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Archives of Environmental Health: An International Journal Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/vzeh20

Occupational Sunlight Exposure and Melanoma in the U.S. Navy Frank C. Garland Gorham a

a b

b

a

b

, Martin R. White , Cedric F. Garland , Eddie Shaw & Edward D.

b

Occupational Medicine Department Naval Health Research Center

b

Department of Community and Family Medicine , School of Medicine University of California , San Diego, California, USA Published online: 03 Aug 2010.

To cite this article: Frank C. Garland , Martin R. White , Cedric F. Garland , Eddie Shaw & Edward D. Gorham (1990) Occupational Sunlight Exposure and Melanoma in the U.S. Navy, Archives of Environmental Health: An International Journal, 45:5, 261-267, DOI: 10.1080/00039896.1990.10118743 To link to this article: http://dx.doi.org/10.1080/00039896.1990.10118743

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Occupational Sunlight Exposure and Melanoma

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in the U.S. Navy

FRANK C. GARLAND Occupational Medicine Department Naval Health Research Center and Department of Community and Family Medicine School of Medicine University of California San Diego, California MARTIN R. WHITE Occupational Medicine Department Naval Health Research Center

CEDRIC F. GARLAND Department of Community and Family Medicine and Cancer Center School of Medicine University of California-San Diego EDDIE SHAW EDWARD D. GORHAM Occupational Medicine Department Naval Health Research Center

ABSTRACT. Melanoma i s the second most common cancer, after testicular cancer, in males in the U.S. Navy. A wide range of occupations with varying exposures to sunlight and other possible etiologic agents are present in the Navy. Person-years at risk and cases of malignant melanoma were ascertained using computerized service history and inpatient hospitalization files maintained at the Naval Health Research Center. A total of 176 confirmed cases of melanoma were identified in active-duty white male enlisted Navy personnel during 1974-1 984. Risk of melanoma was determined for individual occupations and for occupations grouped by review of job descriptions into three categories of sunlight exposure: (1) indoor, (2) outdoor, or (3) indoor and outdoor. Compared with the U.S. civilian population, personnel in indoor occupations had a higher age-adjusted incidence rate of melanoma, i.e., 10.6 per 100 000 ( p = .06). Persons who worked in occupations that required spending time both indoors and outdoors had the lowest rate, i.e., 7.0 per 100 000 ( p = .06). Incidence rates of melanoma were higher on the trunk than on the more commonly sunlightexposed head and arms. Two single occupations were found to have elevated rates of melanoma: (1) aircrew survival equipmentman, SIR = 6.8 ( p < .05); and (2) engineman, SIR = 2.8 ( p < .05). However, there were no cases of melanoma or no excess risk in occupations with similar job descriptions. Findings on the anatomical site of melanoma from this study suggest a protective role for brief, regular exposure to sunlight and fit with recent laboratory studies that have shown vitamin D to suppress growth of malignant melanoma cells in tissue culture. A mechanism is proposed in which vitamin D inhibits previously initiated melanomas from becoming clinically apparent.

THE EPIDEMIOLOGY of cutaneous malignant melanoma i s paradoxical. Sunlight, particularly ultraviolet sunlight, has been suspected of causing melanoma because of the relationship of sunlight to other skin cancers and the ability of ultraviolet light SeptembedOdober 1990 [Vol. 45 (No.5 ) ]

to alter Whereas the epidemiology of melanoma i s complex, the complexities have not arisen from conflicting study results. Epidemiologic studies of individuals have been remarkably similar in their findings. Studies show that light skin pigmentation, 261

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a tendency to freckle, and light hair color are assoUsing SEER rates, we calculated Standardized Inciated with increased risk of m e l a n ~ m a . Perhaps ~-~ cidence Ratios (SIRS) and 95% confidence limits for unexpectedly, studies have also found that (a) melaall Naval occupations having at least one case of noma does not occur more frequently on the areas melanoma. Age adjustment was done using the inof the body most often exposed to ~ u n l i g h t , (b) ~ ~ ~ , direct ~~ method, a technique selected because the indoor occupations are at higher risk than outdoor number of cases i n some categories was not sufficient to provide the stability of rates appropriate for occupation^,^^-^^ and (c) high lifetime exposures to use of direct age adjustment.25 Confidence limits sunlight have been shown to decrease risk of melanoma.h, I b Also, studies of geographic patterns of were calculated using the Poisson distribution.L5 melanoma occurrence in Europe have found higher incidence rates of melanoma i n populations living in Results sunlight-deprived higher latitudes.17-19Placing these findings in a theory of etiology has perplexed invesA total of 176 confirmed cases of cutaneous maligtigators. The paradox has arisen because, if sunlight nant melanoma were included in the study. Diagi s a cause of melanoma, the findings regarding sunnoses were confirmed through review of the original light exposure are not what would be expected. medical records ( n = 95) or by a Medical or Physical Occupational studies may help clarify the role of Evaluation Board findings ( n = 81). Five cases listed sunlight as a cause of this disease. The Navy has a with a hospitalization of melanoma on computer large population working in occupations with widely files were excluded because review of original medvarying exposures to sunlight and other possible etiical records showed no diagnosis of melanoma. ologic agents.2DFor these reasons, we conducted a The average annual age-adjusted incidence rate study of the occurrence of melanoma in the Navy. for melanoma in U.S. Navy enlisted white males was 9.5 per 100 000 person-years, a rate not significantly Methods different from the SEER U.S. population rate of 9.2 per 100 000 (Table I ) . Age-specific rates were similar The Naval Health Research Center (NHRC) mainto those of the U.S. SEER population. tains a Service History File from data supplied by the Increasing duration of service appeared to have Naval Military Personnel Command that contains bano effect on the incidence of melanoma. The agesic demographic and occupational history informaadjusted average annual incidence rate of 9.7 per tion for active-duty enlisted Navy personnel.20 A 100 000 for those with 11 or more y of service was count of person-years contributed by enlisted perclose to that of personnel with fewer than 2 y of sersonnel by age, race, sex, and occupation for the 11vice, i.e., 10.1 per 100 000 (Table 2). y period (1974-1984) was done. Compared with the U.S. SEER population, personThe Naval Health Research Center also maintains nel in indoor occupations had a higher age-adjusted a computerized Inpatient Follow-up Data System incidence rate of melanoma 110.6 per 100 000 that contains all hospitalizations, deaths, and Medi( p = .06]. Outdoor workers had a nonsignificant cal Board and Physical Evaluation Board findings for lower risk of 9.4 per 100 000. Persons who worked in all active-duty enlisted personnel for the same peoccupations that required spending ti me indoors riod.”’ These medical data are provided by the Naval and outdoors had the lowest rate of 7.0 per 100 000 Medical Data Services Center in Bethesda, Mary( p = .06) (Fig. 1). land. In all occupational groups combined, melanoma Cases included all enlisted white male personnel occurred most frequently on the trunk [2.0 per who had a diagnosis of cutaneous malignant mela100 000 person-years (Fig. 21. The rate was statistinoma (International Classification of Diseases, cally significantly elevated on the trunk in outdoor Ninth Revision, Code 172) during January 1, 1974, to personnel (3.9 per 100 000 person-years, p < .05). December 31, 1984.l’ Confirmation of the diagnosis Rates were universally low on areas commonly exwas made by obtaining the original medical record posed to sunlight (range: 0.02 on the lip to 0.52 on from the treating hospital or from the National Perthe neck and scalp). sonnel Records Center in St. Louis, Missouri, where To determine whether a particular occupational medical records are sent for archival storage, or by group showed higher rates than would be expected obtaining a corroborating Medical or Physical Evalubased on the SEER population rates, we calculated ation Board (which usually consists of two or more standardized incidence ratios (SIRS) and 95% confiphysicians, including a specialist in the particular dence limits for each occupation with one or more disease). Age-specific and age-adjusted incidence cases of melanoma. Two occupations showed statisrates were calculated for all enlisted white male tically significantly high SIRS (Table 3): (1) aircrew active-duty Navy personnel (4 075 502 personsurvival equipmentman, SIR = 6.8 ( p < .05), and (2) years), and compared with rates provided by the engineman, SIR = 2.8 ( p < .05). Surveillance, Epidemiology, and End Results (SEER) Program of the National Cancer Institute.22At the Discussion beginning of the study, occupations were grouped Sunlight exposure. I n this study, as i n others, outinto indoor, outdoor, or both by review of Navy job door workers were at lower risk of melanoma than description^.^^,^^ 262

Archives of Environmental Health

Tabk 1.-Average Annual Alp-Specific Incidence Rates for C u t ~ c o u M r a l i n t Melanoma per 100 OOO, Active-Duty Enlisted Navy Pcrsond ud United States SEER Populath (White Maks, 1974-1904)

Population at risk

Age (Y)

Navy personnel No. Average annual cases incidence rate.

705 432 1 767 202 679 509 439 894 341 651 95 347 40-44 24 998 45-49 8 341 50-61 10 128 Unknown Total 4 072 502 Crude average annual rate Average annual age-adjusted rate*

10 45 38 26 42 10 3 2 0 1 76

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17-1 9 20-24 25-29 3634 35-39

SEER average annual incidence ratet 1 .o 2.6 5.1 7.6 9.7 12.0 15.6 17.7

1.4 2.6 5.6 5.9 12.3 10.5 12.0 24.0 0.0 4.3

-

9.5

9.2

'Navy incidence rates based upon first hospitalization for cutaneous malignant melanoma, International Classification of Diseases, 9th rev, Code 172.21 tUnited States population rates were provided by the Surveillance, Epidemiology and End Results (SEER), Incidence and Mortality Data: 1973-1981 *Adjusted by the indirect method using truncated (17 to 61 y of age) age-specific incidence rates provided by SEER and applied to the Navy population.

Table 2.-Average Annual Age-Adjusted Incidence Rates for Cutaneous Malignant Melanoma per 100 OOO by Duration of Service, Active-Duty Enlkted Navy Personnel (White Mak, 1974-1 984) Duration of service (Y)

Person-years at risk

No. cases

Age-adjusted rate*

0.61.9 2.63.9 4.0-6.9 7.0-10.9 11.0+ Unknown Total

1288 909 1 oo0560 5% 657 408 398 767 850 10 128 4 072 502

27 35 17 23 74 0 176

10.1 11.5 6.7 8.7 9.7

-

9.5

'Age-adjusted by the indirect method using truncated (17 to 61 y of age) age-specific incidence rates provided by the Surveillance, Epide Program and applied to

indoor workers, and workers with outdoor and indoor exposures had even lower risk. Cumulative exposure to sunlight has been shown by several investigators to decrease risk of 15, l6Melanoma, with the exception of lentigno malignant melanoma, has been shown to be unassociated with solar elastosis of the nearby skin.26This clinical finding suggests, as do epidemiologic findings, that cumulative exposure to the sun does not increase risk of melanoma or that individuals who exhibit elastoSeptembedoctober1990 [ V d . 45 (No. 5)]

'1

N-130 N-11

Indoor

Both

Outdoor

Fig. 1. Average annual age-adjusted incidence rate for melanoma by work category, activeduty enlisted Navy personnel, white males, 1974-1 984. *Significantly higher than the US. Surveillance, Epidemiology, and End Results Programzzpopulation at p = .06. **Significantly lower than the U S Surveillance, Epidemiology, and End Results Program2*population at p = .06.

sis are otherwise protected from the disease. Absence of exposure to the sun is common in persons not showing solar elastosis and in indoor office workers. CoI~ton and ~ ~Frampton2*have found specific vitamin D receptors in cultured human melanoma cells and have shown that vitamin D metabolites have a dose-dependent inhibitory effect on the growth of these cells in tissue culture. Vitamin D re263

8'

4-

Occupational category

3-

B

a

Number of cases shown above bars

2-

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Indoor Both Outdoor

Head

Trunk

Arms

Unspecified

Fig. 2. Melanoma Occurrence by type of occupation and site, active-duty enlisted Navy personnel, white males, 1974-1984. 'Significantly h m r than indoor or both Occupations at p < .05.

Table 3.-Standardized Incidence Ratios (SIRS)with 95% Confidence limits for Cutaneous M a l i p a n t M e l a m a for Occupations with Four or More C a m (Active-Duty Enlisted Navy Pemwml, White Males, 1974-1984)

Occupation Aircrew survival equipmentman Aviation ASW operator Engineman Boiler technician Aviation boatswain's mate Aviation electrician's mate Seaman recruit Yeoman Aviation structural mechanic Hospital corpsman Machinist's mate Electrician's mate Aviation machinist's mate Personnelman Sonar technician Aviation electronics technician Operation specialist Radioman Boatswain's mate Electronics technician All Navy occupations combined

I

No. cases

Population at risk

SIR

95% confidence limits

6 5 10 9 4 5 13 7 9 10 12 5 6 3 3 4 3 6 4 5 176

18 064 32 051 79 963 108 363 50 497 75 476 462 341 79 498 142 165 177 943 253 155 111 944 115 493 52 077 71 602 105 394 79 552 133 319 78 888 115 281 4 072 502

6.8 3.2 2.8 2.1 1.8 1.4 1.4 1.4 1.3 1.2 1.2 1.1 1.0 1.0 1.0 0.9 0.9 0.9 0.8 0.8 1.0

(2.5, 14.7)' (1.0, 6.7) (1.3, 5.1)* (1.0, 3.9) (0.5, 4.1) (0.4, 3.2) (0.8, 2.5) (0.6, 3.0) (0.6, 2.6) (0.6, 2.2) (0.6, 2.1) (0.4, 2.5) (0.4, 2.2) (0.2, 2.5) (0.2, 2.9) (0.3, 2.0) (0.2, 2.2) (0.3, 1.9) (0.2, 1.9) (0.3, 1.8) (0.9, 1.2)

'Significant at p < .05.

ceptors have also been described in other human cancer cell lines, and inhibition of growth by vitamin D metabolites has been reported for several cell lines of human breast and colon c a n ~ e r , Inhibi~~-~~ 264

tion of growth by vitamin D metabolites and increases in cell differentiation have also been reported for cultured human myeloid leukemia cells and rat osteogenic sarcoma cell^.^'-^^ A r c h i d Environmental HeaHh

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Pre-vitamin D is made in the epidermis and dermis during exposure to ultraviolet sunlight and immediately beings to isomerize to vitamin D.25Individuals who work for long periods of time indoors have been shown to have low levels of vitamin D.36r37 It is proposed here that low levels of vitamin D (either locally available in skin or circulating in plasma) allow melanomas that were previously initiated by sunlight exposure to develop into clinically apparent disease in individuals continuously deprived of sunlight. The line of reasoning for this hypothesis comes from the results of this study, longstanding epidemiologic findings by other investigators, and recent laboratory findings. Studies of mice injected with malignant melanoma cells and exposed to ultraviolet light (and presumed to have higher levels of circulating vitamin D) have shown exposed animals to have a 33% increased lifespan (16.5 wk compared with 12.0 wk in UV-B unexposed DeLuca and O ~ t r e mhave ~ ~ reviewed the role of vitamin D and cancer and conclude that "the vitamin D hormone suppressed growth of melanoma cells in culture . . ." These findings indicate a recently recognized property of vitamin D, which may explain the persistent finding of decreased risk of melanoma in outdoor workers. Vitamin D levels remain high for as long as 7 d in skin exposed to ultraviolet light.3sThe prolonged availability of locally produced vitamin D in the skin on exposure to sunlight may help to explain why melanoma is not more common in normally exposed sites or when solar elastosis is present. Exposure to the sun may increase the initiation of melanoma in sunlight-exposed sites but at the same time decreases the risk in these sites because of vitamin D levels locally produced in the skin. The two factors counter-balance, and commonly exposed sites are at no greater risk (or less risk) than commonly unexposed sites. The amount of ultraviolet light that reaches the melanocyte varies by wavelength. Ultraviolet-B transfers its energy primarily in the uppermost layers of skin, allowing only about 10-25% to reach the depth of the melanocyte.@Ultraviolet-A can penetrate deeper, and about 40% can reach the level of the m e l a n o ~ y t eAbout . ~ ~ 10-20 times as much ultraviolet-A passes through the stratospheric ozone layers to the earth's surface as ultraviolet-B.@Thesetwo factors suggest that at least 10 times as much Ultraviolet-A acts upon the melanocyte, and ultraviolet-A may be more important in the initiation or promotion of melanoma than ultraviolet-B. The most common sunscreens, including homomenthyl salicylate41and block almost solely Ultraviolet-6, thus preventing an erythema1 response but allowing excessive exposure to Ultraviolet-A. This study had one finding that appears to be unique to the Navy in regard to sunlight: persons in outdoor occupations had a significantly higher occurrence of melanoma on the trunk than did persons in indoor occupations with both exposures. Most studies have found that melanoma in persons Septernber/October 1990 [Vol. 45 (No. 5 ) ]

occupationally exposed to sunlight i s lower on normally unexposed sites such as the trunk. The Navy may have some unique exposure related to sunlight that may allow the transmittance of ultraviolet-A while almost entirely blocking transmittance of ultraviolet-B. Individual occupations.

In the Navy population, two occupations were found to be at significantly elevated risk of melanoma (Table 3): aircrew survival equipmentman (SIR = 6.8) and engineman (SIR = 2.8, p

Occupational sunlight exposure and melanoma in the U.S. Navy.

Melanoma is the second most common cancer, after testicular cancer, in males in the U.S. Navy. A wide range of occupations with varying exposures to s...
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