The assessment of the malignant mesothelioma cases and environmental asbestos exposure in Sivas province, Turkey

ORIGINAL PAPER

The assessment of the malignant mesothelioma casesand environmental asbestos exposure in Sivas province,Turkey

Serdar Berk • Huseyin Yalcin •

Omer Tamer Dogan • Kursat Epozturk •

Ibrahim Akkurt • Zehra Seyfikli

Received: 11 September 2012 / Accepted: 25 March 2013 / Published online: 4 April 2013

� Springer Science+Business Media Dordrecht 2013

Abstract One of the most significant diseases

related to environmental asbestos exposure is malig-

nant mesothelioma (MM). Sivas province is located in

the Central Anatolia where asbestos exposure is

common. We aimed to study clinical, demographical

and epidemiologic features of the patients with MM in

Sivas, along with the history of asbestos exposure. In

total, 219 patients with MM who were diagnosed in

our hospital between 1993 and 2010 were retrospec-

tively analyzed in terms of demographical and clinical

features. Rock, soil and house plaster samples were

taken from the habitats of those patients and were

evaluated with optical microscopy and X-ray diffrac-

tion methods. The age of the patients ranged between

18 and 85 years. The male-to-female ratio was 1.4:1.

Most of the patients confirmed an asbestos exposure

history. The most frequent symptoms of the patients

were chest pain (60 %) and dyspnea (50 %). The gap

between the start of first symptoms and the diagnosis

date was approximately 4 months in average. The

plaster materials used in most of the houses were made

up of mainly carbonate and silicate minerals and some

chrysotile. Ophiolitic units contained fibrous minerals

such as serpentine (clino ? orthochrysotile) chiefly

and pectolite, brucite, hydrotalcite and tremolite/

actinolite in smaller amounts. MM is not primarily

related to occupational asbestos exposure in our

region, and hence, environmental asbestos exposure

may be indicted. Yet, single or combined roles and/or

interactions of other fibrous and non-fibrous minerals

in the etiology of MM are not yet fully understood and

remain to be investigated.

Keywords Asbestos � Chrysotile � Environmental

exposure � Malignant mesothelioma

Introduction

The most common primary malignant tumor of the

pleura is malignant mesothelioma (MM), an insidious

neoplasm with a poor prognosis arising from the

mesothelial surfaces of pleural and peritoneal cavities,

as well as from the tunica vaginalis and pericardium.

Eighty percent of all cases of mesothelioma are pleural

in origin (Sterman et al. 2008). The development of

malignant pleural mesothelioma (MPM) is related to

asbestos exposure even if some patients have no such

contact history; the proportion of asbestos-associated

mesotheliomas varies in the literature from 16 to

90 %, probably depending on the accuracy of expo-

sure history (Walker et al. 1983). Asbestos refers to

mineral groups of thin fibers including serpentine type

S. Berk (&) � O. T. Dogan � K. Epozturk �I. Akkurt � Z. Seyfikli

Department of Chest Diseases, Faculty of Medicine,

Cumhuriyet University, 58140 Sivas, Turkey

e-mail: [email protected]

H. Yalcin

Department of Geological Engineering, Cumhuriyet

University, Sivas, Turkey

123

Environ Geochem Health (2014) 36:55–64

DOI 10.1007/s10653-013-9518-y

(chrysotile) and amphibole type (riebeckite/crocido-

lite, cummingtonite-grunerite/amosite, anthophyllite,

actinolite/tremolite). Nearly, 95 % of the asbestos

consumed worldwide is chrysotile and most other

fibers are commonly used in combination with it

(Weiner and Miandoab 2009). Although its use was

widely abandoned in the Western world in the 1980s,

the long latency period between the exposure to

asbestos and the onset of mesothelioma which could

range from 15 to 60 years meant that the mortality

rates from mesothelioma have continued to rise

(Moore et al. 2008).

Our institution is a tertiary referral hospital and

patients originate mostly from Sivas and three neigh-

boring cities, namely Tokat, Erzincan and Yozgat. The

province of Sivas is located in the mid-eastern part of

Anatolia. It includes 17 districts and 1,236 villages; its

population is approximately 600,000, 34 % of which

live in rural areas. Despite a fall in its use in recent

years, asbestos-contaminated soil has been used for

many years as a whitewash and stucco (named locally

as ‘‘white’’ or ‘‘barren’’ soil) in the wall of the houses

in rural areas. After the relationship between meso-

thelioma and asbestos emerged at the beginning of

1960s (Wagner et al. 1960), many studies have been

carried out on this topic and arguments have been still

continued within the scope of medicine and medical

geology (Yang et al. 2008). Previous studies have

revealed that environmental exposure to asbestos

through the use of asbestos-contaminated soil mix-

tures caused a high risk of MPM in some parts of rural

Anatolia in Turkey (Baris 1987; Baris et al. 1979;

Metintas et al. 2002; Senyigit et al. 2000; Yazicioglu

et al. 1980). We aimed in this study to investigate the

relationships between environmental mineralogical

effects and clinical, demographical and exposure

features of patients with MM in the Sivas province.

Materials and methods

Patients

A total of 219 patients with MM who were diagnosed

in our hospital between January 1993 and December

2010 were retrospectively analyzed. Of these, 207

(95 %) were diagnosed histopathologically and 12

(5 %) were diagnosed given the clinical and radiolog-

ical features suggesting MM and the presence of

asbestos exposure history. Clinical information,

including age, sex, birthplace, history of occupational

and environmental exposure to mineral fibers, char-

acter and duration of symptoms, and clinical findings

at presentation, was extracted from the patients’ files.

The environmental exposure is expressed as the

duration of living in houses where asbestos-contam-

inated soil was used.

A map including exclusively the ophiolitic units

with asbestos was prepared based on the 1:500,000

geological maps published by General Directorate of

Mineral Research and Exploration, and the numbers of

patients with MM were placed on it (Fig. 1).

Statistical analyses were performed using the SPSS

statistical software package for Microsoft Windows

(version 14.0, SPSS Inc, Chicago, IL, USA). Results

were expressed as mean ± standard deviation. Stu-

dent’s t-test was used for comparison between

patients. A p value of less than 0.05 was considered

to be statistically significant.

Fig. 1 Simplified map showing the location of serpentine-

bearing ophiolite units (simplified from MTA 2012) and

geographical distributions of patients with MM in the Sivas

and surrounding province (the eight patients from non-

neighboring areas were not marked on the map)

56 Environ Geochem Health (2014) 36:55–64

123

Mineralogical investigations

Since 1990s, hundreds of samples such as rock, soil

and house plasters were collected from habitats of MM

patients and analyzed by optical microscopy and

X-ray diffraction (XRD) methods at the Geological

Engineering Department laboratory and scanning

electron microscopy (SEM) with a JEOL JSM-6490

instrument equipped with IXRF energy dispersive

spectrometry (EDS) system at the Turkish Petroleum

Corporation in Ankara, Turkey. Textural and miner-

alogical features of coarse-grained hard samples with

fibrous minerals were determined on the thin sections

by binocular optical polarizing microscopy. SEM

operating conditions were 32 s counting time and

20 kV accelerating voltage. EDS spot analyses (spot

size of 50 lm for focused electron beam) were also

used during SEM investigations to differentiate

serpentine minerals from similar constituents.

The fine-grained whole-rock and clay fraction XRD

analyses were undertaken using a Rigaku DMAX IIIC

diffractometer with the following settings: Cu-Ka,

35 kV, 15 mA, slits (divergence = 18, scatter = 18,receiving = 0.15 mm, receiving monochromator =

0.30 mm), scan speed 2�2h/min. The semiquantitative

percentages of the minerals were calculated using the

external standard method. Serpentine-bearing clay

fractions (\2 mm) from the inorganic materials were

separated by the sedimentation method and analyzed

under air-dried (at 25 �C for 16 h), ethylene-glycolat-

ed (in a desiccator at 60 �C for 16 h) and heated

(490 �C for 4 h) conditions. Serpentine polytypes for

non-oriented powder samples have been detected with

diagnostic peaks.

Results

Epidemiology and clinical findings

Of the 219 patients, 126 (57.5 %) were men and 93

(42.5 %) women. The male-to-female ratio of the

patients was 1.4:1. The age of the men ranged from 18

to 85 years (mean, 58.8 ± 12.7 years). The age of the

women ranged from 34 to 85 years (mean, 58.9 ±

13.1 years). A large proportion of the patients

(28.8 %) were in the 60–69 years age group, 23.3 %

were 70 years old or above, and 17 patients (7.8 %)

were aged less than 40 years. The youngest patient

was diagnosed at the age of 18. There was no

significant difference in the mean age between men

and women.

More than 84 % of patients were farmers and

housewives, and they had lived in a rural area all their

lives or for a long time. Four (1.8 %) patients had an

occupational history with a potential risk for asbestos

exposure (one dozer operator, one painter, one railway

worker and one working with concrete sleepers). One

hundred and ninety-six (86 %) patients had a history

of living in a house containing asbestos-contaminated

soil, for about 40 ± 20 years in average (minimum: 3,

maximum: 70 years). The most frequent symptoms of

the patients were chest pain (60.2 %) and dyspnea

(50.2 %). There were approximately 4 months in

average between the start of the first symptoms and

the diagnosis date of the disease. There was no

significant difference between men and women in the

duration of symptoms (male: 3.7 ± 3.8 months,

female: 3.9 ± 4.5 months). Table 1 displays some of

the demographical and clinical characteristics of the

patients.

When the places of residence of 219 patients were

assessed, it was determined that 172 (78.5 %) patients

were residing in Sivas and the rest in other provinces.

Nearly, half of the patients came from Yildizeli district

(see Fig. 1).

According to the data from local civil registry

office, it was determined that 34 % of the total

population and 82 % of the population in Yildizeli

particularly were residing in rural areas (Table 2).

Geological and mineralogical findings

Ophiolites are parts of the Earth’s lithosphere that

surfaced above sea level and are often made of green

rocks such as serpentine. Ophiolitic units bearing

serpentine group of mainly Cretaceous age and their

transported products into soils are widespread and

extend hundreds of kilometer in Turkey and particu-

larly in Sivas region based on the map of MTA (2012)

(see Fig. 1). In the Ulas district of southeastern Sivas,

the dark green unaltered peridotitic ultramafic rocks

are preserved as lens-like forms of 1–5 m within the

serpentinites which are cut by thin-coarse grained and

grayish green-black pyroxenite, gabbro and diorite

dykes of commonly 1–2 m (partly 20–30 m) in

thickness. The host rocks of asbestos are layers of

approximately 100 m thick and brecciated

Environ Geochem Health (2014) 36:55–64 57

123

serpentinites of 10–20 m thick. Of these, first is of

blackish green to brown-honey-colored, mesh-tex-

tured, soapy, slippery and abundant cracks, and the

other is similar to layered ones but made up of angular

to sub-angular grains ranging a few mm to 15 cm in

size.

Asbestos occurrences show various morphologies.

Ones in the layered serpentinites have numberless

veins with millimeters to 4 cm thick that are usually

parallel to each other and crosswise in places (Fig. 2a).

Asbestos fibers filling vertically the fractures have a

silky brightness, light green colored, soft and easily

bended and separated one from another (Fig. 2b).

Asbestos veins in the brecciated serpentinites show a

limited distribution and a thickness of 0.1–0.5 cm and

partly cut grains (Fig. 2c). Pseudo-asbestos (picrolite)

veins and lenses with 1–20 cm thick are present in the

layered serpentinites with zigzag structure that contain

white-green prismatic-acicular chrysotile and cut

sometimes asbestos levels (Fig. 2d).

Asbestos-related rocks are ultramafics, serpenti-

nites and listwanites. White-colored ophicarbonate

(calcite, dolomite, aragonite and magnesite), ophihy-

droxide (brucite) and ophisilicate (quartz) mineraliza-

tion are present within the 1–10-cm-thick cracks of

serpentinites as a result of listwanitization. Alteration

zones including white- to black-colored hard rocks

with nearly 1–2 m thick are encountered within the

layered serpentinites. Altered and unaltered pyroxe-

nite, gabbro and basalt mainly are represented by

pyroxene (enstatite, augite, diopsite), amphibole

(hornblende, tremolite/actinolite, eckermannite), pla-

gioclase, vesuvianite, garnet, prehnite, pumpellyite,

natrolite, epidote, chlorite and chromite minerals.

Ophiolitic sequences in the Sivas province contained

fibrous minerals, mainly serpentine ([90 %) and some

pectolite, brucite, hydrotalcite and tremolite/actinolite

(\10 %) in a few samples (Fig. 3).

Scanning electron microscopy (SEM) image shows

that lizardite minerals have platy-like forms (Fig. 4a),

but chrysotile minerals have fibrous and acicular

morphologies with 20–100 lm length that are formed

of bundles with a great number of fibers (Fig. 4b).

Thin and long crystals of chrysotile are usually parallel

to each other and partly curved.

Phyllosilicates are represented by serpentine, chlo-

rite, C–S, talc, brucite and smectite in the asbestos-

related rocks. Serpentine polytypes showed 1T lizar-

dite for platy forms in the layer and brecciated

serpentinites (Fig. 5a), but 2M1 clinochrysotile in

the prismatic-acicular picrolites (Fig. 5b), and

2M1 ? 2Or clino ? orthochrysotile in the fibrous

asbestos (Fig. 5c), based on the identifications of

Bailey (1980).

The plaster materials used in most of the houses of

the patients with MM from Sivas region included

chiefly carbonate, such as calcite, aragonite and/or

dolomite (50–70 %), and silicate minerals, such as

quartz, feldspar and clay (10–30 %), and in a lesser

extent (5–10 %) chrysotile.

Discussion

Malignant mesothelioma (MM) is primarily a disease

of adults and usually presents in the fifth to seventh

decades, and 70–80 % of the cases occurs in men

Table 1 Demographics, exposure history and clinical data of

the patients

Characteristics of the patients (n = 219) n (%)

Sex

Male 126 (57.5)

Female 93 (42.5)

History of asbestos exposure

Yes 190 (86.7)

No 8 (3.7)

Uncertain 21 (9.6)

Occupation

Farmer 88 (40.2)

Housewives 97 (44.3)

White-collar workers 15 (6.8)

Blue-collar workers 6 (2.8)

Unoccupied 13 (5.9)

Symptoms

Chest pain 132 (60.2)

Breathlessness 106 (50.2)

Weight loss 52 (24.6)

Cough 50 (27.9)

Location of MM

Pleural 211 (96.3)

Right hemithorax 99 (46.9)

Left hemithorax 85 (40.3)

Bilateral hemithoraces 11 (5.2)

Not specified 16 (7.6)

Peritoneal 8 (3.7)


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(Moore et al. 2008). Occupational asbestos exposures

were more frequent in men, whereas environmental

asbestos exposure was found to be nearly as frequent

in men and women (Senyigit et al. 2000). In a study

from Turkey, for the environmental asbestos exposure

series of Selcuk, the average age was 50 years, with

one-fourth of the patients being less than 40 years old,

and the male-to-female sex ratio of the patients was

one (Selcuk et al. 1992). Rarely, MM occurs in

patients younger than 20 years (Fraire et al. 1988).

The reasons for such cases were suggested to be

related to genetic predisposition and other unknown

factors other than asbestos exposure. In our series, the

average age at the time of diagnosis was 59 and the

male-to-female ratio was 1.4:1. The youngest patient

was diagnosed at the age of 18 and had no asbestos

exposure.

Malignant pleural mesothelioma (MPM) is more

commonly found to be unilateral (95 %) and located in

the right chest (60 %). The initial clinical presentation

for most patients with MPM is progressive dyspnea

and/or steady chest wall pain. The symptoms may be

insidious and non-specific such that the time from

initial presentation until diagnosis is often 3–6 months

(Ismail-Khan et al. 2006). Our study revealed that

unilateral hemithorax (mostly right hemithorax) was

involved in 87.2 % of the patients, in accordance with

the current literature. The most frequent symptoms of

the patients were chest pain (60 %) and shortness of

breath (50 %). The average time between the onset of

symptoms and the diagnosis was 4 months.

Earlier studies reported various numbers (about

5–30 %) for the frequency of malignant peritoneal

mesothelioma among all MM cases (Bridda et al.

2007; Marinaccio et al. 2007). This variation was

thought to result from confusing peritoneal mesothe-

lioma with abdominal neoplasms, such as peritoneal

serous carcinoma and ovarian serous carcinoma

(Marinaccio et al. 2010). In our series, less than 4 %

of the patients had peritoneal involvement. This

slightly smaller percentage could be the result of

encoding flaws in records.

Exposure to asbestos is identified in 50–90 % of the

patients with MM (Metintas et al. 1999). The latency

period between the time of initial exposure and the

diagnosis is about 30 years and ranges from 20 to

50 years (Carbone et al. 2002). A meta-analysis

involving 21 studies was published in 1992 and the

latency period was calculated as 32 years (Lanphear

and Buncher 1992). In a study evaluating the asbestos

Table 2 Average population of Sivas region and number of malign mesothelioma cases between 1993 and 2010

Regions Average number of

total population (n)

Average number of

rural population n (%)

Number of

MM cases n (%)

Central district of Sivas 308,607 40,118 (13) 47 (21.5)

Yildizeli 51,261 42,034 (82) 102 (46.5)

Kangal 28,506 12,827 (45) 5 (2.3)

Sarkisla 41,046 16,418 (40) 4 (1.8)

Divrigi 19,660 6,291 (32) 3 (1.4)

Imranlı 8,826 5,207 (59) 3 (1.4)

Hafik 9,666 7,056 (73) 2 (0.9)

Susehri 28,120 14,341 (51) 2 (0.9)

Zara 22,399 10,303 (46) 2 (0.9)

Ulas 14,380 10,209 (71) 1 (0.5)

Gemerek 30,036 11,113 (37) 1 (0.5)

Other districts of Sivasa 47,485 29,440 (62) –

Total 60,9992 205,357 (34) 172 (78.5)

Neighboring cities of Sivasb Not specified Not specified 39 (17.8)

Non-neighboring regions Not specified Not specified 8 (3.7)

a Koyulhisar, Gurun, Dogansar, Akincilar, Golova, Altinyaylab Tokat (n = 33); Erzincan (n = 4); Yozgat (n = 2)


123

exposure history of 2,544 patients with MM, occupa-

tional exposure was reported to last 43 years and

household exposure to last 48 years (Marinaccio et al.

2007). In another study, Metintas et al. (2002) found

that people living in rural areas were exposed to

asbestos since birth until the diagnosis and that the

latency time was the same for both sexes, being

59.2 years.

Most of our patients declared to have lived in rural

areas and had environmental asbestos exposure for

many years. Furthermore, no difference in the duration

of exposure was identified between men and women.

Only a small proportion of our patients had a history

for possible occupational exposure. These findings

suggest that environmental exposure to asbestos is

more important in our region compared to

work-related asbestos exposure in urban areas and

that women are exposed to asbestos as much as men.

In recent years, rural–urban migration increased in

Sivas region and newly built houses do not contain

asbestos-contaminated soil. Therefore, it can be

expected that the number of people exposed to

environmental asbestos and the duration of such

exposure will decrease in the years ahead.

Chrysotile is the most common type of asbestos and

accounts for about 90 % of the world’s asbestos

production. Whether chrysotile caused MM had been

the focus of several studies. Some scientists suggested

that chrysotile played an important role in the

pathogenesis of MM because chrysotile fibers induced

DNA damage and chromosome abnormalities in

human and rat mesothelial cells in vitro and caused

Fig. 2 Field photomacrograph of serpentine-type minerals,

a chrysotile fiber alternations parallel to each other within the

cracks of a serpentinite rock, b the silky brightness and light green-

colored asbestos fibers filling vertically the fractures, c asbestos

veins in the brecciated serpentinites cutting partly grains, d the

layered serpentinites with zigzag structures. (Color figure online)


123

MM in animals (Yang et al. 2008). Some authors

claimed that chrysotile may cause MM but at a lower

rate compared to amphibole asbestos. Hodgson and

Darnton stated that the exposure-specific risk of MM

is broadly in the ratio of 1:100:500 for chrysotile,

amosite and crocidolite, respectively (Hodgson and

Darnton 2000). Other authors have instead proposed

that chrysotile did not cause MM and that the

amphibole that often contaminated chrysotile was

the causative agent (Yarborough 2006). On the other

hand, Suzuki et al. (2005) proposed that chrysotile was

the main contributor to the causation of MM based on

their analysis of lung and mesothelial tissues taken

from 168 cases of MM, in which they found that

chrysotile was the most common asbestos type.

White-soil samples displayed contamination with

tremolite, tremolite-chrysotile complex, or various

combinations of actinolite, anthophyllite, or chrysotile

in Eskisehir Region of Turkey (Metintas et al. 2002).

Yazicioglu had also detected tremolite and chrysotile

asbestos in Southeast Turkey (Yazicioglu 1976;

Yazicioglu et al. 1980). Baris et al. 1988 found a

non-asbestos fibrous mineral (erionite) causing MM in

the Cappadocia region of Central Anatolia, which is

approximately 300 km away from the study region.

Asbestos minerals (serpentine: chrysotile; amphi-

bole: riebeckite/crocidolite, cummingtonite-grunerite/

amosite, anthophyllite, actinolite/tremolite) and other

fibrous minerals (pyroxene, pyroxenoid and some non-

silicates) occurred in the metasomatic rocks such as

Fig. 3 The optical microscopy microphotographs of fibrous

and associated minerals from Divrigi area (Srp serpentine, Brc

brucite, Htl hydrotalcite, Act actinolite, Scp scapolite),

a serpentine ? calcite, b serpentine ? brucite, c serpen-

tine ? hydrotalcite, d actinolite ? scapolite


123

mafic, ultramafic, alkali plutonic, metamorphic and

serpentinized ultramafic rocks (Yalcin and Bozkaya

2000, 2004). Volcanic and particularly pyroclastic

rocks contain acicular and/or fibrous zeolites which

are erionite, mordenite, phillipsite, natrolite and

thomsonite (Gundogdu et al. 1996; Temel and Gun-

dogdu 1996; Yalcin 1997). All formations hold an

important place in the geology of Turkey and cover

approximately 10 % of Anatolian lands on the basis of

geographical distribution of ophiolites from geology

map of Turkey (MTA 2012). However, these minerals

were found to be about 1 % in weight and/or volume,

in relation to weather conditions, because they were

scattered within the rocks and soils except for

commercial asbestos deposits.

The study had some limitations. First, the exposure

time to asbestos was self-reported. Therefore, the

latency period could be miscalculated. Second, the

study was focused on asbestos exposure and other

possible factors related to mesothelioma development

were excluded. Third, although this study assessed the

presence of asbestos fibers in the habitat of the patients

with MM, it did not include histopathological findings

that may reveal a causative relation between asbestos

and MM.

Fig. 4 SEM photomicrographs of serpentine minerals, a platy

types of lizardite, b fibrous types of chrysotile

Fig. 5 XRD patterns of serpentine polytypes, a lizardite,

b clinochrysotile, c clinochrysotile and orthochrysotile


123

The mineralogical analyses obtained in this study

showed that MM disease was common in northern

regions of Sivas (especially Yildizeli district) where

serpentine-bearing ophiolite complexes were abun-

dant. On the other hand, the relationship between MM

and the distance of ophiolites could be correlated, as

evidenced by Bayram et al. (2012).

This finding questions the previous opinions

regarding the roles of different asbestos types in the

etiology of MM. However, the unique or combined

effect and/or interactions of other fibrous and non-

fibrous minerals on the development of MM are not

fully known yet and remain to be proven.

Acknowledgments The authors would like to thank the villagers

for their help in the field study, patients and their families for their

patience and department staff for their contribution.

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The assessment of the malignant mesothelioma cases and environmental asbestos exposure in Sivas province, Turkey