IIII
Skin cancer in a Queensland population Adele Green, M.B.B.S., Ph.D.,* Graeme Beardmore, M.B.B.S., F.A.C.D.,** Veronica Hart, M.B.B.S., F.A.C.D.,** David Leslie, M.B.B.S., F.A.C.D., Robin Marks, M.B.B.S., F.A.C.D.,*** and Donald Staines, M.B.B.S.****
Brisbane and Nambour, Australia In the present study we have estimated the current prevalence of actinic skin disease in young and middle-aged adults in Queensland, Australia by surveying a representative community. It was found that 4.6% of persons aged 20 to 69 years had skin cancer, mostly basal cell carcinoma, and 40% had solar keratoses. The age distribution and site distribution of actinic lesions in this population were not as classically described; persons below age 40 years exhibited substantial sun-related skin damage, and a large proportion of actinic lesions occurred on sites other than the head, backs, of hands, or forearms. Allowing for age and sex, the strongest risk factors for skin cancer and solar keratoses were fair skin, as assessed by a dermatologist, and clinical signs of solar damage such as solar lentigines, facial telangiectasia, and actinic elastosis of the neck. Associations with self-reported tendencies toward sunburn, frequent painful sunburns, occupational sun exposure, and a previous history of skin cancer were confirmed. (J AM Acrid DERMATOL1988;19:1045-52.)
The modern cult of sun worship among fairskinned populations is a source of increasing concern as melanoma and other types of skin cancer become more common/,2 This is especially true in tropical and subtropical Australia where solar ultraviolet levels are high and where, unlike in much of North America and Europe, opportunity for recreation in the sun is available to almost everyone all year long. Greater numbers of young persons are being seen with signs of sun damage and skin cancer] and in a survey of a Western Australian community 4 it was estimated that 17%
From the Queensland Institute of Medical Research,* Brisbane; the Royal Brisbane Hospital**; the Anti Cancer Council of Victoria***; and the Community Health Center,**** Nambour. Supported by the Queensland Cancer Fund and the Australian Cancer S~'iety. Dr. Green was supported by a Neil Hamilton Fairley Fellowship of the National Health and Medical Research Council of Australia. Accepted for publication Feb. 18, 1988. Reprint requests to: Dr. Ade[e Green, Queensland Institute of Medical Research, Bramston Terrace, Brisbane Q 4006, Australia. Dr. Leslie is in private practice in Nambour, Australia.
of men and 8% of women under age 40 years had solar keratoses. Accurate estimates of the occurrence of nonmelanoma skin cancer in most populations are prevented by lack of registration by cancer registries 5 and because many basal cell carcinomas and squamous cell carcinomas are treated destructively without histologic diagnosis, especially in areas of high incidence? Published studies of the prevalence of skin cancer in Queensland, Australia have been few, and none is recent. From 1961 to 1963 field surveys 7 provided an estimate of the prevalence of skin cancer and solar keratoses in samples of the general population. Prevalence 7,8 was defined as the percentage of the population over age 20 years who either gave a past history of basal cell carcinoma or squamous cell carcinoma or had the lesion diagnosed clinically during the field survey. The prevalence of skin cancer so estimated in southeast Queensland was 11.3% in men and 9.5% in women over age 20 years? The highest estimated prevalence of skin cancer was found in a tropical coastal population 8 where 22.7% of men 1045
1046
Journal of the American Academy of Dermatology
Green et al.
23o
~Nambour ~_~Brl sbane Fig. 1. Geographic location of Nambour, Queensland.
and 12.8% of w o m e n age 20 years and older were or had been affected? T h e aim of the present survey was to document precisely the current point prevalence and distribution of basal cell carcinoma, squamous cell carcinoma, and solar keratoses in southeast Queensland in young and middle-aged adults by direct examination of a total defined population. In addition, this would provide baseline data for future estimation of incidence a n d for study of trends in occurrence and treatment of skin neoplasia. SUBJECTS AND METHODS The survey was undertaken in Nambour, Australia, an urban center with a population of about 8500. It is situated at 26 degrees 37 minutes South latitude and 8.7 m above sea level and lies 30 km from resort beaches and 100 km north of the capital city, Brisbane, Australia (Fig. 1). In summer the average number of sunlight hours1~ and the solar ultraviolet levelsu are approximately the same as for the rest of the Queensland coast. The majority of the Nambour population was born in Queensland and engage in a range of outdoor and indoor occupations. A random sample of 3000 was chosen from the 5100 persons listed on the state electoral roll as residents of Nambour aged 20 to 69 years (enrollment is compulsory for Australian citizens aged 18 years or older). A total of 2045 persons responded to a letter of invitation to participate in the survey in December 1986. Of the nonresponders it was found that 315 (11%) were no longer residents of Nambour, 55 were temporarily
away (holidays and other travel), 17 could not participate because of illness, and six were dead. After the main survey 100 persons were randomly selected from the 562 nonresponders believed to be currently living in Nambour and were invited to an identical follow-up survey held in March 1987; 50 of the 100 original nonresponders attended. Thus 2095 residents of Nambour were seen, giving an overall 70% response from the electoral sample of 3000; among permanent residents of Nambour, the response rate was 78%. There was little difference in the response rate between sexes, but people aged 30 years and older had a 77% attendance compared with 51% among those aged 20 to 29 years. Participants were interviewed by means of a standard questionnaire. The information obtained included broad patterns of occupational and recreational sun exposure, acute reaction of the skin to strong sun when exposed for the first time in summer for an hour without protection, number of painful sunburns experienced, personal history and family history of skin cancer, and whether or not a suntan was considered healthy. Each subject in the survey was examined by one of 14 dermatologists* according to a set protocol. In 90% of subjects skin examination was confined to head and neck, backs of hands, and forearns (further areas were examined if clinically warranted); in a random 10% of aU subjects, systematic examination was extended to include the skin of the upper chest, back and shoulders, upper arms, and legs. The dermatologists recorded skin color; hair and eye color; number of nevi on the forearms; certain signs of actinic damage including solar lentigines, facial telangiectasia, and actinic elastosis of the neck; and number and site distribution of skin cancers and solar keratoses. (A solar lentigo was defined as a brown to brown-black or black macule occurring on sun-damaged skin with a well-defined edge that may be irregular and normal skin surface creases. When telangiectasia was observed on facial skin, it was graded in three categories from mild (+) with only occasional foci of dilated vessels to severe ( + + + ) where large areas of the face appeared florid with visible vessels. Actinic elastosis was diagnosed on the back, sides, or front of the neck if skin thickening and a well-defined furrowed network were present and was graded as mild to moderate (+) or severe (++). A solar keratosis was defined as a lesion with a variably thick and adherent *The followingdermatologistsparticipatedin the Nambour survey:J. Auld, G. Beardmore,S. Condon,M. Deakin,W. Harley,V. Hart, D. Leslie, R. Marks, P. McLaran, J. Nedwieh, R. Needham, S. Reid, I. Robertson,and G. Stephenson,with the assistanceof Dr. B. DeAmbrosis.
Volume 19 Number 6 December 1988
Skin cancer in Queensland population
1047
Table I. Age-specific prevalence rates of basal cell carcinomas per 100 people in Nambour, Queensland in December 1986 Basal cell carcinomas prevalence rate
No. of persons
Age (yr)
20-29 (nl = 407, n2 = 41) 30-39 (nl = 487, n2 = 34) 40-49 (n~ = 473, n2 = 45) 50-59 (n~ = 400, n2 = 45) 60-69 (nl = 328, n2 = 40) Total no. of persons (NI = 2095, N2 = 205) Total lesions
Head/neck/ hands/forearms
All other sites
Head/neck/ hands/forearms
[ I
All other sites
Total
0 3 6 11 9 29
0 0 1 1 4 6
-0.6 1.3 2.8 2.7 1.4
--2.2 2.2 10.0 2.9
-0.6 3.5 5.0 12.4 4.2
33
11
1.6
5.4
7.0
n~, Total number of persons examined in age group; n2, random sample of persons in age group who had all body sites examined.
hyperkeratotic surface, with or without pigmentation. When either basal cell carcinoma or squamous cell carcinoma was diagnosed, a biopsy specimen was obtained with the subject's consent, and each slide was examined by a dermatopathologist who made a histologic diagnosis without knowledge of the clinical diagnosis.) The measure of prevalence is the prevalence rate, L2 which in this study is the proportion of persons in the surveyed population who were diagnosed as having a particular neoplastic lesion of the skin. Associations between the prevalence of such lesions and various risk factors and clinical signs have been quantified by means of the prevalence odds ratio, ~3 which is the ratio of the prevalence odds among those exposed to the prevalence odds among those not exposed to a particular factor. (The prevalence odds is the prevalence rate divided by [ 1 minus the prevalence rate] in a given exposure category.) Associations considered of interest after univariate screening or on biologic grounds were investigated in multivariate models incorporating age, sex, and other potential confounding variables. Basal cell carcinoma and squamous cell carcinoma were considered together (basal cell carcinoma and squamous cell carcinoma) as the dependent variable "skin cancer" in the models rather than separately because of the small numbers involved. Logistic regression with generalized linear interactive model 3.77 was employed to estimate final prevalence odds ratios and their 95% confidence intervals. RESULTS There were 54 invasive, histologically confirmed skin cancers diagnosed in 43 of the 2095 subjects
who participated in the survey, and 11 of these cancers occurred on the randomly selected 205 subjects who were fully examined. The overall prevalence of skin cancer in this group was 4.6% and 7.5% in persons 20 to 69 years of age. Basal cell carcinoma occurred in 34 subjects (of whom 23 (66%) were men), with a prevalence rate of 4.2% of persons aged 20 to 69 years. The prevalence was 1.4% of persons with lesions on the head or neck, hands, or forearms (on the basis of all 2095 subjects); 2.9% of persons had lesions elsewhere on the body (on the basis of the random l 0% subsampie) (Table I). Highest age-specific prevalence rates were seen in persons aged 60 to 69 years, 2.7% having basal cell carcinoma on head, neck, hands, or forearms, and 10.0% having basal cell carcinoma on other sites (one subject had basal cell carcinoma present on several site categories: head, forearms, and other sites). There were nine subjects, seven men (78%), with squarnous cell carcinoma, giving a prevalence rate of 0.4% of persons aged 20 to 69 years; the highest rate of 1.5% again occurred among those aged 60 to 69 years (Table II). Squamous cell carcinoma was seen only on the head, neck, hands, and forearms in this survey population and was not observed in persons under age 40 years. Solar keratoses were diagnosed clinically in 834 (40%) of the survey population, yielding prevalence rates of 44.0% of men and 36.5% of women (Table llI). Among persons aged 20 to 29 years, prevalence rates of 9.5% and 5.3% were observed for
1048
Journal of the American Academy of Dermatology
Green et aL
Table II. Age-specific prevalence rates of squamous cell carcinoma per 100 people in Nambour, Queensland in December 1986 l Age (yr)
20-29 (n = 407) 30-39 (n = 487) 40-49 (n = 473) 50-59
No. of
Squamous cell carcinoma
persons
prevalence rate*
0
--
0
--
1
0.2
3
0.8
5
1.5
9 10
0.4 0.5
(n = 4o0)
60-69 (n = 328) Total persons Total lesions
*Squamous cell carcinomas were diagnosed only on head, neck, hands, and forearms.
men and women, respectively, and 10% had more than one lesion. At age 60 to 69 years prevalence of solar keratoses increased to 79.4% in men and 68.1% in women, with 67% of affected persons having more than one. Solar keratoses occurred on sites other than head, neck, hands, and forearms in 125 (61%) of those who received full examination. Well-known associations between the presence of skin cancer and factors relating to pigment phenotype and sun exposure were largely confirmed (Table IV). Fair skin, as assessed by a dermatologist, was strongly associated with the presence of basal cell carcinoma and squamous cell carcinoma (prevalence odds ratio 8.20) and with solar keratoses (prevalence odds ratio 6.33). Persons who stated that they did not burn after 1 hour of exposure to strong summer sun without protection had the lowest prevalence rate of neoplastic lesions, and those whose reported tendency was to burn and then tan had a higher relative prevalence of basal cell carcinoma and squamous cell carcinoma (prevalence odds ratio 1.82) compared with those who tended to burn only (prevalence odds ratio 1.01). Although there was no consistent association with occupational status beyond a slightly higher prevalence of skin cancer in nonprofessional workers, basal cell carcinoma and squa-
Table III. Age-specific prevalence rates of solar keratoses per 100 people in Nambour, Queensland in December 1986 Solar keratosis prevalence rate*
(yr)
Men (n = 404)
20-29 30-39 40-49 50-59 60-69 Total
9.5 30.5 46.9 64.3 79.4 44.0
Age
[
Women
(n = 430)
5.3 23.9 35.5 58.0 68.1 36.5
*Solar keratose~ were diagnosed on head, neck, hands, or forearms in all subjects also having solar keratose,s at other sites.
mous cell carcinoma were more prevalent among those who had worked mostly outdoors throughout life (prevalence odds ratio 1.76), as were solar keratoses (prevalence odds ratio 2.27). Multiple painful sunburns (six or more in fife) were also related to prevalence of skin cancer (for basal cell carcinoma and squamous cell carcinoma, prevalence odds ratio 1.66) and to prevalence of solar keratosis (prevalence odds ratio 1.47), but there was no consistent association when fewer than six sunburns were reported. A history of previous skin cancer treated by a physician was associated with approximately twice the prevalence odds of both skin cancer and solar keratosis. No independent association between skin cancer and recreational sun exposure was observed, although 78% of men and 62% of women whose occupations were mainly outdoors stated that their sports or leisure activities were spent mainly outdoors also. Because most (89%) of the survey population was born in Australia and had Australian parentage (81% had fathers born in Australia, and 76% had mothers who were born in Australia), the effect of age at migration to Australia or of ethnic background could not be assessed properly. Family history of the disease was common but was not associated with the prevalence of skin cancer or solar keratoses. Eye color, hair color, and number of nevi on the forearms failed to show any independent association with skin cancer prevalence. The only information about attitude to sun exposure,
Volutne 19 Number 6 D e c e m b e r 1988
Skin cancer in Queensland population
1049
Table IV. Associations between prevalence of skin cancer (basal cell carcinoma or squamous cell carcinoma) and solar keratoses and factors adjusted for age and sex relating to complexion, sun exposure, and previous skin cancer Basal cell carcinoma and Squamous cell carcinoma Survey population* Factor
Skin color Olive Medium Fair Short-term reaction to sun Tan only Burn then tan Burn only Occupational exposure]. Indoors Both indoors and outdoors Outdoors No. of painful sunburnsJ" 0 1 2-5 6+ Past history of skin cancer]" Absent Present
Solar keratosis
(n = 42)
(n = 834)
Prevalence odds ratio (95% confidence intervals)
Prevalence odds ratio (95% confidence intervals)
229 912 934
1.00 2.61 (0.33-20.67) 8.20 (1.05-64.20)
1.00 2.33 (1.55-3.50) 6.33 (4.16-9.64)
478 1293 323
1.00 1.82 (0.62-5.36) 1.01 (0.29-3.56)
1.00 1.06 (0.78-1.44) 1.63 (0.74-1.53)
947 677 470
1.00 1.01 (0.44-2.3 I) 1.76 (0.77-4.05)
1.00 1.29 ( 1.00-1.66) 2.27 (1.68-3.07)
264 329 923 579
1.00 0.77 (0.22-2.61) 1.09 (0.41-2.95) 1.66 (0.59-4.64)
1.00 1.35 (0.91-2.00) 0.99 (0.70-1.40) 1.47 (1.01-2.14)
1702 377
1.00 1.84 (0.94-3.46)
1.00 2.28 (1.72-3.02)
(n = 2095)
*Totals may vary as a result of mi.,zing information. +Prevalence odds ratios for these variables are adjusted for confounding effects of age, sex, skin color, and short-term reaction to sun exposure.
which was elicited in the survey, regarded the participant's stated belief in the healthful effects of having a suntan. It was found that 885 (42%) of the survey population considered a suntan healthy, though the belief was not significantly associated with the occurrence of actinic lesions. In comparison with associations between skin cancer and self-reported factors relating to sun exposure, the associations with observed clinical signs of excessive sun exposure were strong and consistent. Because of potential confounding among the different signs of actinic damage, they were included together in a final model with age and sex. The strength and significance of associations with individual clinical signs were diminished, although clear trends associated with increasing degree of sun damage remained (Table V). When more than 20 solar lentigines were observed on the backs of the hands, there was about a fourfold
higher prevalence of basal cell carcinoma, squamous cell carcinoma, and solar keratoses. Number of solar lentigines on the face showed similar though weaker trends in prevalence odds ratios. Other signs of actinic damage to the skin of the face, too, were strongly related to the presence of skin cancer. Compared with the prevalence of lesions when no facial telangiectasia was observed, a mild degree was associated with approximately a twofold increase in prevalence odds ratios, a moderate degree with a threefold increase, and severe telangiectasia (graded + + + ) was associat~ with prevalence odds ratios of 3.67 for basal cell carcinoma and squamous ceU carcinoma and 4.57 for solar keratoses. When severe elastosis of the neck was present, the prevalence odds ratios were 1.75 for basal cell carcinoma and squamous cell carcinoma and 2.24 for solar keratoses. Finally, the number of early neoplastic lesions was associated
Journal of the American Academy of Dermatology
1050 Green et al.
Table V. Association between prevalence of skin cancer (basal cell carcinoma or squamous cell
carcinoma) and solar keratoses and clinical signs of actinic damage
Clinical sign
Solar lentigines (hands) 0 1-10 11-20 >20 Telangiectasia (face) None Mild Moderate Severe Actinic elastosis (neck) None Mild-moderate Severe Solar keratoses (face) 0 1-5 6-20 21-50 >50
Survey population* (n = 2095)
Basal cell carcinoma or Squamous cell carcinoma (n = 42) Prevalence odds ratio (95% confidence intervals)
1557 408 88 41
1.00 1.61 (0.78-3.35) 1.43 (0.43-4.77) 3.78 (1.06-13.41)
1.78 (0.87-3.66) 1.73 (0.53-5.61) 4.10 (1.17-14.30)
878 936 244 37
1.00 1.63 (0.58-4.57) 2.74 (0.89-8.40) 3.67 (0.79-17.11)
1.00 1.71 (0.62-4.75) 3.10 (1.02-9.41) 4.57 (1.02-20.56)
1093 781 221
1.00 1.42 (0.53-3.80) 1.75 (0.56-5.45)
1.00
1377 467 192 21 38
1.00 1.55 (0.67-3.59) 1.86 (0.69-5.04) 3.00 (0.54-16.69) 2.72 (0.73-10.15)
Solar keratosis (n 834) Prevalence odds ratiot (95% confidence intervals) =
1.00
1.59 (0.61-4.18) 2.24 (0.75-6.67)
*Totals may vary as a resuR of missing information. tPrevalence odds r a f t s are adjusted for confounding effects of age, sex, and all signs of actinic damage apart from the one under consideration.
with prevalence of malignant skill lesions. The trends associated with solar keratoses on the face and on the hands were similar, and as more subjects (718, 34%) had keratoses present on the face than on the hands (493, 24%), the prevalence data for the former have been presented. Those who had over 20 keratoses counted on the face had a prevalence odds ratio for basal cell carcinoma and squamous cell carcinoma about three times that associated with no facial keratoses. When the random sample of original nonresponders who attended the ad hoc follow-up survey were assessed for comparability with the remainder of the survey population, they appeared similar and there were no significant (p > 0.05) differences in their patterns of occupational sun exposure, frequency of previous history of skin cancer, hair color, or the prevalence of solar keratoses on head and neck and hands and forearms.
DISCUSSION In the present study the observed prevalence of active skin cancer in a typical Queensland community was 4.6% of persons aged 20 to 69 years, thus confirming that this population has one of the world's highest rates of skin cancer. 14Persons aged 60 to 69 years were most frequently affected, and the lowest detectable rate of skin cancer (0.6%) occurred among those aged between 30 and 39 years. By means of whole-body examination of a random sample of participants we have also shown the extent to which sites other than the head, forearms, and hands may be affected by skin cancers. In persons aged 60 to 69 years, basal cell carcinoma appeared to be even more common on sites other than the face and hands. Because prevalence rates are affected not only by the rate of appearance (incidence rates) but also by the rate of disappearance of lesions, the observed reversal of
Volume I9 Number 6 December 1988
the classic site distribution2 of prevalent basal cell carcinomas probably reflects the high level of awareness of skin cancer among medical practitioners and the Queensland community at large. For example, of the 328 survey subjects aged 60 to 69 years, there were 120 (37%) on whom no active basal cell carcinoma was found on the head, forearms, or hands at the time of the survey but who gave a history of skin cancer treated by a physician at some time before the survey. Given the usual age and site distribution of skin cancer, the majority of these 120 persons probably had lesions on the head or hands, which were treated in the previous 5 years--lesions that might otherwise, if the community were less educated about skin cancer, have been diagnosed during our prevalence survey. The uncommon site distribution of basal cell carcinoma also reflects the uncommonly high sun exposure received by the whole body in the Queensland environment.15 Although the increasing prevalence of skin cancer and solar keratoses with increasing age is well-known, the high prevalence of actinic lesions in persons under age 40 years has not been documented accurately in Queensland before. We found that 7% of people in their twenties and 27% of those in their thirties had at least one solar keratosis compared with 74% of persons aged 60 to 69 years. The prevalence rates of solar keratoses are comparable to prevalence rates described among populations in other parts of Australia, 4' 16 which, despite large differences in latitude, receive similar solar ultraviolet-B levels during the summer months. ,1 The associations of skin cancers and solar keraroses with sun-sensitive complexion types and sun exposure have been described many times,~'9'~7 although the greater prevalence of skin cancer among persons who tended to burn and then tan after short-term sun exposure compared with those who burned without tanning, was unexpected. A possible explanation may be that those who never tan avoid the sun when possible. Also, the popular perception that a suntan is somehow protective (nearly half the population considered a suntan healthy) and socially desirable may result in higher prevalence rates of basal cell carcinoma and squa-
Skin cancer in Queensland population
1051
mous cell carcinoma among those who sunburn first after a lifelong pattern of attempting to acquire a tan. Actual clinical signs of excessive sun exposure such as solar lentigines on the backs of hands, facial telangiectasia, and actinic elastosis of the neck were the most consistent predictors of neoplastic lesions. Apart from an association between basal cell carcinoma and dermal elastosis diagnosed histologically, ~8 quantified associations with objective signs of solar damage have not been reported. Underlying such clinical signs of sun damage are the known photobiologic skin reactions to solar ultraviolet-B and ultraviolet-A radiation: enlargement of superficial and deep vascular plexuses and loss of collagen with shortening and homogenization of elastic fibers and atrophy of the epidermis? '9 The photobiologic mechanisms of carcinogenesis are not so clear. Ultraviolet-B rather than ultraviolet-A is regarded as being the carcinogenic component of sunlight,2~and there is experimental evidence of ultraviolet-induced systemic suppression of immunologic surveiUance. This immune suppression, which can be passively transferred with lymphoid cells containing suppressor T lymphocytes from ultraviolet-B-irradiated animals, 2' may result from an interaction between urocanic acid in the superficial epidermis and ultraviolet light~2 and perhaps from depletion of immunocompetent Langerhans ceils. 23 If people with solar skin damage were more likely to attend the skin cancer survey than those without, our observations could be biased. This, however, is considered unlikely given that a sample of the original nonresponders was similar to the original responders in the distribution of major risk factors and in the prevalence of clinical signs of actinic damage. Also, on reviewing known reasons for nonattendance among younger subjects, it was observed that of the 315 persons incorrectly registered on the electoral roll as current residents of Nambour, 74% were younger than age 40 years. Thus lack of opportunity to attend rather than lack of motivation because of low risk of skin cancer largely explained the relatively poor response rate among persons aged 20 to 39 years. Special surveys such as the Nambour survey described here remain the only way in which
1052
Journal of the American Academy of Dermatology
Green e t al.
a c c u r a t e population-based e s t i m a t e s of skin c a n c e r p r e v a l e n c e c a n be o b t a i n e d ? 4 I n high-risk p o p u l a tions, k n o w l e d g e of the prevalence o f skin c a n c e r is especially i m p o r t a n t to s t u d y incidence rates a n d m o n i t o r secular trends a n d t h u s e v a l u a t e t h e success o f preventive measures to lessen the individual b u r d e n of disease and the s u b s t a n t i a l e c o n o m i c c o s t 2~ to m e d i c a l services.
12. 13. 14. 15. 16,
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