Pseudoasbestos Bodies and Fibers in Bronchoalveolar Lavage of ...

Pseudoasbestos Bodies and Fibers in BronchoalveolarLavage of Refractory Ceramic Fiber UsersPASCAL DUMORTIER, INGRID BROUCKE, and PAUL DE VUYSTChest Department, Hôpital Erasme, Université Libre de Bruxelles, Brussels, BelgiumRefractory ceramic fibers (RCF) are widely used to replace asbestosin applications requiring high heat resistance. Ferruginousbodies mimicking asbestos bodies (ABs) have been detected in thelungs of RCF production workers. This raises the question abouttheir presence in other occupational groups and whether “typicalABs” still reflect past asbestos exposures in all settings. An ABcounting by phase-contrast light microscopy and a screening testby analytical electron microscopy were systematically performedon all bronchoalveolar lavage fluids (BALF) submitted to our laboratoryin 1992 through 1997 (n 1,800). When RCF were detectedin electron microscopy, the structures considered as “typicalABs” were marked under light microscopy and prepared forfurther chemical and structural analysis. Pseudo-ABs on RCF weredetected in samples from nine subjects (0.5%). All of them hadworked either as foundry workers, steel workers, or welders. Inthese subjects, alumino-silicate fibers compatible with RCF accountedfor 42% of the core fibers analyzed, other nonasbestos fibersfor 28%, and asbestos fibers for 30%. ABs thus remain a validmarker of asbestos retention but attention must be paid to a possibleoccurrence of pseudo-asbestos bodies on RCF and other nonasbestosfibers in end-users of refractory fibers.Keywords: asbestos; refractory ceramic fibers; biopersistence; bronchoalveolarlavage fluid; transmission electron microscopyInhaled particles and fibers deposited in the lungs are usuallyphagocytized by alveolar macrophages. Ferruginous bodiesresult from the deposition of an iron-rich protein layer at thecell–particle interface of biopersistent fibers or particles that aretoo large to be completely phagocytized. Ferruginous bodiesmostly form on particles larger or fibers longer than 10 m (1,2). They may occur on a wide variety of materials, includingasbestos fibers, sheet silicates, diatomaceous earth, coal particles,metal compounds, and silicon carbide (3–5). The mechanismsleading to ferruginous bodies formation are not fullyunderstood. Experimental evidence suggests that they couldbe formed by an exocytotic activity of macrophages or giantcells (6). In rodents, coated fibers can be detected in light microscopypreparations 2 to 3 mo after exposure (2).Coated asbestos fibers are referred to as asbestos bodies(ABs). In light microscopy the central core of a “typical” ABis a thin, straight, transparent, and colorless fiber. The fiber iscovered by a regularly segmented or continuous golden yellowto red brown coating. Some branched or curved forms can beobserved (1, 3, 7). The validity of this definition is supported(Received in original form December 5, 2000 and in revised form April 10, 2001)This work was partly supported by Grant 3.4525.97 from the Fonds de la RechercheScientifique Médicale. I. Broucke was supported by a grant from the FondationErasme.Correspondence and requests for reprints should be addressed to P. Dumortier,Chest Department, CUB Hôpital Erasme, Route de Lennik 808, B1070 Brussels,Belgium. E-mail: pdumorti@ulb.ac.beThis article has an online data supplement, which is accessible from this issue’stable of contents online at www.atsjournals.orgAm J Respir Crit Care Med Vol 164. pp 499–503, 2001Internet address: www.atsjournals.orgby numerous electron microscopy analyses which have demonstratedthat 95 to 98% of the core fibers of structures correspondingto this definition are indeed asbestos fibers (1, 8).Most ABs are built on amphibole asbestos fibers and the ABburden correlates with the amphibole content of the lung (9).ABs on chrysotile have been observed in subjects recently exposedto this type of fiber despite its shorter biopersistence(7). Concentrations above 1 AB/ml in bronchoalveolar lavagefluid (BALF) or above 1,000 AB/g dry lung tissue indicatenontrivial asbestos exposure, and the concentrations of ABs inBALF and lung tissue are correlated (10).Typical ABs can usually be distinguished from other ferruginousbodies. The latter have brown to black cores or broadtransparent to yellow cores, usually with an irregular coating(3). The terms “ferruginous body” and “pseudo-asbestos body”are equally used for these atypical structures. In this article,we will use the term “ferruginous body” for atypical structureseasy to distinguish from ABs in routine phase-contrast lightmicroscopy and restrict the term “pseudo-asbestos body”(pseudo-AB) to structures that look like typical ABs but arebuilt on nonasbestos core fibers.Pseudo-ABs form at least on erionite (11) and on refractoryceramic fibers (RCF) (12, 13). Because erionite exposureis limited to a few villages in Cappadocia (Turkey), pseudo-ABs on erionite do not really interfere with evaluation of occupationalasbestos exposures.Pseudo-ABs on RCF have been occasionally described inBALF (13) and lung tissue (12) of RCF production workers.RCF are man-made vitreous fibers produced from a meltedmixture of Al 2 O 3 and SiO 2 or from calcined kaolin clay. Otheroxides, such as ZrO 2 , B 2 O 3 , TiO 2 , and Cr 2 O 3 , can be added inorder to change the fiber properties. They are used to replaceasbestos in high-temperature insulation such as insulation offurnaces and kilns; high-temperature filtration; and refractoryblankets, papers, felts, and textiles. Production of RCF wasuncommon before the 1970s. RCF represent 1 to 2% of thecurrent total production of man-made vitreous fibers. BesidesRCF, refractory fibers made of crystalline aluminum oxide orcrystalline zirconium oxide are also produced (14).The increasing use of RCF raises the question whether “typicalABs” still reflect asbestos exposures in all settings. Thisstudy concerns the occurrence of RCF and other refractory fibersin routine electron microscopy analyses.METHODSEach year, approximately 300 BALF samples from clinical or medicolegalcases are referred to our laboratory for fiber or particle analysis.For each sample the referring chest physician is requested to fill ina questionnaire on clinical data, occupational and environmentalbackground, and the type of particles that must be searched for. Becausethe questionnaire is rarely fully completed, we have developeda routine analytical procedure to minimize the possibility to overlookunsuspected exposures. It includes an AB and uncovered fiberscounting by light microscopy and a quick evaluation of the particulateburden through a screening test by analytical transmission electronmicroscopy.

500 AMERICAN JOURNAL OF RESPIRATORY AND CRITICAL CARE MEDICINE VOL 164 2001Additional information about BALF sampling, preparation, andexamination by light and electron microscopy is available in the onlinedata supplement.If RCF were detected as pseudo-ABs core or uncoated fibers duringthe electron microscopy screening test, the light microscopy slideswere reexamined. Some typical ABs were randomly selected, examinedin natural light at a higher magnification (400 to 1,250),marked with a high-precision object marker (15), and photographed.These marked bodies were transferred to electron microscopy gridsand their core fiber was analyzed by energy-dispersive spectrometry andmeasured. This allowed us to determine the percentage of true andpseudo-ABs contained in a BALF and to compare their morphologicand optical characteristics.The concentration of ABs, pseudo-ABs, and fibers and their size(width, length, and aspect ratio) are presented as geometric mean(GM) (geometric standard deviation [GSD] 95% confidence interval;[CI]). Mann-Whitney U tests were used to compare fiber sizes.RESULTSPatientsBetween January 1, 1992 and December 31, 1997, BALF samplesfrom 1,800 patients were examined. AB counts were 1AB/ml BALF in 617 (34%) patients and 5 AB/ml BALF in310 (17%). The electron microscopy screening test revealedalumino-silicate fibers compatible with RCF as pseudo-ABscores or uncovered fibers in the BALF of nine of 1,800 patients.Demographic, occupational, and clinical data and theindication for the mineralogical analysis of BALF are reportedin Table 1. The nine patients had all been working infoundries, steelworks, or as welders. All patients were stillworking in possible contact with RCF when BALF was performed,except Patient 6 who had worked as a radiology technicianfor 9 yr. Exposure to RCF was never reported in the occupationalhistory given by the referring physician.BALF AB, Pseudo-AB, and Ferruginous Body ContentTable 2 summarizes the results of the mineralogical analyses.All 9 patients had more than 1 typical AB/ml in BALF andseven had more than 5 typical AB/ml. Altogether, 257 structures(237 typical ABs and 20 uncovered fibers) were markedand analyzed (Figures 1 and 2). Several types of nonasbestoscore fibers were identified. They were distributed into six categories(Si Al, Al Si, Si, Al, Fe, no signal) according tothe major peaks detected in the chemical spectra. Amorphousalumino-silicate fibers accounted for 42% of the body coresanalyzed, other nonasbestos fibers for 28%, and asbestos for30%. Nonasbestos core fibers accounted for 50% or more infive of the nine patients. Although electron diffraction indicatedthat the silicon-, aluminum-, and iron-rich fibers had acrystalline structure, interpretable electron diffraction patternscould not be obtained.No distinction could be made between the different core fibersduring routine phase-contrast light microscopy analysis. Someiron-rich core fibers could, however, be discriminated owing totheir reddish-brown color when examined under natural light athigher magnification (1,000) with oil immersion objectives.During the period covered by the study, two other patientspresented with pseudo-ABs on crystalline silica and on crystallineiron oxide core fibers, but no RCF. They had bothpseudo-AB concentration greater than 5/ml of BALF. Interestingly,these two patients were respectively working as agrinder and as a trimmer in two different foundries.Pseudo-AB Size ParametersCore fibers of pseudo-ABs were thicker, shorter, and hadlower aspect ratios than those of true ABs from our database(Table 3). When comparisons were performed according toasbestos fiber type, pseudo-ABs core fibers are thicker andlonger than crocidolite and chrysotile core fibers (p 0.005),shorter than amosite core fibers (p 0.005), but have diametersimilar to amosite (GM [GSD; 95% CI]:0.24 m [1.92; 0.22to 0.26]; p 0.23) and tremolite (0.31 m [2.09; 0.29 to 0.34];p 0.079) and length similar to tremolite (33.6 m [1.57; 31.9to 35.4]; p 0.136) core fibers. Among pseudo-ABs, 50% ofthe core fibers were longer than 30 m and thinner than 0.5 m.Most pseudo-ABs fibers (71%) were thinner than 0.4 m andfew (10%) were thicker than 1 m.Quantitative chemical analysis of fibers and other observationsmade on the BALF of these patients are reported anddiscussed in the online data supplement.DISCUSSIONWe report the presence of coated and uncoated RCF in BALF.It was not possible to make a distinction between pseudo-ABsTABLE 1. EXPOSURE AND CLINICAL DATA OF THE PATIENTS WITH RCF IN BALF SAMPLESCaseNo.Age(yr)ReportedOccupationDuration(yr) Clinical Data* Suspected Exposure1 37 Grinder in a foundry 9 N Asbestos, metalsBlowlamp operator loading 5and unloading of furnaces2 25 Grinder in steelworks 3 N Asbestos, ‡ metals3 42 Furnace cleaning in a foundry 20 Progressive massive fibrosis Asbestos, silica4 54 Furnace worker 14 N Asbestos5 37 Furnace mason 10 Pleural effusion Asbestos6 39 Furnace installation and 6 Pulmonary and pleural Asbestos, coal, silicadismantlingfibrosis of upper zonessecondary to radiationtherapy for Hodgkin’slymphoma7 50 Concrete preparator 1 Pleural plaques † Asbestos, coal, aluminum, rock woolFurnace worker in steelworks 3Foundry worker 1Boiler welder 288 40 Welder 25 Pleural effusion Asbestos9 52 Furnace worker in steelworks 27 Pleural plaques † Asbestos* N No detectable pulmonary or pleural abnormality.†Confirmed by CT scan.‡Possible environmental exposure to tremolite asbestos in Turkey until the age of 19.

Dumortier, Broucke, and De Vuyst: Pseudo-asbestos Bodies on RCF 501TABLE 2. CONCENTRATION OF FIBERS AND BODIES IN BALF SAMPLES OF PATIENTS IN WHOM RCFs WERE DETECTEDCaseNo.TypicalAB/mlLight MicroscopyUF/mlElectron MicroscopyNumberof Typical % with% of Each Type of Nonasbestos Core Fiber §AtypicalFB/mlABsAnalyzedNonasbestosCore Fiber Si Al Al Si Si Al Fe No signal1 † 29 11 20 105 97.1 23.8 19 29.5 4.8 202 22 1.9 3 33 84.8 33.3 30.3 3 18.23 41 5.3 3.6 19 84.2 47.4 10.5 15.8 5.3 5.34 8.2 16 ND 12 83.3 66.7 16.75 1.2 116 ND 20* 50* 20* 30*6 8.7 11 ND 15 26.7 6.7 207 ‡ 28 20 0.3 21 28.6 14.3 4.8 9.58 6.8 1.6 ND 16 12.5 12.59 2.5 0.16 ND 16 12.5 12.5Mean 53.3 24.8 15.6 5.9 3.1 2.8 1.1Definition of abbreviations: AB asbestos body, FB ferruginous body, ND not detected; UF = uncovered fiber longer than 10 m.* The number of typical ABs was low, and analyses were performed on 20 uncovered fibers located and marked under light microscopy.†Mean concentration from three BAL samples (second and third samples obtained, respectively, 32 and 47 mo after the first one).‡Mean concentration of two samples (second sample obtained 13 mo after the first one).§Categories defined according to the main peaks in energy-dispersive X-ray spectrometry.on RCF and true ABs when applying the morphologic or opticalcharacteristics routinely used for light microscopy ABcounting. Indeed, the various types of pseudo-ABs would nothave been detected in the absence of the systematic electronmicroscopy screening test performed on all the BALF samplesexamined in our laboratory. For the period examined (1992through 1997), significant amounts of pseudo-ABs on RCFand other refractory fibers were observed in respectively 0.5%of all the patients examined, 1.5% of those with 1 AB/ml,and 2.3% of those with 5 AB/ml BALF. Moreover, pseudo-ABs formed only on other types of nonasbestos core fibers(crystalline silica and crystalline iron oxide) were detected intwo additional patients. All cases were revealed as a result ofthe abundance of pseudo-ABs or of RCF. The sensitivity ofthe electron microscopy screening test to detect bodies and fibersis much lower than that of light microscopy. In particular,when true ABs largely outnumber pseudo-ABs or if there areonly a few bodies, the presence of pseudo-ABs is more likelyto remain undetected. It is thus possible that there were additionalcases to those reported and that the foregoing percentagesare underestimated.There are no data about the presence of pseudo-ABs on RCFand other refractory fibers in the lungs of patients examined beforethe end of 1991. Accordingly, it is not possible to concludeon any time trends in the occurrence of such fibers in BALF, buttheir relative occurrence in comparison with asbestos fibers willprobably increase with increasing replacement of asbestos byRCF in industrial settings where high heat resistance is required.The patients were exposed as end-users or by working inthe vicinity of sources of refractory fibers and were never employedin the production of these fibers. Interestingly, all thesubjects had been exposed in foundries, steelworks, or aswelders. Exposure to refractory fibers had not been suspected,and a confusion with asbestos exposure in the occupationalhistory reported initially by the patients or the referent physiciansis obvious (Table 1). This reflects the similar applicationsof these two kinds of fibers and the lack of information aboutthe actual exposure conditions of patients using RCF.Figure 1. Light (A) and transmissionelectron microscopy (B)views of the same pseudo-ABon a RCF. Energy-dispersiveX-ray spectrometry chemicalcomposition spectrum (C) wasobtained from the fiber segmentindicated by an arrow.

502 AMERICAN JOURNAL OF RESPIRATORY AND CRITICAL CARE MEDICINE VOL 164 2001Figure 2. Light (A) and transmissionelectron microscopy (B)views of the same pseudo-ABon a crystalline iron compoundfiber. Energy-dispersive X-rayspectrometry chemical compositionspectrum (C) was obtainedfrom the fiber segmentindicated by an arrow.The detection of refractory fibers in the lungs confirms therelease of respirable fibers in the work environment of the patients.Mean airborne fiber concentrations measured duringinstallation or removal of RCF furnace insulation are close to1 fiber/ml air (16), but concentrations as high as 23 f/ml havebeen detected (17). This contrasts with the current fiber concentrationsat workplace in RCF production plants whichrarely exceed 1 fiber/ml (16, 18, 19). Similarly, the heaviest exposuresand the highest number of asbestos-exposed workerswere also not necessarily found in the production of asbestosor of asbestos-containing products.On the other hand, the variety of fiber types observed inthe BALF of our patients, including asbestos, silica-rich, andiron-rich fibers together with various refractory fibers, and thepresence of elevated concentrations of nonfibrous particles,reflects the complexity of mixed exposures in foundries, steelworks,and welding. The most probable hypotheses for silicarich,aluminum-rich, and iron-rich fibers are respectively siliconcarbide (5) or silica, aluminum oxide refractory fibers, andiron oxide (20) fibers released at workplace.Although RCF are reported to be fibrogenic and carcinogenicin animal experiments (21), there is no evidence in epidemiologicstudies on RCF production workers of an associationbetween workplace exposure and an increased risk oflung fibrosis, lung cancer, or mesothelioma (18, 22, 23). Thismust nevertheless be interpreted with caution, because of thesmall number of exposed workers in the cohorts [n 628 forthe European study (18) and n 652 for the U.S. study (23),respectively], the relatively short surveillance period, and theaverage low levels of exposure ( 1 fiber/ml air). Consequently,it is not yet possible to draw definitive conclusions on the riskssuch exposures may cause for exposed workers. In addition tothe observations from production workers, cohorts data areneeded concerning end-users who may be exposed to higherfiber levels and to mixtures of dusts.Radiologic studies have shown a possible association betweenexposure to RCF and pleural plaques (22, 23), althoughthis has not been confirmed by computed tomographic (CT)scan studies. The occurrence of pleural plaques after low-dosecumulative exposures to RCF is, however, plausible, by analogywith what has been observed with asbestos. In our series,however, the two patients with typical pleural plaques (Patients7 and 9) had a majority of asbestos fibers as body cores.The chest X-ray of Patient 3 showing a progressive massive fibrosiswith large opacities was more consistent with the diagnosisof silicosis than of asbestosis or idiopathic lung fibrosis.In Patient 8, benign asbestos-induced pleural effusion wasconsidered as the most probable diagnosis. Other studies haveTABLE 3. DIMENSIONS OF THE CORE FIBERS OF TRUE AND PSEUDO-ABsPseudo-asbestosBodiesAsbestos Bodies(All types)Mann-Whitneyp ValueNumber of core fibers analyzed 125 1,081Diameter, mGM (GSD; 95% CI) 0.27 (2.6; 0.23–0.32) 0.14 (2.8; 0.13–0.15) 0.0001Range 0.01–2.0 0.01–1.65Length, mGM (GSD; 95% CI) 35.4 (1.9; 32.2–39.0) 31.8 (1.74; 30.8–32.9) 0.01Range 6–338 5–276Aspect ratioGM (GSD; 95% CI) 136 (2.8, 113–163) 219 (2.6; 207–232) 0.0001Range 15–2,300 15–6,300

Dumortier, Broucke, and De Vuyst: Pseudo-asbestos Bodies on RCF 503also indicated a possible promoting effect of RCF on airwaysobstruction in smokers (18).Last but not least, despite the widespread use of glass wool,rock wool, and slagwool for insulation, we were unable to detectferruginous bodies on such fibers in the whole series of1,800 electron microscopy screening tests. Only one alteredrock wool structure was detected. This is largely in accordancewith the hypothesis that those materials mainly release nonrespirablefibers or that these fibers are not biopersistent (24).ConclusionsAB counting in BALF or lung tissue remains in most cases avalid marker of asbestos exposure but attention must be paidto a possible occurrence of ferruginous bodies on nonasbestosfibers in end-users of RCF. Targeted electron microscopic fiberanalysis in BALF is helpful if exposure to such fibers issuspected. The RCF detected in BALF showed size characteristicssimilar to those of amphibole asbestos fibers. Occupationalgroups at risk of exposure to RCF should be identifiedand airborne fiber measurements need to be performed toevaluate exposure levels in these groups. Preventive protectionmeasures must be taken to minimize the exposure ofthese workers.References1. Churg AM, Warnock ML. Asbestos and other ferruginous bodies; theirformation and clinical significance. Am J Pathol 1981;102:447–456.2. Morgan A, Holmes A. The enigmatic asbestos body: its formation andsignificance in asbestos-related disease. Environ Res 1985;38:283–292.3. Churg A, Warnock ML, Green N. Analysis of the cores of ferruginous(asbestos) bodies from the general population: II. True asbestos bodiesand pseudoasbestos bodies. Lab Invest 1979;40:31–38.4. De Vuyst P, Vande Weyer R, De Coster A, Marchandise FX, DumortierP, Ketelbant P, Jedwab J, Yernault JC. 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