Study Article

B R I E F R E P O R T

Geographic distribution of incidence of pericardial and paratesticular mesotheliomas in the USA

Sarah J. Lowry1 • Noel S. Weiss1

Received: 8 April 2016 / Accepted: 25 October 2016 / Published online: 3 November 2016

� Springer International Publishing Switzerland 2016

Abstract

Purpose Exposure to asbestos is thought to cause the large

majority of pleural mesotheliomas in the USA. It is

unknown whether asbestos exposure plays a role in the

etiology of rarer forms of mesothelioma, e.g., those located

in the pericardium or in the tunica vaginalis of the testis. In

order to address this question, we sought to determine

whether geographic patterns of incidence of these

mesotheliomas have paralleled those of pleural

mesotheliomas.

Methods We used age-adjusted incidence data from the

nine populations served by the National Cancer Institute’s

Surveillance, Epidemiology, and End Results program

during 1973–2011. Among men ages C50 years, we

compared the incidence of pericardial and paratesticular

mesotheliomas, respectively, with the incidence of pleural

mesothelioma across the nine populations.

Results The rate of pleural mesothelioma was approxi-

mately twice as high in the San Francisco–Oakland (SFO)

and Seattle–Puget Sound (SPS) areas compared to the other

regions. In contrast, rates of paratesticular and pericardial

mesotheliomas were not elevated in SFO (n = 3 parates-

ticular, 1 pericardial) or SPS (n = 4 paratesticular, 1

pericardial) relative to other regions.

Conclusions The results of this ecologic study do not sup-

port a role for asbestos exposure in the etiologies of either

pericardial or paratesticular mesotheliomas; however, this

study was limited by small numbers and was unable to

directly ascertain asbestos exposure.

Keywords Mesothelioma � Asbestos � Pericardial mesothelioma � Paratesticular mesothelioma � SEER

Introduction

Occupational exposure to asbestos is a well-established

cause of mesothelioma of the pleura [1–3]. However, no

doubt due to their relative rarity, the etiologies of pericar-

dial, and paratesticular mesotheliomas (which arise in the

tunica vaginalis, spermatic cord, epididymis, and tunica

albuginea [4]) has received little attention. It has been sug-

gested that asbestos may play a role in these mesotheliomas

as well [5, 6]. We hypothesized that if the incidence of either

(or both) paratesticular or pericardial mesothelioma was

strongly related to asbestos exposure, their incidence would

have been highest in the parts of the USA in which the

incidence of pleural mesothelioma has been highest.

Methods

We conducted an ecologic study using nine registries of the

National Cancer Institute’s (NCI) Surveillance, Epidemi-

ology, and End Results program (SEER) to compare geo-

graphic patterns of the different types of mesothelioma.

Because the majority of pleural mesotheliomas are thought

to be caused by asbestos exposure [1–3], we hypothesized

that the regional patterns in incidence of paratesticular and

pericardial mesotheliomas would parallel those of pleural

mesotheliomas if in fact occupational asbestos exposure

causes those rarer types as well.

& Sarah J. Lowry [email protected]

1 Department of Epidemiology, School of Public Health and

Community Medicine, University of Washington, 1959 NE

Pacific Street, Health Sciences Bldg, F-262,

Box 357236, Seattle, WA 98195, USA

123

Cancer Causes Control (2016) 27:1487–1489

DOI 10.1007/s10552-016-0825-3

The nine population-based SEER cancer registries

included in this study were established between 1973 and

1975 in San Francisco–Oakland, Seattle–Puget Sound,

Connecticut, Detroit (metropolitan area), Hawaii, Iowa,

New Mexico, Utah, and Atlanta (metropolitan area). Each

registry seeks to include data on every cancer diagnosed

within the specified region, as well as data on age, sex,

race, year, and specific details on diagnosis. Previous

studies have reported the SEER registries to be approxi-

mately 97% complete [7, 8]. We limited our study popu-

lation to men aged C50 years at diagnosis, because most

occupational exposure to asbestos has historically occurred

in men. Also, risk of pleural mesothelioma increases with

age and tends to occur many years after the earliest

exposure to asbestos [2].

We used ICD-O-3 histology codes 9050/3–9053/3 to

identify cases of mesothelioma. To distinguish mesothe-

liomas of specific anatomic sites of interest, we used the

collaborative staging (CS) designation in the SEER registry

(CS v. 02.04, which corresponds to the 7th edition of the

AJCC Cancer Staging manual) [9]. The SEER*Stat soft-

ware (version 8.1.5) [10] was used to generate age-adjusted

rates and 95% confidence intervals (CIs) based on the US

2000 standard population, for each of the nine SEER

regions.

Results

Among men C50 years old, the annual incidence of pleural

mesothelioma was approximately 99 per million in the

Seattle–Puget Sound region and 76 per million in the San

Francisco–Oakland region, compared to between 31 and 55

cases per million in the remaining seven geographic

regions (Table 1). Higher rates observed in the Seattle–

Puget Sound and San Francisco–Oakland regions have

previously been attributed to the fact that a larger fraction

of the population had been employed in the shipbuilding

industry, which historically had high levels of exposure to

asbestos [11]. There were four and three cases of parates-

ticular mesothelioma that were reported among residents of

the Seattle–Puget Sound and San Francisco–Oakland

populations during the period of the study, corresponding

to rates of 0.29 and 0.15 cases per million person-years,

respectively. The range of incidence among the remaining

seven SEER populations was 0.16–1.03 per million person-

years. Similarly for pericardial mesothelioma, the one case

diagnosed in the Seattle–Puget Sound population and the

one in the San Francisco–Oakland population did not

correspond to an elevated rate relative to that in the other

seven SEER populations.

Discussion

Prior literature on the relationship between asbestos

exposure and pericardial and paratesticular mesotheliomas

is limited. A study based on a national mesothelioma

registry in Denmark reported that the incidence of pleural

mesothelioma in men steadily increased between 1943 and

2009, rising from \0.1 to 1.76 cases per 100,000 person- years, whereas incidence of pericardial mesothelioma

remained at a relatively constant low level of incidence

(\0.1 cases per 100,000 person-years) over that period

Table 1 Incidence of pleural, paratesticular, and pericardial mesothelioma in nine SEER regions of the USA among males C50 years

Person-years Pleural Paratesticular Pericardial

Cases Rate a

(95% CI) Cases Rate a

(95% CI) Cases Rate a

(95% CI)

US Region b

San Francisco–Oakland SMSA 18,041,379 1,188 76.40 (72.02–80.97) 3 0.15 (0.03–0.46) 1 0.08 (0–0.39)

Seattle (PS) 16,285,389 1,370 99.19 (93.88–104.72) 4 0.29 (0.07–0.75) 1 0.11 (0.00–0.50)

Connecticut 16,768,718 821 54.70 (50.95–58.65) 7 0.43 (0.17–0.91) 0 0.00 (0.00–0.25)

Detroit (Metr.) 18,595,840 764 48.28 (44.82–51.95) 3 0.21 (0.04–0.63) 2 0.12 (0.01–0.44)

Hawaii 5,576,302 206 39.94 (34.59–45.88) 1 0.16 (0.00–1.01) 2 0.49 (0.06–1.67)

Iowa 15,027,083 574 39.55 (36.35–42.95) 6 0.43 (0.16–0.94) 1 0.07 (0.00–0.40)

New Mexico 7,459,983 352 51.42 (46.05–57.24) 5 0.69 (0.22–1.66) 7 0.98 (0.38–2.07)

Utah 6,978,251 318 51.57 (45.92–57.72) 2 0.37 (0.04–1.28) 3 0.51 (0.10–1.48)

Atlanta (Metr.) 8,347,185 196 30.85 (26.39–35.83) 7 1.03 (0.37–2.26) 1 0.09 (0.00–0.78)

Sites of mesothelioma defined according to a diagnosis with mesothelioma (ICD-O-3 histology code of 9050–9055, and with CS Schema v 0204

categories assigned as follows: Pleura includes CS Schema v 0204 sites ‘‘Pleura’’ and ‘‘Lung.’’ Paratesticular includes ‘‘Testis,’’ ‘‘Scrotum,’’

and ‘‘Genital Male Other.’’ Pericardial includes ‘‘Heart’’. Metr. metropolitan, P Puget Sound, CI confidence interval) a

Rates are age adjusted to the 2000 US population ages 50 ? years and are expressed as number of cases per 1,000,000 person-years b

All 1973–2011 except Atlanta (1975–2011) and Seattle (Puget Sound) (1974–2011)

1488 Cancer Causes Control (2016) 27:1487–1489

123

[12]. Additionally, some prior studies have used national or

regional mesothelioma registries which include data on

cases’ history of possible asbestos exposure; however, such

studies have been somewhat limited by data missingness,

inconsistencies in exposure ascertainment approaches

across regions, and/or lack of exposure data on non-cases

[13–15]. Other studies of mesothelioma incidence which

include mention of pericardial or paratesticular disease

include no more than one or two cases of these types of

mesothelioma [16, 17].

This study found no association between the incidence of

either pericardial or paratesticular mesothelioma and that of

pleural mesothelioma, across nine regions of the USA. This

is, however, an ecologic study based on very small numbers

of cases, which was unable to directly ascertain asbestos

exposure, and thus, the strength of evidence is limited. The

absence of a correlation in this study suggests that the

association between asbestos exposure and these rarer forms

of mesothelioma, if there is one, may not be as strong as the

association with pleural mesotheliomas.

Acknowledgments This manuscript was supported by the National Cancer Institute Training Grant 2T32CA009168-36.

References

1. Robinson BW, Musk AW, Lake RA (2005) Malignant

mesothelioma. Lancet 366(9483):397–408 (PMID: 16054941) 2. Selikoff IJ, Lilis R, Nicholson WJ (1979) Asbestos disease in

United States shipyards. Ann N Y Acad Sci 330:295–311

(PMID: 294180) 3. Peto J, Doll R, Hermon C, Binns W, Clayton R, Goffe T (1985)

Relationship of mortality to measures of environmental asbestos

pollution in an asbestos textile factory. Ann Occup Hyg

29(3):305–355 (PMID: 4073702) 4. Akin Y, Bassorgun I, Basara I, Yucel S (2015) Malignant

mesothelioma of tunica vaginalis: an extremely rare case pre-

senting without risk factors. Singap Med J 56(3):e53–e55

(PMCID: PMC4371211) 5. Bisceglia M, Dor DB, Carosi I, Vairo M, Pasquinelli G (2010)

Paratesticular mesothelioma. Report of a case with comprehen-

sive review of literature. Adv Anat Pathol 17(1):53–70. doi:10.

1097/PAP.0b013e3181c66fbc (PMID: 20032640)

6. Mensi C, Pellegatta M, Sieno C, Consonni D, Riboldi L, Bertazzi

PA (2012) Mesothelioma of tunica vaginalis testis and asbestos

exposure. BJU Int 110(4):533–537. doi:10.1111/j.1464-410X.

2012.10932.x (Epub 9 February 2012; PMID: 22321205) 7. Zippin C, Lum D, Hankey BF (1995) Completeness of hospital

cancer case reporting from the SEER Program of the National

Cancer Institute. Cancer 76(11):2343–2350 (PMID: 8635041) 8. Nattinger AB, McAuliffe TL, Schapira MM (1997) Generaliz-

ability of the surveillance, epidemiology, and end results registry

population: factors relevant to epidemiologic and health care

research. J Clin Epidemiol 50(8):939–945 (PMID: 9291879) 9. Collaborative Stage Work Group of the American Joint Com-

mittee on Cancer (2012) Collaborative stage v02.04 coding

instructions. http://www.ncra-usa.org/files/public/PartISectio

n1and2v02.04.pdf

10. National Cancer Institute Surveillance, Epidemiology, and End

Results Program, SEER*Stat software www.seer.cancer.gov/

seerstat v. 8.1.5

11. Treggiari MM, Weiss NS (2004) Occupational asbestos exposure

and the incidence of non-Hodgkin lymphoma of the gastroin-

testinal tract: an ecologic study. Ann Epidemiol 14(3):168–171

(PMID: 15036219) 12. Skammeritz E, Omland Ø, Hansen J, Johansen JP (2013)

Regional differences in incidence of malignant mesothelioma in

Denmark. Dan Med J 60(3):A4592

13. Marinaccio A, Binazzi A, Di Marzio D, Scarselli A, Verardo M,

Mirabelli D, Gennaro V, Mensi C, Merler E, De Zotti R, Man-

gone L, Chellini E, Pascucci C, Ascoli V, Menegozzo S, Cavone

D, Cauzillo G, Nicita C, Melis M, Iavicoli S (2010) Incidence of

extrapleural malignant mesothelioma and asbestos exposure,

from the Italian National Register. Occup Environ Med

67(11):760–765. doi:10.1136/oem.2009.051466 (Epub 25 August 2010; PMID: 20798014)

14. Gemba K, Fujimoto N, Kato K, Aoe K, Takeshima Y, Inai K,

Kishimoto T (2012) National survey of malignant mesothe-

lioma and asbestos exposure in Japan. Cancer Sci

103(3):483–490. doi:10.1111/j.1349-7006.2011.02165.x (PMID: 22126592)

15. Mensi C, Giacomini S, Sieno C, Consonni D, Riboldi L (2011)

Pericardial mesothelioma and asbestos exposure. Int J Hyg

Environ Health 214(3):276–279

16. Maltoni C, Pinto C (1997) Mesotheliomas in some selected

Italian population groups. Med Lav 88(4):321–332 (PMID: 9396218)

17. Fujimoto N, Aoe K, Gemba K, Kato K, Yamazaki K, Kishimoto

T (2010) Clinical investigation of malignant mesothelioma in

Japan. J Cancer Res Clin Oncol 136(11):1755–1759. doi:10.1007/

s00432-010-0834-7 (PMID: 20213099)

Cancer Causes Control (2016) 27:1487–1489 1489

123