An evaluation of the risks of lung cancer and mesothelioma from exposure to amphibole cleavage fragments

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Abstract

Amphiboles are hydrated mineral silicates five of which occur in asbestiform habits as asbestos grunerite (amosite) asbestos, riebeckite (crocidolite) asbestos, anthophyllite asbestos, tremolite asbestos and actinolite asbestos] and non-asbestiform habits (grunerite, riebeckite, anthophyllite, tremolite and actinolite). The asbestiform varieties are characterized by long, thin fibers while non-asbestiform varieties such as cleavage fragments form short fibers with larger widths. The U.S. regulatory method for counting asbestos fibers (aspect ratio ⩾3:1, length ⩾5 μm) does not distinguish between asbestos and cleavage fragments. The method biases toward increased counts of non-asbestiform cleavage fragments compared to long, thin asbestos fibers. One consequence of this regulatory approach is that workers can be erroneously classified as exposed to concentrations of asbestos (asbestiform amphiboles) above the U.S. 0.1 f/mL exposure standard when in fact they are not exposed to asbestos at all but non-asbestiform amphibole cleavage fragments. Another consequence is that the known carcinogenic effects of asbestos may be falsely attributed to non-asbestiform amphibole cleavage fragments of the same mineral. The purpose of this review is to assess whether amphibole cleavage fragments pose the same risk of lung cancer and mesothelioma characteristic of amphibole asbestos fibers.

We identified three groups of workers exposed to non-asbestiform amphiboles: two groups exposed to grunerite (Homestake gold miners and taconite miners) and one group exposed to industrial talc containing non-asbestiform tremolite and anthophyllite in St. Lawrence County, NY. In addition to assessing strength of association and exposure–response trends in the non-asbestiform amphibole cohorts, comparisons were also made with cohorts exposed to the asbestiform counterpart (positive control) and cohorts exposed to the mineral (e.g. talc) that does not contain amphiboles (negative controls).

The cohorts exposed to non-asbestiform amphiboles had no excesses of lung cancer or mesothelioma. Similar results were observed in the negative control groups, in stark contrast to the excess risks of asbestos-related disease found in the asbestos cohorts. The only possible exception is the twofold increased risk of lung cancer where exposure was to industrial talc containing cleavage fragments of tremolite and anthophyllite. However, this risk is not considered attributable to the talc or amphibole cleavage fragments for several reasons. A similar increased risk of lung cancer was found in Vermont talc workers, studied in the same time period. Their exposure was to relatively pure talc. There was no relationship between lung cancer mortality and exposure measured as mg/m3 years and years worked. A case–control study reported that all the lung cancer cases were smokers (or former smokers) and attributed the excess to smoking. There were two mesothelioma cases among the NY State talc workers exposed to cleavage fragments of tremolite and anthophyllite, but talc is not a plausible cause because of too short latency and potential for previous asbestos exposure. The positive controls of tremolite asbestos and anthophyllite asbestos exposed workers showed excess risks of both lung cancer and mesothelioma and positive exposure–response trends. St. Lawrence, NY talc does not produce mesotheliomas in animals while amphibole asbestos does. In sum, the weight of evidence fully supports a conclusion that non-asbestiform amphiboles do not increase the risk of lung cancer or mesothelioma.

Introduction

Asbestos is a generic term applied to a group of hydrated fibrous mineral silicates. Their asbestiform habit permits them to be easily separated into long, thin, flexible, strong fibers and ultimately fibrils (single fibers). Included are the asbestiform serpentine (chrysotile) and the asbestiform amphiboles, riebeckite (crocidolite) asbestos, anthophyllite asbestos, grunerite (amosite) asbestos, tremolite asbestos and actinolite asbestos. These minerals also crystallize with non-asbestiform habits, their counterparts being lizardite or antigorite (chrysotile), riebeckite, anthophyllite, grunerite, tremolite and actinolite, respectively. Crystal habit is a description of the shapes in which a certain mineral is likely to occur, both in nature and when grown synthetically. Tremolite is a mineral in the tremolite–ferro-actinolite series that has fewer than 0.5 atoms of iron, and more than 4.5 atoms of magnesium per formula unit; actinolite has between 0.5 and 2.5 atoms of iron, and 2.5 atoms of magnesium per formula unit; ferro-actinolite has more than 2.5 atoms of iron per formula unit with the balance being magnesium.

By the early 1970s, airborne concentrations of asbestos fiber were being measured using “the membrane filter phase contrast method (PCM)”. In many countries, including the USA, this method was adopted for the regulatory control of asbestos. Fundamental to the method was the definition of a fiber as an elongated particle having a length: breadth ratio (aspect ratio) of at least 3:1 and a minimum length of 5 micrometers (μm). Such a definition does not allow the microcopist to distinguish between asbestos fibers and non-asbestos amphibole particles. Consequently, in work environments where there exist many elongated particles meeting the PCM fiber definition, they are counted as if they are “asbestos” even if they are neither asbestos minerals nor even amphiboles. This results in concern by workers and health professionals about health risks and potential economic impacts for companies mining ore deposits where amphibole minerals are present. This is because the amphiboles have cleavage planes such that when they are crushed they produce elongated prismatic particles called cleavage fragments.

All amphiboles that were once exploited commercially as asbestos have non-asbestiform counterparts. Hence, workers in industries where amphibole cleavage fragments are present, but not asbestos, are often erroneously reported as being exposed to asbestos based on current regulatory counting strategies and protocols. On the other hand, the evidence concerning the health consequences of exposure to cleavage fragments has never been widely understood. Industries involving exposure to cleavage fragments should not be exempt from similar controls to the asbestos industries, if elongated particles meeting the PCM definition of fibers pose qualitatively and quantitatively the same levels of health risk as their asbestiform counterparts. However, if cleavage fragments pose no or a lesser risk than the asbestos minerals, they should be regulated accordingly.

The purpose of this paper is to compare, as far as possible, the cancer risks (lung cancer and mesothelioma) for workers exposed to airborne amphibole cleavage fragments with those associated with exposure to amphibole analogues that formed asbestos fibers. Pneumoconiosis risk will not be compared because some of the minerals associated with the amphibole cleavage fragments are recognized in their own right as causing lung fibrosis (e.g.: talc and crystalline silica). However, pneumoconiosis is sometimes used to assess whether exposure is high enough and latency long enough to detect carcinogenic risk and to evaluate the exposure–response.

Section snippets

Methods

The extent to which the carcinogenic risks of exposure to cleavage fragments differ from those associated with exposure to asbestos was examined in several ways.

The potential of particles to cause health effects depends on the characteristics of the particles (e.g.: size, shape, respirability, solubility, toxicity, carcinogenic potential), the level and duration of exposure as well as host and other factors. It is important to determine whether amphibole cleavage fragments differ sufficiently

The amphiboles

The crystallographic structure of amphiboles consists of double chains of silica tetrahedra. Their general chemistry incorporates (Si, Al)8O22(OH)2. The amphibole group of minerals is made up of a number of mineral series. These series result from the substitution of different elements in the structure. For example tremolite and actinolite are part of a homologous series of minerals—tremolite–actinolite–ferro-actinolite with chemistry Ca2(MgFe)5Si8O22(OH)2. Actinolite is Ca2(Mg4.5Fe0.5)Si8O22

Properties of asbestiform and non-asbestiform amphiboles

While the chemical compositions of the asbestiform and non-asbestiform amphibole minerals are identical, the characteristics resulting from their differences in crystal habit are significant. The properties of the amphibole asbestos minerals include fibrous habit with parallel fibers occurring in bundles, fiber bundles with split or splayed ends, fibers showing curvature and fibers with high tensile strength. The high tensile strength and axial nature of asbestos means the diameters of asbestos

Grunerite occurrence

Grunerite is the mineralogically correct name for amphiboles of the cummingtonite–grunerite series in which iron is at the 50% point in the 100 times Fe/(Fe + Mg)) ratio. Amosite (from the “Asbestos Mines of South Africa”) is the commercial asbestiform product that was used in insulation and building materials. Grunerite asbestos is no longer mined.

The non-asbestiform variety of cummingtonite–grunerite (C–G) has no commercial use per se other than as an aggregate but occurs in nature in

Grunerite (amosite) asbestos

Amosite is the trade name given to a mineral that was previously mined in Penge region in the Transvaal of South Africa. The mineralogical name is grunerite asbestos. In the bulk specimen the fibers can be several inches long. The color, ranging grey to brown depends on whether the fiber was mined from a weathered or un-weathered zone. The size distribution of the airborne fibers in the mine and mill have been reported by Gibbs and Hwang (1980). In mining and milling 12.6% and 6.6%,

Non-asbestiform grunerite cohorts

Several groups of workers from Homestake gold mine and the Minnesota taconite deposits have been exposed to cleavage fragments of grunerite and studied to assess possible “asbestos-related” diseases (Table 3). The non-asbestiform amphiboles present in these mines generally crystallize in a prismatic habit with well-developed cleavage so breaks occur both perpendicular and parallel to particle length.

Comparison of mesothelioma experience

One method of assessing whether non-asbestiform grunerite acts similarly to grunerite (amosite) asbestos is to compare the proportional mortality from mesothelioma in grunerite (amosite) asbestos exposed workers and in non-asbestiform grunerite exposed workers. Mesothelioma is a cancer which can clearly be caused by amosite without known confounders such as smoking, although there are a small number of other potential causes (Pelnar, 1988, Price and Ware, 2004). Hodgson and Darnton (2000) argue

Comparison of lung cancer experience

There are statistically significant excesses of respiratory cancer in all the grunerite (amosite) asbestos industries (except mining). In contrast, it is very clear that, with the exception of the first small study of Homestake gold miners (Gilliam et al., 1976), there is no increased risk of lung cancer in the non-asbestiform amphibole exposed industries. The results from the study by Gilliam have not been reproduced in subsequent studies with complete ascertainment of the cohort and longer

Overall conclusion concerning asbestiform and non-asbestiform grunerite

It is evident that the “fibers” to which the non-asbestiform amphibole workers were exposed were considerably shorter (and wider) than those to which grunerite (amosite) asbestos workers were exposed. While both studies of grunerite (amosite) asbestos and non-asbestiform grunerite (plus other non-asbestiform amphiboles) may have limitations as far as estimates of fiber exposure are concerned, the results indicate very large differences in the mortality from mesothelioma and from lung cancer

The mineral talc

The term talc is used in two ways. First, it is a term applied to a commercial or industrial product that contains finely divided mineral or rock powder that usually, but not always contains the mineral talc as its main component. Second, it can refer to the mineral talc which is a phyllosilicate mineral with the chemical formula Mg6Si8O20(OH)4. Since talc is a metamorphic mineral it is often associated with other minerals and is rarely found in its pure form. Co-exposures are specific to each

The New York and Norwegian talc deposits

There are at least two talc deposits containing non-asbestiform tremolite and anthophyllite which have been studied, one in New York State and one in Norway (Table 6). The best known and best characterised is the industrial talc in New York. There has been considerable discussion in the literature concerning whether the tremolite and anthophyllite present in this talc is asbestiform or non-asbestiform. However, the evidence is supportive of non-asbestiform amphiboles (Skinner et al., 1988).

Non-asbestiform amphiboles in South Carolina vermiculite

There are several small vermiculite pits in South Carolina containing nearly 50% tremolite/actinolite but is believed to be virtually free of fibrous tremolite (McDonald et al., 1988). Mining and the first part of the milling process are carried out wet. Four types of elongated fibers were identified in air samples using analytical transmission EM and energy dispersive X-ray spectroscopy (EDSX): tremolite–actinolite (48%), vermiculite fragments (8%), talc/anthophyllite (5%), iron-rich fibers

Other talc deposits

There are several mortality studies of talc where amphibole minerals are reported to be absent and the talc is relatively “pure” talc. These include studies of workers in the Vermont talc mines (Selevan et al., 1979), Italian talc mines (Coggiola et al., 2003), French and Austrian talc mines (Wild et al., 2002) (Table 6). According to Wild et al. (2002) “no asbestos contamination has ever been clearly documented in the talc deposits, at least not in the European sites”.

Lung cancer in New York and Vermont talc miners and millers

In contrast to the high levels of amphibole cleavage fragments in New York’s St. Lawrence County talcs, geological studies conducted since the early 1900s have shown no “asbestos” and little quartz in Vermont talc deposits (Boundy et al., 1979). Analyses of bulk samples collected in 1975/1976 from mines and mills of the three major Vermont talc companies showed talc and magnesite as major components (20–100%) and chlorite and/or dolomite as minor constituents (5–20%). There were trace amounts

Italian talc

Italian talc is very pure and is used in the pharmaceutical and cosmetic industries. Miners and millers in this industry were studied for mortality (Rubino et al., 1976, Rubino et al., 1979, Coggiola et al., 2003). Miners were analyzed separately from millers because of silica exposure in the mine. The silica content of airborne dust in the mines was as high as 18% in drilling operations from footwall contact rocks, rock type inclusions, and carbonate, calcite and magnesite inclusions. The

French and Austrian talcs

Wild et al. (2002) conducted cohort studies of talc workers in France and Austria with nested case–control studies of lung cancer and NMRD. The French ore was a talc chlorite mixture with quartz contamination ranging from undetectable to less than 3%. In Austria, three mines were studied. At one site the ore was a talc–chlorite mixture with 0.5–4% quartz. Rock containing about 25% gneiss was not milled. A talc–dolomite mixture of 25% medium talc and <1% quartz in the final product was the

Asbestos-exposed cohorts for comparison with talc workers

There are two ore deposits containing tremolite asbestos or anthophyllite asbestos potentially suitable for comparison with the talc cohorts exposed to non-asbestiform tremolite and asbestos. One site is the vermiculite mine located in Libby, Montana with significant contamination from tremolite asbestos. The other is an anthophyllite asbestos mine in Finland.

Biological plausibility

Biological plausibility is not a necessary prerequisite to establishing a causal association, but it is considered “helpful” (Hill, 1965). Experimental evidence is available to consider whether or not cleavage fragments are more or less carcinogenic than asbestos fibers. These issues have been independently evaluated by Addison and McConnell and Mossman, elsewhere in this volume.

Experimental studies have the potential advantage of precisely defining the characteristics of the minerals and

Statistical analysis of potency by size, shape and mineralogy

Berman et al. (1995) conducted a statistical reanalysis of inhalation studies using data from studies of AF/HAN rats exposed to different types of asbestos to identify the exposure metrics that best predicted the incidence of lung cancer or mesothelioma. New exposure metrics were first generated from samples of the original dust because of limitations in the original characterizations. This analysis provided more detailed information on mineralogy [i.e., chrysotile, grunerite (amosite)

Other amphiboles and other minerals

A search of the literature for studies containing both health outcomes and descriptions of exposure to cleavage fragments failed to identify additional studies that would be of immediate assistance in examining the health risks associated with cleavage fragments. The review did identify studies such as that in Finland where the percentages of asbestiform tremolite and cleavage fragments and fibrous wollastonite and cleavage fragments of wollastonite were characterised in metamorphic limestone

Conflict of Interest

The authors declare that they have no conflicts of interest.

Funding Source

The article funded by The National Stone and Gravel Association.

Acknowledgments

We acknowledge with thanks the very helpful comments of Dr. Anne G. Wylie, Mr. John Addison, Dr. EE McConnell, and Mr. J. Kelse. This work would not have been possible without financial support from the National Stone Sand and Gravel Association, Alexandria, Virginia.

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