a Hugh Adam Cancer Epidemiology Unit, Department of Preventive and Social Medicine, Dunedin School of Medicine, University of Otago, Dunedin, New Zealand.
Reprint requests to: J-L Bulliard, Institut universitaire de médecine sociale et préventive, rue du Bugnon 17, 1005 Lausanne, Switzerland. E-mail: Jean-Luc.Bulliard{at}inst.hospvd.ch
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Abstract |
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Methods Trends in incidence and mortality from melanoma in New Zealand were analysed between 1969 and 1993, by sex and body site. A graphical representation of the trend by birth-cohort and age-period-cohort modelling were used.
Results For all sites combined, the annual increase in incidence was 6.7% (95% CI : 6.37.1%) in men and 3.1% (95% CI : 2.33.7%) in women. The increase was significantly greater at each site for males. The largest increases occurred for the upper limbs in males (7.3% a year) and the trunk in females (3.8% a year). Incidence rates slowed appreciably in the later years (currently about 26/100 000 for each sex) and no further increase in lifetime risk of melanoma was observed among post World War II generations. Mortality trends paralleled those for incidence with a 25-year gap, with a more modest rate of increase (23% per annum for each sex), essentially due to the increased risk among generations born up to 1919 or 1924. Age-standardized death rates have now stabilized in New Zealand at about 5.5/100 000 (men) and 3.2/100 000 (women). Trends between cohorts were the most marked for sites with a likely intermittent pattern of exposure, and were consistent overall for the trunk and the limbs.
Conclusions Results support the hypothesis that changes in lifestyle factors resulted in a pattern of carcinogenic exposures that explains both the upsurge in melanoma in the last few decades and the current levelling off in incidence.
Keywords Melanoma, trends, incidence, mortality, New Zealand, body site
Accepted 17 December 1999
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Introduction |
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If the long-term increases are caused by changes in sun exposure and behaviour between generations, site-specific measurements have been recommended as the most effective way of monitoring these changes.9 Incidence trends have differed between melanoma sites and across Caucasian populations, both in their magnitude7,9 and in their pattern.1012 The greatest increase has generally occurred on skin areas exposed intermittently to solar ultraviolet and incidence trends for the trunk and the limbs have been consistent with birth-cohort changes in risk.8,12
Mortality is less sensitive than incidence to changes over time in ascertainment, detection and awareness, and provides a useful and complementary source to incidence for investigating time trends. New Zealand experiences some of the highest incidence and mortality rates from melanoma in the world13,14 and most registrations and death notifications include the site of origin. Incidence and mortality trends by melanoma site have not previously been reported in New Zealand.
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Materials and Methods |
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Data were aggregated in five quinquennial time periods (19691973, 19741978, 19791983, 19841988, 19891993). The 4th digit of the code of the International Classification of Diseases, Ninth Revision (ICD-9), was used to group the body sites into five regions: face, scalp and neck, trunk, upper limbs (which include the shoulder) and the lower limbs. Sex- and site-specific rates per 100 000 person-years were computed and directly adjusted to the World standard population.14 To separate the random and artificial components of the year-to-year fluctuations, which were substantial for some sites, 3-year average site-specific rates were calculated.
In addition to the existing code for unspecified skin site (172.9), a code for other specified skin site (172.8) was introduced in the ICD-9. During its first year of operation only, 1979, this new code was extensively used (in 21% and 49% of male and female registrations, respectively). Because this affected melanoma sites in different proportions, cases diagnosed in 1979 were excluded. Similarly, the site information from mortality records for 1988 was not used as the usual matching of the death and cancer records was incomplete and resulted in a much greater use of unspecified codes for that year.
Estimates of the time trends were based on Poisson log-linear regression using maximum likelihood methods available from GLIM.15 Statistical analyses were confined to people aged 20 because there were few cases at younger ages. In all, 18 10-year overlapping birth-cohorts, centred between 1884 and 1969, were constructed. The hierarchical age-period-cohort (APC) modelling approach proposed by Clayton and Schifflers16,17 was used. An interaction was systematically detected between the variable site of melanoma and each of the three time factors, so APC modelling was conducted separately for each site and sex. The significant interaction terms meant that different age, period and cohort effects between sites was likely. The difference in deviances and degrees of freedom between two nested models is asymptotically
2 distributed and provides a test of the goodness of fit between models. The non-linearity in the period and cohort effects (adjusted for cohort and period, respectively) was tested by comparing the saturated model containing the three time variables with, respectively, an age-cohort and age-period model. The annual percentage change was calculated from the overall linear trend (drift16).
When cohort effects are present and changes in the age-specific rates due to influences occurring in successive time periods can be regarded as small, the relationship between age and risk of melanoma can be examined by comparing the individual cohort curves. The age-specific incidence and mortality rates were plotted by site and sex against the median year of birth to identify potential cohort effects. An increase or decrease was only reported when rates between two adjacent birth-cohorts, compared at various ages, differed systematically.
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Results |
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For women, a cohort effect in incidence for facial melanomas appeared to be present only for generations born early this century, as for men; this was not mirrored in trends for mortality. The trends by median year of birth fluctuated substantially for the scalp and neck. However, neither incidence nor mortality data clearly indicated a cohort effect. The incidence patterns for the trunk and the upper and lower limbs were somewhat less consistent than for men and suggested that the increases between successive generations could have started earlier on the limbs than the trunk. Signs of a levelling off were clearer for the limbs than the trunk. Systematic changes in the age-specific mortality rates for the trunk and the limbs were rare between female cohorts.
Except for the scalp and neck in females, age alone was insufficient to describe the trends for incidence (data from model, not shown). That is, the addition of a linear trend (the drift parameter) improved significantly the fit of all other models. Significant influences of calendar time and period existed but, in many instances, could not be considered linear. Non-linear period and cohort effects were detected for all sites together in both sexes, as well as for the scalp and neck, the trunk and the upper limbs in men, and the limb sites in women. No departure from linearity was found for the head sites for women. Of note, the risk of facial melanoma increased exponentially with age for both genders.
Age alone adequately explained the mortality trends for the face and the scalp and neck in males and females, as well as for the trunk in women. Whereas significant departure from linearity occurred occasionally for the cohort trends for mortality, no model indicated a significant non-linearity in period effect, regardless of body site.
The incidence of melanoma was estimated to increase at a rate of 6.7% a year in males and this did not differ significantly between sites, ranging from 5.9% for the lower limbs to 7.3% for the upper limbs (Table 3). The annual percentage change was smaller for mortality, at 2.8%, and a significant increase only existed for the trunk and the limbs, particularly the upper limbs. However, the rate of increase may be slightly underestimated as the greatest annual change occurred for melanoma not otherwise specified (NOS). The magnitude of the trends was considerably less for women, especially for incidence, and indicated a greater divergence in trends between anatomical sites than for men. A significant increase over time in both incidence and mortality only occurred for the limbs. No linear trend in incidence or mortality was found for the scalp and neck in women and the face showed a modest increase confined to incidence.
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Discussion |
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Time trend evaluations are by nature subject to factors affecting the incidence or mortality (particularly the former) which are likely to vary with time. Changes in histopathological criteria or in classification of melanoma have been too small to explain the steady rise in incidence over the past decades. A decline in the degree of ascertainment of melanoma with time has probably occurred in many cancer registries relying on voluntary reporting as the diagnosis and treatment of melanoma has increasingly been provided solely on an outpatient basis, often using private pathology services whose records may be less accessible. These influences also exist in New Zealand and some underreporting is known to have occurred around 1985, when a few pathologists withdrew their support for the Cancer Registry.18 This can explain the decline observed in incidence rates around 1985 (Figure 1). The rise in about 19881989 concurred with the conduct of a study collating all melanoma records from private and public sources in four regions of New Zealand19 and this might have temporarily boosted the number of new registrations forwarded to the Cancer Registry.
Variation in completeness of registration generally affects patients of all ages and can spuriously lead to accentuated period-based changes in incidence. This would support the detection of non-linear period effects confined to incidence. However, this is unlikely to explain the diverging trends in various age groups for both incidence and mortality and the different pattern of trends between anatomical sites. The presence of strong generation effects, particularly pronounced for sites likely to be intermittently sun-exposed, suggests that other factors have played a predominant role in these trends.
Three time effects are implicitly involved in any trend analysis: age, year of diagnosis or death (period) and year of birth (cohort). Because these parameters are linearly dependent, their effects are not uniquely estimable unless specifying additional constraints on the model parameters. When not arbitrary,20 constraints generally require or assume a sound a priori biological or epidemiological knowledge of the disease under study, which is not yet the case for melanoma. They tend to lack of robustness,16,17,21,22 increasing thereby the risk of mis- or over-interpretation of the results. One approach to the non-identifiability problem is to focus on estimable functions of the parameters and separate each time effect into a linear trend (overall slope) and a non-linear trend (curvature). While the curvature components of the trend are uniquely estimable,21,22 the slopes are individually indeterminate. However, the sum of the period and cohort slopes (drift) can be assessed16 and provides a useful measure of the overall linear trend.
If the upsurge in melanoma has predominantly been caused by societal changes in dressing patterns and outdoor leisure activities, the impact of recreational sun exposure on the trends might be best assessed by examination of site-specific trends. The relatively simultaneous generation effects for the trunk and the limb sites supports effects related to increased sun exposure from changes in recreational habits and fashion, which gradually emerged from the late 19th century, following improved economic conditions and shortened working hours. Cohort-driven trends were the least marked for the scalp and neck, areas mostly sun-protected, particularly in women, and thus unlikely to be considerably altered by changes in sun exposure patterns. These results were largely corroborated by the estimated site-specific annual percentage changes which were greatest for the trunk and the upper limb region, and negligible for the scalp and neck in women. However, a distinctive pattern between sites most and least likely to be intermittently sun-exposed was less clear when based on the rate of annual increase. The smallest rate of change for the lower limbs in males agreed with reports from the UK and North America but remained unexplained.79,12
Mortality is less vulnerable to diagnostic practices and changes in degree of ascertainment and, in the absence of major therapeutic progress, should be considered more reliable than incidence. A reduction in risk of melanoma would be expected to curb incidence and death rates for the same cohorts. Since the levelling off occurred approximately 25 years earlier for mortality, some melanomas diagnosed during this period may have had a better prognosis than those recorded for older generations or effective treatment may have been more uniformly available. However, a shift towards thinner diagnosed lesions, due to increased and earlier detection, is the most plausible explanation for the discrepancy between incidence and mortality. This would have begun with cohorts of males born from about 1924 and generations of women born since about 1929 (Tables 1 and 2). Although patchy, data on tumour thickness in New Zealand suggest a steep increase in incidence of thin lesions (<0.76 mm thick) over time.23 However, despite a decrease in their proportional distribution, rates of deep melanoma have not concurrently fallen.
Maori have a comparatively low incidence14 and different site distribution24 of the disease. Despite an active search for information from past hospital admissions by the Cancer Registry, the proportion of cases without an ethnic specification has so far remained too considerable to identify reliably non-Maori cases notified after the change in registration practices of July 1994. Maori represent a growing fraction of the population, particularly in younger age groups, and their future inclusion could distort the trends in recent generations by underestimating the rates in younger age groups.
The incidence and mortality trends were of smaller magnitude than previously estimated25 and the predicted stabilization of the death rates for melanoma in New Zealand2 has finally occurred. A similar, favourable trend has only been reported for Australians.1 Programmes to improve early detection and ultimately reverse the mortality trends have long been implemented in Australasia, but their contribution to the current plateau appears likely to be modest since the observed birth-cohort changes clearly predate any educational efforts.26 Although the recent favourable incidence trend seems to be predominantly due to an attenuated increase in risk among younger birth-cohorts, the extent to which the deceleration in rate of increase has been accentuated by recent underreporting is unknown. The levelling off observed among those born from about 1949 may reflect a changing pattern in sun exposure for these younger generations, although no data from which trends in sun exposure by generation could be derived are yet available to substantiate this assumption. If the current trend persists, and assuming that other relevant factors associated with increased risk remain constant, incidence should reach a plateau with the advent of the new millennium.
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Acknowledgments |
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Notes |
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References |
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