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Rounded atelectasis in workers exposed to asbestosBrazilian Journal of Medical and Biological Research (2003) 36: 1341-1347ISSN 0100-879X

Identification of rounded atelectasisin workers exposed to asbestos bycontrast helical computed tomography

1Grupo Interinstitucional de Estudos de Doenças Relacionadas ao Amianto doEstado de São Paulo, Brasil2Disciplina de Pneumologia, Instituto do Coração, Hospital das Clínicas,Faculdade de Medicina, Universidade de São Paulo, São Paulo, SP, BrasilDisciplinas de 3Radiologia and 4Patologia, Faculdade de Medicina,Universidade de São Paulo, São Paulo, SP, Brasil5Área de Medicina Ocupacional, Faculdade de Medicina,Universidade Estadual de Campinas, Campinas, SP, BrasilDisciplinas de 6Pneumologia and 7Radiologia, Escola Paulista de Medicina,Universidade Federal de São Paulo, São Paulo, SP, Brasil

M. Terra-Filho1,2,J. Kavakama1,3,

E. Bagatin1,5,V.L. Capelozzi1,4,

L.E. Nery1,6 andR. Tavares1,7

Abstract

Rounded atelectasis (RA) is a benign and unusual form of subpleurallung collapse that has been described mostly in asbestos-exposedworkers. This form of atelectasis manifests as a lung nodule and can beconfused with bronchogenic carcinoma upon conventional radiologicexamination. The objective of the present study was to evaluate thevariation in contrast uptake in computed tomography for the identifi-cation of asbestos-related RA in Brazil. Between January 1998 andDecember 2000, high-resolution computed tomography (HRCT) wasperformed in 1658 asbestos-exposed workers. The diagnosis wasmade in nine patients based on a history of prior asbestos exposure, thepresence of characteristic (HRCT) findings and lesions unchanged insize over 2 years or more. In three of them the diagnosis was confirmedduring surgery. The dynamic contrast enhancement study was modi-fied to evaluate nodules and pulmonary masses. All nine patients withRA received iodide contrast according to weight. The average en-hancement after iodide contrast was infused, reported as Hounsfieldunits (HU), increased from 62.5 ± 9.7 to 125.4 ± 20.7 (P < 0.05), witha mean enhancement of 62.5 ± 19.7 (range 40 to 89) and with auniform dense opacification. In conclusion, in this study all patientswith RA showed contrast enhancement with uniform dense opacifica-tion. The main clinical implication of this finding is that this proceduredoes not permit differentiation between RA and malignant pulmonaryneoplasm.

CorrespondenceM. Terra-Filho

Rua Pintassilgo, 519/80

04514-032 São Paulo, SP

Brasil

Fax: +55-11-3082-7040

E-mail: pnemario@incor.usp.br

Research partially supported

by FAPESP (No. 96-10415-6).

Received October 2, 2002

Accepted May 7, 2003

Key words• Rounded atelectasis• Asbestos• Helical computed

tomography• Asbestos-exposed workers

Introduction

Rounded atelectasis (RA) is character-ized by a reduction in volume of peripherallung tissue, also known as atelectatic pseudo-

tumor or folded lung, and it is a chronic formof atelectasis which manifests as a lung nod-ule and which can be confused with bron-chogenic carcinoma upon conventional ra-diologic examination (1). RA is considered

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to be one of the manifestations of asbestos-related diseases; however, any type of pleu-ral inflammatory reaction can cause this lungalteration (2,3). RA was described for thefirst time at the beginning of the last century(4), and since has been detected with in-creasing frequency mainly as a result of theuse of computed tomography (CT) in work-ers exposed to asbestos.

RA is found adjacent to areas of pleuralfibrosis and consists of collapsed pulmonaryparenchyma surrounded by thickened andinvaginated pleura (5,6). Several theorieshave been proposed to explain its pathogen-esis, with the following two being the cur-rently most accepted ones: i) RA resultsfrom the compression of pulmonary paren-chyma due to pleural hemorrhage involvingand distorting the adjacent lung, and ii) RAformed by fibrotic pleura compresses thepulmonary parenchyma, leading to its col-lapse (2,6).

The lung alterations present in RA areradiologically characterized as opacities,nodules or masses close to the pleura, whichoften cannot be differentiated from malig-nant neoplasias (1) even upon chest tomog-raphy. Therefore, new diagnostic methodsare being studied in an attempt to restrict theuse of invasive procedures for the identifica-tion of these lung alterations. Recently,Swensen et al. (7) proposed that malignantlung nodules can be identified tomographi-cally as long as their density increases sig-nificantly after contrast injection by a stan-dard technique. This method is easy to carryout; however, numerous false-positive caseshave been reported (8).

Asbestos is a known cancerogenic agent,and lung nodules and masses are a commonfinding in workers and ex-workers exposedto asbestos fibers. Diseases such as RA andmalignant neoplasias are more prevalent inindividuals occupationally exposed to as-bestos, and frequently show poorly charac-terized radiologic alterations, thus requiringthe use of complementary methods for the

determination of their nature.The objective of the present study was to

determine the variation in contrast uptake byCT in individuals with a diagnosis of RAwho had been occupationally exposed toasbestos.

Patients and Methods

A total of 6696 workers and ex-workersexposed to asbestos during their employ-ment in the mining (4650) and fibrocement(2046) industry were assessed by the Interin-stitutional Asbestos Study Group consistingof professors from the Faculty of Medicine,University of São Paulo, from Escola Paulis-ta de Medicina, Federal University of SãoPaulo, and from the Occupational Health Area,State University of Campinas (UNICAMP),during the period from January 1998 to De-cember 2000.

A total of 1658 high-resolution computedtomography (HRCT) scans were obtained fromthese individuals. The project was approvedby the Ethics Committee of UNICAMP, andall patients signed an informed consent formto participate in the study. A clinical andoccupational history was obtained from allpatients, who were submitted to physicalexamination, chest X-ray and spirometry.

The indications for HRCT were based onthe following criteria: i) clinical criteria, i.e.,respiratory complaints, abnormalities uponphysical examination and/or alterations de-tected by chest X-ray; ii) all workers whohad been engaged in their professional ac-tivities for more than 10 years before 1980;iii) workers and ex-workers of the miningindustry who showed an exposure load equalto or higher than 10 fibers/year, irrespectiveof the duration of exposure.

All individuals who presented tomo-graphic alterations compatible with RA andfrom whom no pleuropulmonary biopsy wasobtained were followed up annually for aperiod of 2 years.

Criteria for the inclusion in the present

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study were: a history of asbestos exposure,no evidence of past tuberculosis, histoplas-mosis or pleural handling, and individualsfor whom HRCT revealed signs compatiblewith RA, which remained stable for a periodof 2 years or longer, or individuals who werefollowed up for a shorter period of time butin whom alterations compatible with RAwere identified upon lung biopsy and ana-tomopathologic examination.

High-resolution computed tomography

The exams were carried out with thepatient in ventral decubitus according to thestandard norms of Webb et al. (9), and equip-ment providing 1.5-mm thick sections andreconstructing the image in a 512 x 512matrix were obtained using a high-resolu-tion spatial filter and an exposure time of1.2 s. Scans were documented with a laserprinter on 14 x 17 inch films formatted intosix images, and a window for soft parts withformatting into 15 images. A window withan opening of 1200 Hounsfield units(HU) and a level of 800 was used for assess-ment of the lung, and a window of 600/800HU with a level of 20/40 for assessment ofsoft parts.

The HRCT scans were analyzed usingthe semiquantitative classification of Gamsuet al. (10), which consists of the evaluationof the extent and type of interstitial pulmo-nary impairment: a) extent of interstitial pul-monary involvement (four degrees): 0 = nor-mal, 1 = few interstitial alterations at fourfoci at most, unilateral and present in at leastthree sections, 2 = multifocal alterations oflimited extent but affecting both hemithora-ces, or alterations in at least two planes of thesame hemithorax, and 3 = diffuse bilateralimpairment; b) type of interstitial pulmonaryimpairment: interlobular and centrolobularseptal thickening, parenchymatous bands,subpleural lines, subpleural nodules, distor-tion of the architecture of the pulmonaryparenchyma, honeycombing, and traction

bronchiectasis.The diagnosis of asbestosis was made in

patients with compatible exposure based onthe following tomographic alterations: i)presence of at least two abnormalities thathistologically characterize fibrosis, such ashoneycombing and traction bronchiectasisin at least two sections, or ii) multifocalabnormalities such as bands, subpleural lines,lobular disorganization or irregular septaand subpleural reticulate located in bothhemithoraces and present in more thanthree sections. Pleural involvement was de-termined by the presence or absence of pleu-ral plaques.

The following tomographic findings sug-gested a diagnosis of RA: i) round or ovalopacity, ii) peripheral localization adjacentto the pleural surface, and iii) associationwith pulmonary or bronchial vessels bend-ing in the direction of the lesion and associa-tion with homolateral pleural abnormalities,hemorrhage or pleural thickening.

All tomographs were analyzed by twoexperienced radiologists and one pneumolo-gist, who were not aware of the clinicalconditions of the patients.

Modified Swensen protocol (11)

All nine patients with RA received io-dide contrast according to weight, with 70 kgcorresponding to the use of 100 ml contrastdye. None of the patients had a history ofallergy to the iodide material or of renalfailure. The density of atelectasis measuredin HU was determined before intravenousadministration of the nonionic iodide con-trast, and 1, 2, 3 and 4 min after the begin-ning of infusion with an injector pump at arate of 2 ml/s.

Statistical analysis

Descriptive statistics was used for datapresentation (mean and standard deviation).Numerical variables were compared by the

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Student t-test, with the level of significanceset at 5%.

Results

All nine individuals who fulfilled theinclusion criteria were males. Three of themwere submitted to pleuropulmonary biopsy,with the anatomopathologic findings beingcompatible with RA. The age of the patientsranged from 54 to 60 years. The mean pre-contrast density was 62.5 ± 9.7 HU and themean post-contrast value was 125.4 ± 20.7HU, with the difference being statisticallysignificant (P < 0.05). All patients showedan increase in density after contrast injectionhigher than 15 HU (Table 1), with a meanincrease of 62.5 ± 19.7 HU. With respect tolocalization, RA was located in the rightsuperior lobe in one patient, in the middlelobe in one, in the lingula in one, in the rightinferior lobe in three, and in the left inferiorlobe in three. Six patients showed pleuralplaques and two presented asbestosis. Thesize of the atelectasis ranged from 2.0 to 4.8cm.

Discussion

In Brazil, asbestos mining started at theSão Félix Mine, municipality of Poções,Bahia, which remained commercially pro-ductive until 1967, when the Cana BravaMine, located in the municipality of Minaçu,Goiânia, was discovered. It is estimated thatmore than 10,000 workers were exposedduring the period from 1940 to 1996. In1996, the Interinstitutional Asbestos StudyGroup consisting of professors from the Uni-versity of São Paulo, University of Campi-nas and Federal University of São Paulo wasfounded. A total of 4650 individuals who areor were engaged in professional activities atthe São Félix Mine, Canabrava Mine, orboth, were assessed during a period of 4years. These individuals participated in thepresent study, in addition to 2046 ex-work-ers from fibrocement processing factories.

RA is a radiologically well-defined ab-normality, which was initially described byLoeschke (4) in 1928. In the English medicalliterature RA was characterized in detail byBlesovsky (5) who called it folded lung.Later, other investigators have clinically andradiologically described this abnormality, anddifferent terms were created such as pleuralfibroma, pleurosoma or Blesovsky's syn-drome (6).

A chest X-ray generally reveals a roundor oval opacity adjacent to an area of pleuralthickening. The borders can be sharp orpoorly defined. A highly characteristic signconsists of curvilinear lines directed at thelesion (comet tail sign) which representbronchovascular branches (6).

From a tomographic viewpoint (Figure1), the findings are closely similar to thoseobtained by conventional radiology, i.e.,round or oval opacity, peripheral location,association with pulmonary vessels bendingtowards the lesion (comet tail sign), andassociation with homolateral pleural abnor-malities, hemorrhage or pleural thickening(12).

Table 1. Patient age and density, location and size of the rounded atelectasis, andpresence of pleural plaques and asbestosis.

Patient Age ∆ (HU) Location Pleural Asbestosis(years) (size in cm) plaques

1 58 52-141 (89) RIL (3.2) Yes No

2 54 74-114 (40) RIL (4.8) Yes No

3 56 50-93 (43) ML (4.5) Yes No

4 60 58-124 (66) RSL (4.0) Yes Yes

5 55 67-113 (46) Lingula (2.5) No Yes

6 56 63-136 (73) LIL (2.5) Yes No

7 55 56-129 (73) RIL (2.0) Yes No

8 54 54-108 (54) LIL (2.5) Yes No

9 55 79-161 (82) LIL (2.0) No No

HU = density (in Hounsfield units) before and after contrast injection; ∆ = difference(in HU) before and after iodide contrast injection; LIL = left inferior lobe; ML = middlelobe; RIL = right inferior lobe; RSL = right superior lobe.

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The main etiologic cause of RA is asbes-tos exposure. In many patients, RA is char-acterized by radiologic opacities that corre-spond to areas of lung collapse and pleuro-pulmonary fibrosis, which cannot be inter-preted as asbestosis and which do not pres-ent a clear relationship with pulmonary dys-functions (12).

Hillerdall (13), studying 74 patients withRA, observed that this abnormality was un-related to asbestos exposure in only 10 pa-tients. RA was secondary to chest trauma intwo cases and to nonspecific pleural exu-dates in four, while in the other cases nocause could be established. RA has alsobeen described in association with histoplas-mosis (2) and tuberculosis, and in patientssubmitted to therapeutic pneumothorax (3).In the present study, all patients had a well-documented history of occupational asbes-tos exposure, since they worked without ex-ception in the asbestos extraction or process-ing industry, and data proving this exposurewere provided by the employers.

Patients with RA are practically asymp-tomatic. Evidence obtained from individualswho are periodically submitted to clinicaland radiologic assessment, but not to inva-sive procedures for an eventual diagnosis,shows that the abnormality generally doesnot progress and, on some occasions, theopacification may resolve spontaneously(14). Autopsy or the result of patients sub-mitted to thoracotomy demonstrates that theradiologic abnormalities correspond to col-lapsed pulmonary areas and areas of visceralpleural fibrosis (15).

In patients exposed to asbestos, RA mightrepresent a sequela of a preexisting pleuralexudate, or might be the result of adjacentpleural fibrosis or diffuse pleural thickening(16). According to the latter investigators, insome workers exposed to these fibers, RAmight reflect the evolution of parenchyma-tous bands.

In the present study in which all individu-als were assessed by CT this abnormality

Figure 1. Rounded atelectasis: oval opacity, peripheral localization adjacent to the pleuralsurface, curvilinear lines directed at the lesion.

was observed in the inferior lobes in sixpatients (6/9), in the lingular segment in one(1/9), in the middle lobe in one (1/9), and inthe superior lobe in one (1/9). This predomi-nant location in the inferior lobes has alsobeen reported by others (17). In contrast, thepreferred locations observed by Hillerdall(13) for 74 patients with RA were the middlelobe and lingular segment (62%). It shouldbe noted, however, that this investigator useda chest X-ray for evaluation.

RA ranging from 2 to 7 cm in diameterhave been described (17). In the presentstudy, the size of RA ranged from 2 to 4.8cm, values that are within the limits reportedby others.

A higher frequency of RA in patientswith asbestosis has been reported by severalinvestigators (18). In the present study, onlytwo of the nine patients had asbestosis, whilemost of them, seven patients, presented pleu-ral plaques. Only one showed a radiologi-cally normal pleura and pulmonary paren-chyma, indicating that there was an associa-tion between pleuropulmonary alterationsand RA in workers and ex-workers exposed

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alterations in density after contrast injectionrevealed a minimum increase of 200% in thevalues observed. In contrast, in the presentstudy using a different technique a smallerincrease in post-contrast density was ob-served, ranging from 40 to 271%, with theincrease being homogenous in all cases.

Bronchogenic carcinoma usually concen-trates contrast dye in both a homogenous andheterogenous manner (19). Therefore, thedetermination alone of how the contrast dyeis concentrated within the lesion is insuffi-cient for a perfect differentiation betweenRA and lung cancer (19).

More recently, Swensen et al. (7) pro-posed that malignant lung nodules can beidentified by chest CT as long as their den-sity increases more than 15 HU after intrave-nous contrast injection by a standard tech-nique. Patients who show increases below15 HU can be considered to have benignnodules. All patients assessed in the presentstudy (Figures 2 and 3) showed an increasein post-contrast density ≥40 HU (mean =62.5 ± 19.7), with this increase thus beinghigher than the 15 HU proposed by Swensenet al. (7). Moreover, none of the patientswith RA studied here showed an increasebelow 15 HU, that could therefore be con-sidered a benign process of the lung. How-ever, it is important to note that the indica-tions for the contrast assessment reported bySwensen et al. (7) were restricted to thestudy of lung nodules, in contrast to thepresent study in which lung masses and nod-ules were analyzed. In addition, significantincreases in post-contrast density in non-neoplastic pulmonary processes such asgranulomas and hamartomas have also beenreported by others (8,21).

A possible criticism to the present studyis that only three patients were submitted toa pleuropulmonary biopsy; thus, a definitivediagnosis was only obtained for these pa-tients. However, we should consider thatthese procedures were carried out exactly onthe first cases in 1998. After this period,

Figure 2. Rounded atelectasis: pre-contrast density = 54.14 HU.

Figure 3. Rounded atelectasis: post-contrast density = 108.05 HU.

to asbestos. RA represents an area of lungcollapse and might therefore show a signifi-cant increase in radiologic density after in-travenous injection of contrast dye due to thevascularization of pulmonary tissue, despitethe existence of adjacent fibrotic pleuralareas (19). A CT study (20) demonstrating

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several investigators have established withexcellent precision the tomographic criteriacompatible with RA (12,22), in such a waythat invasive procedures for the diagnosis ofRA can be eliminated (12) if the alterationscharacteristic of RA observed upon tomog-raphy remain unchanged for a period longerthan one year. Six patients in the presentstudy who were not submitted to biopsywere followed up for a minimum period of 2years, and only those presenting unchanged

radiologic alterations were included in thestudy.

The results of the present study lead us toconclude that individuals occupationally ex-posed to asbestos show an increase in den-sity in the pulmonary region affected by RAafter contrast injection by a standard tech-nique. The main clinical implication of thisfinding is that this procedure does not permitthe differentiation between malignant pul-monary neoplasias and RA.

References

1. Payne CR, Jacques PF & Kerr IH (1980). Lung folding simulatingperipheral pulmonary neoplasm (Blesovsky’s syndrome). Thorax,35: 936-940.

2. Pasik AS, Mendelson DS & Maron Z (1990). Rounded atelectasiscaused by histoplasmosis. American Journal of Radiology, 155:275-276.

3. Batra P, Brown K, Hayashi K & Mori M (1996). Rounded atelectasis.Journal of Thoracic Imaging, 11: 187-197.

4. Loeschke H (1928). Störungen des Luftgehalts der Lunge. In:Handbuch der Speziellen Pathologischen Anatomie und Histologie.1st edn. Springer, Berlin, Germany.

5. Blesovsky A (1966). The folded lung. British Journal of Diseases ofthe Chest, 60: 19-22.

6. Menzies R & Frazer R (1987). Round atelectasis. American Journalof Surgical Pathology, 11: 674-681.

7. Swensen SJ, Viggiano RW, Midthun DE et al. (2000). Lung noduleenhancement at CT: multicenter study. Radiology, 214: 73-80.

8. Fraser RS, Müller NL, Colman N & Paré PD (1999). Pulmonarycarcinoma. In: Fraser RS & Paré PD (Editors), Diagnosis of theDiseases of the Chest. 4th edn. W.B. Saunders Company, Philadel-phia.

9. Webb WR, Müller NL & Naidich DP (Editors) (2001). Technicalaspects of high resolution computed tomography. In: High Resolu-tion CT of the Lung. 3rd edn. Lippincott Williams and Wilkins,Philadelphia.

10. Gamsu G, Salmon CJ, Warnock ML & Blanc PD (1995). CT quantifi-cation of interstitial fibrosis in patients with asbestosis: a compari-son of two methods. American Journal of Radiology, 164: 63-68.

11. Terra-Filho M, Kavakama J, Nery LE, Rodrigues RT, Capellozi VL &Bagatin E (2002). Asbestos related rounded atelectasis in Brazil: adynamic contrast enhancement study. American Journal of Respi-ratory and Critical Care Medicine, 8: A530 (Abstract).

12. Webb WR, Müller NL & Naidich DP (Editors) (2001). Diseases

characterized by linear and reticular opacities. In: High ResolutionCT of the Lung. 3rd edn. Lippincott Williams and Wilkins, Philadel-phia.

13. Hillerdall G (1989). Rounded atelectasis. Clinical experience with 74patients. Chest, 95: 836-841.

14. Smith LS & Schillaci RF (1984). Rounded atelectasis due to acuteexudative effusion - spontaneous resolution. Chest, 85: 830-832.

15. Dervenik L, Gatzinsky P, Hultman E, Selin K, William-Olson G &Zettergren L (1982). Shrinking pleuritis with atelectasis. Thorax, 37:252-258.

16. Genevois PA, de Maertelaer V & Madami A (1998). Asbestosis,pleural plaques, and diffuse pleura thickening: three distinct benignresponses to asbestos exposure. European Respiratory Journal, 11:1021-1027.

17. Lynch DA, Gamsu G, Ray CS & Aberle DR (1988). Asbestos-relatedfocal lung masses: Manifestations on conventional and HRCT scans.Radiology, 163: 603-611.

18. Verschakelen JÁ, Demaerel P, Demets M, Marchal G & Baert AL(1989). Rounded atelectasis of the lung: MR appearance. AmericanJournal of Radiology, 152: 965-966.

19. Taylor PM (1988). Dynamic contrast enhancement of asbestos-related pulmonary pseudotumors. British Journal of Radiology, 61:1070-1072.

20. Westcott JL, Hallisey MJ & Volpe JP (1991). Dynamic CT of roundatelectasis. Radiology, 181: (P)182 (Abstract).

21. Yamashita K, Matsunobe S & Tsuda T (1997). Intratumoral necrosisof lung carcinoma: A potential pitfall in incremental dynamic com-puted tomography analysis of solitary nodules? Journal of ThoracicImaging, 12: 181-187.

22. Fraser RS, Müller NL, Colman N & Paré PD (1999). Round atelecta-sis. In: Fraser RS & Paré PD (Editors), Diagnosis of the Diseases ofthe Chest. 4th edn. W.B. Saunders Company, Philadelphia.