by this technique.'01' A ground glass pat-tern on lung high resolution computed tomo-graphy is thought to reflect either minimalthickening of alveolar septa or partial fillingof the alveolar air space with fluid or cells."Although the significance of ground glassopacities is incompletely understood, it hasbeen shown to correlate with disease activity inidiopathic pulmonary fibrosis and to be revers-ible under corticosteroid treatment.3' 32 In arecent study evaluating the correlation betweencomputed tomographic findings and lung histo-logy in bronchiolitis obliterans organisingpneumonia biopsy specimens obtained fromareas of ground glass opacities contained"alveolar septal inflammation and alveolar des-quamation".33 Very recently biopsy specimensof localised areas of ground glass pattern havebeen studied in one patient with sarcoidosis andwere found to contain mainly granulomas.34

In summary, a diffuse ground glass radio-graphic pattern at the time of diagnosis ofsarcoidosis was observed exclusively in whitepatients, many of whom were cigarettesmokers. The disease proved to be of recentonset and quite active. Although rare, this modeof presentation of the disease is noteworthybecause, in our experience, it tends to have achronic evolution requiring prolonged treat-ment with oral corticosteroids.

1 Scadding JG, Mitchell DN. Prevalence, incidence and modesof presentation. In: Scadding JG, Mitchell DN, eds.Sarcoidosis. 2nd edn. London: Chapman and Hall Medical,1985:43-71.

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