Cutaneous malignant melanoma in New Zealand: trends by anatomical site, 1969–1993

Jean-Luc Bulliarda,b and Brian Coxa

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


    Abstract
 Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Background Site-specific trend analysis is probably the most effective method available for assessing how the long-term trend in melanoma rates relates to changes in sun exposure and behaviour. New Zealand has very high incidence of and mortality from melanoma and the fraction of melanoma cases and deaths with a site specified has been comparatively high.

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 : 6.3–7.1%) in men and 3.1% (95% CI : 2.3–3.7%) 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 (2–3% 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


    Introduction
 Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Cutaneous malignant melanoma (melanoma) has been rising considerably in incidence and mortality among fair-skinned populations for several decades, with a sharper increase for incidence than mortality. In the high incidence regions of Australia and New Zealand, a plateau in the death rates from melanoma has been observed since the 1980s for women, and is anticipated in the short term for men.1,2 Signs of a future decrease in death rates are less clear in European community countries3,4 but there are indications of a reversal in the mortality trends in the US for the next few decades.5,6 A stabilization or downturn in incidence rates has recently been predicted in a few countries where the risk of developing melanoma appears to be attenuated for those born from about 1950.68

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.


    Materials and Methods
 Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 
The annual number of non-Maori registrations of, and deaths from, melanoma between 1969 and 1993 and the corresponding population estimates were derived from publications of the New Zealand Health Information Service (NZHIS), for each sex and 5-year age group. Cancer notification became mandatory in New Zealand from July 1994. Melanomas diagnosed in 1994 were not used because the mid-1994 change in cancer notification led to a greater proportion of melanoma registrations based on pathology reports with no ethnicity recorded and no subsequent admission to hospital (J Fraser, NZHIS, personal communication).

Data were aggregated in five quinquennial time periods (1969–1973, 1974–1978, 1979–1983, 1984–1988, 1989–1993). 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 {chi}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.


    Results
 Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 
This study included 15 167 invasive cases and 3053 certified deaths from melanoma in the non-Maori population of New Zealand. The site of origin was unspecified in 7.5% and 3.8% of male and female registrations, respectively, and in 17.2% (men) and 14.2% (women) of death notifications. Between 1969 and 1993, the annual age-standardized incidence rates increased from approximately 7 and 12 cases per 100 000 person-years for men and women, respectively, to about 26/100 000 in both sexes (Figure 1Go). The historically higher incidence rates in females seemed to disappear in the early 1990s. The pattern of yearly fluctuations was similar for each gender and when random variations were removed, the trough in the mid-1980s and the relative peak in rates in about 1988–1989 persisted (data not shown). In contrast, increases in annual death rates have been modest, particularly among women whose risk of dying from melanoma has plateaued since the mid-1980s to about 3.2/100 000. No clear increase in mortality was observed in men from 1990 with annual death rates of approximately 5.5/100 000.



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Figure 1 Age-standardized incidence (with 95% CI) and mortality rates of melanoma of all sites combined by sex and calendar year, 1969–1993

 
Incidence trends differed between cutaneous sites (Figure 2Go). The greatest absolute increase in rates occurred for the trunk in men and the lower limbs in women with respective incidence levels of about 8 and 12/100 000 in recent years. Estimates of the relative annual percentage change by body site, based on the APC models, are presented later (Table 3Go). The upward trend was the least pronounced, in each sex, for the head sites. In particular, rates for melanoma of the scalp and neck in females were similar at both ends of the 25-year period (0.6/100 000). The peak in incidence rates in 1988–1989 was present at most sites, after allowance for random fluctuations. Increases in site-specific rates over time were less marked for mortality but were overall consistent with the pattern for incidence (data not shown).




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Figure 2 Age-standardized incidence rates of melanoma by sex and anatomical site, 1969–1993, A males, B females, 3-year moving average

 

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Table 3 Estimated annual percentage change in melanoma incidence and mortality in New Zealand by sex and anatomical site, 1969–1993
 
As age-standardized rates can conceal diverging trends across age groups, age-specific rates were analysed by birth-cohort. Trends in incidence and mortality rates of melanoma between successive generations are summarized by site and sex in Tables 1 and 2GoGo. Only systematic changes in risk between successive generations, comparable in at least two different age groups, are represented (respectively by an ascending and descending arrow) so that the synoptic tables show the trends for the 16 central cohorts identified by median year of births from 1889 to 1964. For instance, the increase reported for the female cohort born about 1929 indicates that their rates at age 45–49, 50–54, 55–59 and 60–64 were greater than those among women born about 1924.


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Table 1 Summary of birth-cohort trends for melanoma between successive generations of non-Maori New Zealand men by anatomical site
 

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Table 2 Summary of birth-cohort trends for melanoma between successive generations of non-Maori New Zealand men by anatomical site
 
The risk of developing melanoma increased steadily for successive generations of men born from about 1904 to 1924, and again for cohorts centred about 1934 and 1944 (Table 1Go and Figure 3Go). A marked increase in risk of dying from melanoma was present for men born about 1899, 1909 and 1919. Women born between 1914 and 1939, in particular, experienced increased rates of melanoma (Table 2Go and Figure 3Go). As for men, mortality increases between birth-cohorts were less pronounced than for incidence, and ceased about 25 years before those observed for incidence. Incidence rates have stabilized among post World War II generations of males and females and signs of a possible reduction in melanoma risk were observed.



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Figure 3 Age-specific incidence rates of melanoma of all sites combined by birth-cohort of A males, B females

 
For males, the incidence pattern for the trunk and the limbs generally corresponded to that for all sites combined. A deceleration in the rate of increase appeared to have occurred at about the same time for these three sites in men born about 1949. In contrast, increases were less obvious for head sites and essentially noted in those born during the first decade of the 20th century. Because of the large fluctuation in age- and site-specific death rates, caution is required when interpreting site- and sex-specific trends for mortality. Three features were nevertheless observed for males: (1) the face was the site with the least indication of a cohort effect and most suggestive of a decline in age-specific rates in younger generations, (2) birth-cohort trends were discordant between the face and the scalp and neck (unlike for incidence), (3) increases between generations were the most marked for the trunk where death rates rose substantially among men born from about 1904 to 1914.

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 3Go). 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.


    Discussion
 Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 
The annual increase in incidence of melanoma among non-Maori was significantly greater among men (6.7%) than women (2.8%) in New Zealand, and this was so for each anatomical site. The rate of increase slowed substantially in recent years and data indicated that no further increase in lifetime risk has occurred among generations of males and females born after World War II. The rise in mortality level was modest, particularly in females, and rates have stabilized first in women and recently in men. The levelling off in risk between successive generations was apparent about 25 years earlier for mortality than for incidence.

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 1Go). The rise in about 1988–1989 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.7–9,12

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 2GoGo). 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.


    Acknowledgments
 
This research was conducted during the tenure by J-LB of a Training Fellowship of the Health Research Council of New Zealand. Dr Cox received support from the Cancer Bequest Funds of the University of Otago. Incidence and mortality records were kindly provided by the New Zealand Health Information Service, Ministry of Health.


    Notes
 
b Current address: Unité d'épidémiologie du cancer, Institut universitaire de médecine sociale et préventive, rue du Bugnon 17, 1005 Lausanne, Switzerland. Back


    References
 Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 
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