Reproduced, with permission, from:
Stenbeck, K. D., K. P. Balanda, M. J. Williams, I. T. Ring, R. MacLennan, J. E. Chick, and A. P. Morton. 1990. Patterns of treated non-melanoma skin cancer in Queensland--the region with the highest incidence rate in the world. Medical Journal Australia 153: 511-15.
ABSTRACT The incidence of non-melanoma skin cancer, comprising basal cell carcinoma, was studied in Queensland during 1984. The world-standardised annual incidence rates (per 100 000 population) for the number of persons with non-melanoma skin cancer were estimated to be 1372 for men and 702 for women, the highest recorded incidence rates in the world. Rates in men were nearly double the rates in women and age-specific incidence rates increased curvilinearly with age. There were, on average, 1.4 skin cancers per person with non-melanoma skin cancer and the ratio of basal cell carcinomas to squamous cell carcinomas was approximately three to one. The age-standardised annual incidence rate (per 100 000 population) of basal cell carcinoma for residents of the Gold Coast was 1.83 times the Brisbane rate for men and 1.57 times that for women, indicating significant differences between the two regions. For squamous cell carcinoma the regional differences were not statistically significant. The average potential number of non-melanoma skin cancers (per person) treated during the lifetime of a cohort of 100 000 was estimated to be 0.014 for men and 0.009 for women by age 40. By age 65, these numbers increased to 0.22 for men and 0.11 for women. At age 90, these average numbers were 1.09 and 0.42 respectively. Although the incidence of non-melanoma skin cancer is much higher in the older age groups, it should be kept in mind that it also affects the younger population; 1028 Queenslanders under 40 required treatment for 2300 non-melanoma skin cancers in 1984. This study which provides baseline information about the occurrence of non-melanoma skin cancer in Queensland emphasises the importance of developing safe sun-exposure habits, detecting non-melanoma skin cancer early and protecting and restoring the atmosphere.
(Med J Aust 1990; 153: 511-515)
Australia, particularly the area above latitude 29deg. south, has the highest incidence rates of non-melanoma skin cancer in the world.[1] Queensland lies between latitudes 10deg. and 29deg. south. Cumulative exposure to ultraviolet radiation is a risk factor for the development of non-melanoma skin cancer,[2] and it is expected that depletion of the ozone layer will increase the incidence of skin cancer.[3] Previous studies have investigated incidence rates for regions of Queensland from data supplied by the Queensland Radium Institute[4] or from pathologists' and dermatologists' records.[5]
Accurate estimates of the patterns of incidence of non-melanoma skin cancer in Queensland are needed to enable changes to be monitored. Standard cancer registry methods are inadequate, since only tumours confirmed by histopathological examination (about two-thirds of non-melanoma skin cancers treated in Queensland) are recorded as a routine. In a national incidence study which also reported State estimates,[1] respondents to a market research household survey in 1985 were asked if they had been treated for skin cancer in the past six months, and details were then extracted from medical records. This study relied heavily on the response and recall of those who were interviewed and on existing medical records.
To describe in detail the regional incidence of treated non-melanoma skin cancer in Queensland, a survey of general practitioners and hospital outpatient departments was conducted in 1984. The average potential number of non-melanoma skin cancers per person at different ages was estimated from the survey incidence data. It should be emphasised that such a survey will underestimate the true incidence of non-melanoma skin cancer since only treated cancers are recorded.
Methods
The survey was conducted in four survey areas--Brisbane, the Gold Coast, Toowoomba, and Cairns. These major centres of population in Queensland were chosen to represent four regions of the State labelled Brisbane, Moreton, the Darling Downs-Southwestern Queensland, and North Queensland (Figure 1). About three-quarters of the State's general practitioners are located in the survey areas.
The Royal Brisbane and Princess Alexandra Hospitals in Brisbane, the Toowoomba General Hospital, and the Cairns and Gold Coast Base Hospitals were asked to record all new cases of non-melanoma skin cancer diagnosed in their outpatient departments during the survey period. Random samples of 50 general practitioners were selected from Brisbane, Toowoomba and Cairns, 42 from the Gold Coast. In addition, nine general practitioners were selected from Mount Isa in northwest Queensland but were subsequently excluded because of unsatisfactory data. The random selection of general practitioners ensures that the sample of doctors accurately represents the doctors in the survey area and regions. Specialists who treat non-melanoma skin cancer such as dermatologists and surgeons were excluded from the study because patients require referral to them by a general practitioner. A medical practitioner recruited the general practitioners and a trained nurse conducted follow-up.
Each general practitioner and outpatient department was requested to report all basal cell carcinomas and squamous cell carcinomas diagnosed during a six-month period (within the interval March to October 1984 with variable starting dates) on standard recording sheets. Details of the patient's age, sex, diagnosis and the anatomical site of the cancer (coded 0 to 9 using ICD 9[6]) were recorded for each non-melanoma skin cancer. The data sheets for the general practitioners also included details of patients referred elsewhere. Histological diagnosis was known in 66% of the cases; in the remaining 34% the clinical diagnosis was used in the analysis Since some patients required treatment for multiple non-melanoma skin cancers both the number of persons (counting people only) and the number of cancers (counting each cancer separately) were analysed. It was assumed that the patients treated by a provider in the survey resided in the region
Regional age-specific count estimates were obtained by applying appropriate weights to the number of patients and non-melanoma skin cancers recorded in each survey area for both diagnostic methods--those confirmed by histopathological examination and those clinically diagnosed. For the general practitioner stratum these weights were the ratio of the number of general practitioners in the entire region to the number participating in the survey from the corresponding survey area. For the outpatient department estimates, the weights were the ratio of the total daily average occasions of service for non-inpatients for all hospitals in the region to the total daily average occasions of service for non-inpatient for the participating hospitals in the corresponding survey area. These weights were further adjusted to provide annual estimates. Regional, State and diagnostic method-specific estimates were obtained by summing the estimates from the appropriate strata. Age-specific incidence rates were obtained from the count estimates based on the 1983 estimated resident populations.[7] World-standardised rates were calculated by means of the method of direct standardisation.[8] This approach assumes that the number of patients and the diagnostic patterns seen by general practitioners and the staff of outpatient departments in a survey area are representative of those seen by general practitioners and outpatient department staff in the corresponding region.
Variance estimates were calculated by assuming a Poisson distribution for the number of patients presenting to general practitioners and outpatient departments and the number of non-melanoma skin cancers diagnosed within each age group and region during the survey period.[8] Tumour numbers were sufficiently large for the large-sample normal approximation to then be used to calculate confidence limits (CL) for age-standardised rates. The concept of the average potential number of non-melanoma skin cancers that a person will develop by age x, assuming that everyone in that birth cohort survives until age x, was developed from the waiting time onset distribution up to the step where lifetime prevalence, not estimated in our survey, was required.[9] Finally, the number of histologically confirmed cancers was compared with the number registered at the Queensland Cancer Registry.
Results
Forty general practitioners did not participate for various reasons (not in practice, 4; retired, 7; not able to be contacted, 6; deceased, 1; refused to participate, 5; dropped out, 14; not in area, 3), leaving 152 general practitioners in the analysis. All invited hospital outpatient departments participated.
During the survey, 3048 tumours were recorded, with 2805 non-melanoma skin cancers (2106 basal cell carcinomas and 699 squamous cell carcinomas) and 243 other tumours including benign lesions, keratoacanthomas and intraepidermal carcinomas; 1503 people were treated for basal cell carcinomas and 566 for squamous cell carcinomas.
The annual State estimates of histologically confirmed cancers were compared with histologically confirmed cancers notified to the Queensland Cancer Registry in 1982. There was good agreement between the two: the current survey underestimated the registry notifications of basal cell carcinomas by 5% and overestimated squamous cell carcinomas by 4%.
The estimated annual total number of newly diagnosed non-melanoma skin cancers for the State in 1984 was 41 542 (29 570 persons with non-melanoma skin cancer), comprising 30 972 basal cell carcinomas and 10 570 squamous cell carcinomas, with a crude basal cell carcinoma to squamous cell carcinoma ratio of 2.92. It was estimated that 78% of the cancers were seen by general practitioners and the remaining 22% were treated at hospital outpatient departments. Brisbane accounted for 38% of the estimated number, followed by North Queensland (24%), Moreton (22%) and Darling Downs-Southwestern Queensland (16%). Brisbane constitutes 47% of the Queensland population, North Queensland 18%, Moreton 13% and Darling Downs-Southwestern Queensland 22%. A relatively larger proportion of non-melanoma skin cancers, therefore, occurred in Moreton and North Queensland while a relatively smaller proportion occurred in Brisbane and the Darling Downs. These differences persisted after age-standardisation (Tables 1 and 2).
The estimated annual age-standardised rates (per 100 000 population) for non-melanoma skin cancers, basal cell carcinomas and squamous cell carcinomas for each region and sex are shown in Table 1 (for the number of persons) and Table 2 (for the number of cancers). The rate for men with non-melanoma skin cancer was estimated to be 1372 (95% CL, 1267, 1476), the estimate for women was 702 (95% CL, 630,773), and overall the rate was 1012. The Queensland age-standardised rates for the number of persons with non-melanoma skin cancer are depicted in Figure 2. This graphical representation highlights the difference between the rates in men and women, and also the regional differences, with Moreton and North Queensland showing higher rates than Brisbane and the Darling Downs.
The annual age-specific rates of non-melanoma skin cancer (per 100 000 population) for each region are shown in Table 3. These increased with age at a rate somewhere between linear and exponential, as shown in Figure 3. For those under 40, the State-wide rates were 122 for men and 100 for women; for those 60-69 years, the rates increased to 5861 for men and 3008 for women. For those 80 years of age and over, the rates were 12 931 for men and 5120 for women. Rates for men were about double those for women, and there were, on average, 1.4 new cancers per person with non-melanoma skin cancer. Although the incidence increases with age, non-melanoma skin cancer also affects young people. It was estimated that 1028 persons under the age of 40 required treatment for 2300 non-melanoma skin cancers in 1984.
The age-standardised rates of basal cell carcinoma for persons in North Queensland and Moreton were similar, as were the rates for Brisbane and the Darling Downs, the former two being substantially larger. There was a similar pattern for squamous cell carcinomas in men the lowest rate being for the Darling Downs and the highest for North Queensland. For women with squamous cell carcinomas the lowest rates occurred in North Queensland and Brisbane and the highest rate in Moreton. However the squamous cell carcinoma rate for the number of cancers in women in North Queensland was relatively high due to the occurrence of multiple cancers. In general, for both basal cell carcinomas and squamous cell carcinomas the regional patterns were similar for the number of persons and cancers.
The age-standardised annual incidence rate of basal cell carcinoma (per 100 000 population) for men in Brisbane was 854 (95% CL, 708 1001) and for the adjacent Gold Coast was 1563 (959% CL, 1236 1891). These differences were statistically significant. For squamous cell carcinoma the rates for men were 425 and 448 respectively and for women the corresponding rates were 184 and 242 respectively. These differences were not statistically significant.
Most basal cell carcinomas occurred on the face in both sexes--41.5% of basal cell carcinomas in men and 46.6% in women. The next most frequent site was the trunk for men (15.7%) and the arm for women (17.3%). The more-exposed areas of the skin (the lip, eyelid, ear, face, neck and arm) accounted for 76.9% of basal cell carcinomas in men and 80.4% in women. In Brisbane 23.2% of basal cell carcinomas were found on less-exposed body areas (trunk and leg) compared with 26.6% in the Gold Coast sample. The difference was 3.4% (95% CL, - 1.2%,7.9%), which is not statistically significant.
The anatomical distribution of squamous cell carcinomas differed from that of basal cell carcinomas. For men, the most frequent site was the face (26.6%) followed by the arm (21.2%) and the leg (17.2%). For women, the most frequent site was the arm (33.2%), followed by the face (28.7%) and leg (15.7%). Less-exposed sites, the trunk and leg, accounted for 26.6% of squamous cell carcinomas in men and 26% in women.
The average potential number of non-melanoma skin cancers treated during a lifetime is shown in Figure 4. (This average number of non-melanoma skin cancers per person, multiplied by a factor of 10,[5] may be interpreted as the total potential number of treated non-melanoma skin cancers in a cohort of 100 000, assuming no deaths have occurred.) This number rose substantially in the older age groups, especially after age 60. At the age of 50, men had an average potential number of 0.055 non-melanoma skin cancers and women had 0.040. By age 65, this average had increased to 0.22 for men and 0.11 for women. At the age of 80, the average potential number of treated non-melanoma skin cancers was 0.67 for men and 0.29 for women. At age 90, in a cohort of 100 000 men, assuming no deaths, the total potential number of treated non-melanoma skin cancers was estimated to be 108 791, and in a cohort of 100 000 women to be 41 958.
Discussion
A survey of treatment providers offers an alternative method of estimating the incidence of non-melanoma skin cancer. It should be emphasised that this method will underestimate the true incidence, since only treated cancers are included. A population-based survey, such as the one conducted by Marks et al.,[10] would be required to cover all cases. However, to obtain estimates for the entire State by such a method would be prohibitively expensive. These survey estimates are fairly crude incidence estimates, but they nevertheless give useful indications of the patterns of newly diagnosed cases in Queensland. This method estimates non-melanoma skin cancers for which a biopsy or other treatment has been carried out, and in this sense offers an advantage over the method of the Queensland Cancer Registry, which records only cases for which a biopsy has been performed. Although the overall estimates of those histologically diagnosed cancers were in agreement with the figures from the Queensland Cancer Registry, it should be kept in mind that this is the first study to address the issue and is not meant to undermine the usefulness of cancer registries based on these findings.
A population-based survey conducted by Giles et al.,[1] designed to generate national rather than regional estimates of treated cancers, provided estimates for the region above latitude 29deg. south, which included Queensland. The age-standardised incidence rates for persons 14 years old and over (per 100 000 person-years) in this northern region were 1476 for men, 1004 for women and 1242 overall. Our treatment-provider survey, which included persons of all ages, found rates of 1372 for men, 702 for women, and 1012 overall. These rates are not directly comparable; different ages were included, and the estimates of Giles et al. are for an area which includes Queensland and all other regions north of the 29th parallel.
The estimates of the histopathologically diagnosed non-melanoma skin cancers broadly concur with the estimates obtained from the cancer registry. By surveying different regions, the current study was able to obtain estimates on a regional level. The large number of cancers reported made it feasible to study the patterns of occurrence of non-melanoma skin cancer in greater detail than possible in former studies.
Recently, Marks et al. have reported the results of a five-year prospective study, estimating the minimal age-standardised incidence rate for non-melanoma skin cancer in Maryborough, Victoria, to be 874 (per 100 000), with a basal cell carcinoma to squamous cell carcinoma ratio of 3.34.(10)
The highest standardised incidence rates recorded outside Australia were from a survey conducted in the United States in 1977-1978.[11] The rates (per 100 000) for the number of white persons of non-Hispanic origin with non-melanoma skin cancer in Albuquerque, New Mexico, were 751.9 for men and 403.2 for women. For all white persons in New Orleans the rates were 562.9 (men) and 264.2 (women); in Atlanta, 554.2 (men) and 281.1 (women); in the entire State of Utah, 450.5 (men) and 243.6 (women); and in the State of New Mexico, 443.5 (men) and 247.0 (women). In a study conducted in 1971, the same group estimated the age-standardised incidence rates (per 100 000) for the number of persons with non-melanoma skin cancer in Dallas-Fort Worth to be 539 (men) and 259 (women).[12] New Mexico, Dallas-Fort Worth, New Orleans and Atlanta all have warm climates similar to Queensland, although situated further from the equator. Keeping in mind that the standard populations used in calculating the rates were different, it is still apparent that Queensland's standardised rates (1372 for men and 702 for women) are nearly double those in the American cities.
These comparisons indicate that Queensland has the highest incidence rate for non-melanoma skin cancer in the world. Part of the reason for such high figures may be the tumours developing at a faster rate. As the atmosphere becomes increasingly damaged, this rate may well escalate.[3] Data showing contemporary rates are necessary to make comparisons between regions and to calculate temporal changes in the incidence of non-melanoma skin cancer within those regions.
The relationship between latitude[12] and lifestyle[10] for the development of non-melanoma skin cancer has been confirmed in our study. North Queensland, the region with the lowest latitude studied, showed the highest age-standardised rates. Brisbane and the Darling Downs, regions of similar latitude (and further from the equator than North Queensland), had similar rates which were significantly lower than those for North Queensland.
The Moreton (Gold Coast) population is quite complex, affected by selective migration of retired people and year-round tourism. Although close to Brisbane, the Moreton region showed age-standardised rates similar to those of North Queensland. The age-specific incidence rates in Moreton were significantly higher than those in Brisbane. A large number of basal cell carcinomas may be prevented if Gold Coast residents were to reduce their sun exposure to levels similar to those of Brisbane residents. Further surveys should include the respondent's place of residence and the age at which a non-melanoma skin cancer first occurred to enable more details to be estimated.
Although the potential to develop non-melanoma skin cancer is extremely high in Queensland, its occurrence is not unavoidable. There is evidence that non-melanoma skin cancer may be the result of excessive exposure to sunlight at an early age,[3] and because the incidence increases dramatically with age cumulative exposure to ultraviolet radiation is considered an important factor in the development of non-melanoma skin cancer.[2] Lifestyle changes aimed at reducing exposure to the sun should be instituted at an early age if the incidence of non-melanoma skin cancer is to be reduced. Efficient methods for the early detection and treatment of skin cancer should be made readily available. Finally, the atmosphere and its ozone layer need to be protected and restored.
Acknowledgments
We gratefully acknowledge the financial support of the Queensland Cancer fund for this study. The work of the general practitioners and casualty staff of the hospitals participating in the study is also greatly appreciated.
3. McCarthy W, Shaw H. Skin cancer in Australia. Med J Aust 1989; 150: 469-470.
9. Eland-Johnson R, Johnson N. Survival models and data analysis. New York: Wiley, 1980: 392-411.
(Received Feb. 8; accepted Jun 13, 1990)
