annoncannoncAnnals of Oncology1569-80410923-7534Oxford University Press10.1093/annonc/mdm087original articlesepidemiologyUp-to-date survival estimates and historical trends of cutaneous malignant melanoma in the south-east of The Netherlandsde VriesE12*HoutermanS2Janssen-HeijnenMLG2NijstenT3van de SchansSAM2EggermontAMM4CoeberghJWW121Department of Public Health, Erasmus MC University Medical Centre Rotterdam, Rotterdam2Eindhoven Cancer Registry, Comprehensive Cancer Centre South, Eindhoven3Department of Dermatology, Erasmus MC University Medical Centre Rotterdam, Rotterdam4Department of Surgical Oncology, Erasmus MC University Medical Centre Rotterdam, Rotterdam, The Netherlands*Correspondence to: Dr E. de Vries, Department of Public Health, Erasmus MC University Medical Centre Rotterdam, PO Box 2040, 3000 CA Rotterdam, The Netherlands. Tel: +31-10-4087730; Fax: +31-10-4638475; E-mail: e.devries@erasmusmc.nl62007134200718611101116158200623120071222007© 2007 European Society for Medical Oncology2007Background: We present survival outcomes of patients registered in the Dutch population-based Eindhoven Cancer Registry (ECR).Patients and methods: Data on patients diagnosed with a melanoma between 1980 and 2002 were obtained from the ECR. Data on vital status up to 1 January 2005 were obtained, up-to-date survival rates were calculated using period analysis. Multivariate analyses were carried out using Cox proportional hazards model.Results: Ten-year crude survival rates were 82% for women and 60% for men (P < 0.05). Thin melanomas (Breslow thickness ≤ 2.0 mm) had 5-year crude survival rates >74%, for melanomas >4.0 mm these rates were <65% (P < 0.05). In the early 1980s, 5-year relative survival rates were 84% and 62% for young (<60 years) women and men, and 66% and 69%, respectively, for the elderly (aged 60+). In the period 2000–2002, these rates had improved to >90% for females and to >72% for males. Multivariate analyses showed increased hazard ratios with increasing age and Breslow thickness, being male, having a melanoma on the trunk or unknown sites and having a nodular melanoma.Conclusions: Despite the absence of improvements in treatment options for melanoma, survival improved significantly, except for elderly males.crude survivalcutaneous malignant melanomaperiod analysispopulation-basedrelative survivalintroductionIncidence and survival rates of cutaneous malignant melanoma (melanoma) have been increasing markedly over the past decades in Caucasian populations [1–3]. There is, however, a shortage of up-to-date population-based survival statistics of melanoma patients. Most available survival estimates are for patients diagnosed up to 1996 [1–6]; very few recent population-based estimates are available [7].Clinicians and policy makers should use the most recent available information about survival of newly diagnosed cancer patients; however, almost all available survival estimates are based on patients diagnosed up to 1996. A new method of survival analysis, the so-called period analysis [8], results in more up-to-date long-term survival rates than the traditional methods for estimating survival rates [9–11]. This is especially important when there have been recent improvements in survival, as is the case for melanoma [12].In this study, we evaluated the trends in incidence and survival of cutaneous malignant melanoma using information from the Eindhoven Cancer Registry (ECR). In order to provide up-to-date survival statistics, we estimated relative and crude survival rates of patients diagnosed with cutaneous melanoma by means of period analysis, stratifying or correcting for age, Breslow thickness, site and histogenetic subtype. As there are gender differences in both incidence and survival statistics, all analyses were stratified by sex. Multivariate analyses were carried out to simultaneously control for all these factors and investigate their effects on survival.patients and methodsThe ECR collects data on all patients with newly diagnosed cancer in the southeastern part of The Netherlands. The registry serves a population of 2.4 million inhabitants. The area offers good access to specialised medical care in 10 general hospitals and two large radiotherapy institutes. In the last 25 years, the number of dermatologists in the region increased from ∼30–45. Until 1988, the Registry only collected data on patients from the eastern part of the region, after which another part (the west) was also included. Data on vital status, available until 1 January 2005, was obtained from the hospital records and the death registry of the Central Bureau for Genealogy (that registers all deceased in The Netherlands via the municipal civil registries). Incidence rates were age standardised using the European standard population, resulting in European standardised sates.Distribution of melanoma cases diagnosed in the period 1980–2002 by sex, age, body site and histogenetic type were calculated, excluding noncutaneous sites. Trends in incidence were estimated by calculating the estimated annual percentage change (EAPC). EAPC's were calculated by fitting a regression line to the natural logarithm of the rates (y) using calendar year (x) as regressor variable, i.e. y = mx + b; the EAPC = 100 (em − 1). One EAPC value was calculated for the whole period 1980–2002 because visual inspection of trends in incidence rates in this period showed no clear changes in the trends, making join point analyses unnecessary.Survival times were calculated from the date of diagnosis of primary melanoma until the date of death and considered censored for patients who were alive at their last date of follow-up. In addition to crude survival rates, relative survival rates were calculated. Relative survival is an estimation of disease-specific survival, as it is corrected for the background mortality in the general population within the same age- and sex groups. As different (sub)types of cancer often occur in patient groups with different age structures, comparisons between patient groups, registries or countries, should use relative rather than crude survival estimates. The relative survival is calculated as the crude survival rate among cancer patients divided by the expected survival rate from the general population with the same sex and age structure [14]. Standard errors were calculated according to Greenwood's method [15].In order to provide up-to-date estimates of long-term relative survival for a recent time period (1992–2002), period analysis was used. This means that all observations included in the analyses are left-truncated at the beginning of the period of interest in addition to being right censored at its end. The method of period analysis is described in detail elsewhere [8, 16, 17]. Relative survival estimates for patients diagnosed in earlier time periods were made using traditional cohort-based analysis. Relative survival rates were calculated with the SAS computer package (SAS Institute Inc., Cary, NC 1999), using a publicly available macro[18].We analysed relative survival by the known prognostic factors that were available from the cancer registry: age at diagnosis, sex, body site, histogenetic subtype and Breslow thickness of the melanomas. We subdivided the patients into young (<60 years) and elderly (60 years and older) melanoma patients and carried out all analyses separately for men and women. Body site was subdivided into head and neck, arms, trunk, legs, other and unknown body sites. Histogenetic subtype was divided into superficial spreading melanomas (SSM), nodular melanomas (NM), lentigo maligna melanomas and other melanomas, which included all other types of melanomas and melanomas of which histogenetic subtype was unknown. We made a subdivision into melanomas with a Breslow thickness thinner than 1.0 mm, between 1.01 and 2.0 mm, 2.01–4.0 mm and >4.0 mm. Eleven per cent of male and 7% of female melanoma patients had an unknown Breslow thickness.Multivariate analyses were carried out using the Cox proportional hazards model, including the variables year of diagnosis, age and Breslow thickness as continuous variables, sex, body site and histogenetic subtype in the same categories as used for the stratified univariate analyses described above.resultsA total of 1644 male and 2372 female melanoma patients were included in the analyses (Table 1). Incidence of melanoma has been increasing rapidly. Current and past incidence rates per 100 000 person-years by sex, age, body site, histogenetic subtype and Breslow thickness of the melanomas are given in Table 1. Overall, increases in incidence during the period 1980–2002 were 4.8% for men and 4.3% for women. Strong increases (>4.5%) were observed for melanomas on the trunk (both sexes), melanomas on the arms (women), SSM and NM (both sexes), melanomas with a thickness of ≤1.0 mm (both sexes) and for melanomas with a thickness >1.0 mm (men).Table 1.Age-standardised incidence rates (European standard population) per 100 000 person-years of melanoma patients diagnosed between 1980 and 2002 in the Eindhoven Cancer Registry regionEuropean standardised rateTotal (N)EAPC (%)P value1980–19841985–19891990–19941995–19992000–2002Males    Total5.56.48.310.812.216444.8<0.001Age (years)    <604.54.75.88.18.310643.80.16    60+11.315.621.225.032.95805.4<0.001Body site    Trunk1.82.63.44.95.27036.7<0.001    Head and neck1.11.21.42.02.62984.1<0.001    Arm1.30.91.41.42.02603.70.01    Leg0.81.21.41.91.82774.3<0.001    X0.50.50.60.70.71062.40.02Histogenetic subtype    SSM0.71.73.04.45.06098.4<0.001    NM0.11.01.32.02.226812.5<0.001    LMM0.10.10.20.10.4322.80.21    Other4.73.63.84.24.67350.30.713Breslow thickness (in mm)    ≤1.01.31.52.34.04.35307.9<0.001    1.01–2.01.31.21.52.53.13644.9<0.001    2.01–4.01.41.42.42.02.23594.50.012    >4.00.81.20.91.41.62094.50.009    X0.71.11.21.01.11822.00.121Females    Total7.89.411.314.915.023724.3<0.001Age (years)    <607.08.39.813.113.016783.50.09    60+12,015,019,024,225,86944.10.01Body site    Trunk0.91.73.04.33.958510.5<0.001    Head and neck1.50.81.21.61.32621.80.30    Arm1.71.92.33.23.25025.4<0.001    Leg0.81.21.41.91.89502.8<0.001    X0.20.30.40.50.4730.60.77Histogenetic subtype    SSM0.63.25.36.88.310229.9<0.001    NM0.60.91.51.41.82677.0<0.001    LMM0.10.10.20.20.4482.80.24    Other6.55.24.36.44.51035−0.40.68Breslow thickness (in mm)    ≤1.02.13.24.97.48.210647.9<0.001    1.01–2.02.22.82.93.23.35673.60.004    2.01–4.01.61.92.02.32.04011.70.084    >4.01.00.90.71.01.01840.30.821    X0.90.70.90.90.51560.00.999EAPC, estimated annual percentage change; SSM, superficial spreading melanoma; NM, nodular melanoma; LMM, lentigo maligna melanoma; Other, other and unspecified melanomas; X, unknown.Median age at diagnosis was higher for men (53 years) than women (49 years). Sixty-nine per cent of women and 54% of men were diagnosed with a relatively thin melanoma (Breslow thickness ≤ 2.0 mm). Among females, but not males, a strong shift to earlier diagnosis seems to have occurred; increases are only seen in the categories with thinner Breslow thickness, whereas no significant increases were observed for the categories with a Breslow thickness ≥2.0 mm (Table 1).Ten-year crude survival rates were 82% [95% confidence interval (CI) 78% to 86%] for females and 60% (54% to 66%) for males. Twenty-year relative survival rates were 12%–13% units higher than the crude survival rates: 93% (89% to 98%) for females and 72% (65% to 79%) for males (Figure 1).Figure 1.Relative and crude survival rates of melanoma cases diagnosed in the Eindhoven Cancer Registry region (period analysis 2000–2002).Ten-year crude and relative survival of head and neck melanomas were lower than that of other body sites among males, but only reached significance for crude survival, after taking the background mortality into account (relative survival) this difference was not longer significant (Table 2). Five-year survival rates of melanomas in the head and neck area and on the trunk were significantly higher for females than males; among males NMs exhibited a significantly worse survival than the other histogenetic subtypes.Table 2.Sex-specific 5- and 10-year crude and relative survival rates of melanoma patients diagnosed in the Eindhoven Cancer Registry region (period analysis 2000–2002)5-year relative survival rates10-year crude survival ratesCrude(95% CI)Relative(95% CI)Crude(95% CI)Relative(95% CI)Males    Overall69(64–74)76(71–81)60(54–66)72(65–79)Age    <60 (ref)76(71–81)78(73–84)71(65–77)74(68–81)    60+56a(47–65)72a(61–83)36a(24–48)64(42–86)Site    Arm (ref)81(70–92)86(75–97)70(55–85)78(61–95)    Trunk73(66–80)78(71–85)68(61–75)79(70–88)    Head and neck55a(43–67)66(52–81)40a(26–54)Na    Leg79(69–89)86(75–97)70(56–84)81(65–97)Histogenetic subtype    SSM (ref)80(74–86)86(79–93)75(67–83)86(77–95)    NM55a(43–67)60a(47–73)47a(32–62)41a(28–54)    LMMNaNaNaNa    Other66a(59–73)73(65–81)58a(49–67)70(59–81)Breslow thickness (in mm)    ≤1.0 (ref)89(85–93)98(91–105)87(80–94)101(93–109)    1.01–2.074a(63–85)80(68–92)62a(48–76)71a(55–87)    2.01–4.057a(41–73)63a(46–80)Na–Na–    >4.0NaNaNa–Na–Females    Overall89(86–92)94(91–97)82(78–86)93(89–98)Age    <60 (ref)94(91–97)95(93–98)91(88–94)93(90–96)    60+78a(71–85)93(85–101)59a(47–71)94(75–113)Site    Arm (ref)89(83–95)94(88–100)84(76–92)96(87–105)    Trunk89(84–94)91(86–96)86(80–92)91(85–98)    Head and neck88(79–97)102(92–112)62(46–78)89(66–113)    Leg92(88–96)96(92–100)86(80–92)95(88–102)Histogenetic subtype    SSM (ref)93(90–96)97(94–100)86(80–92)96(90–102)    NM88(80–96)97(88–106)74(59–89)89(72–106)    LMMNaNaNaNa    Other85a(80–90)89a(84–94)80(74–86)91(85–98)Breslow thickness (in mm)    ≤1.0 (ref)96(93–99)100(97–103)93(89–97)102(98–106)    1.01–2.084a(75–93)88(79–97)81(71–91)90(79–101)    2.01–4.081(68–94)90(75–105)Na–Na–    >4.065a(48–82)70a(51–89)Na–Na–aSignificantly different (P < 0.05) from (ref) category.Na, not sufficient cases left to calculate survival rates (i.e. <10 cases surviving).CI, confidence interval; SSM, superficial spreading melanoma; NM, nodular melanoma; LMM, lentigo maligna melanoma; other, other and unspecified melanomas.Trends in 5- and 10-year relative survival over time are depicted in Figure 2. Since the early 1980s, survival of melanoma has improved substantially, except for elderly males, whose survival rates remained stable. In the early 1980s, 5-year relative survival was 84% (95% CI 77% to 91%) and 62% (51% to 73%) for young (<60 years of age) females and males, and 66% (46% to 86%) and 69% (42% to 96%) for elderly (aged 60 and over) females and males, respectively. This improved to >90% for females of all ages [young females 95% (92% to 98%) and elderly females 93% (85% to 101%)] in the period 2000–2002. Five-year relative survival rates in 2000–2002 for young and elderly males were 78% (73% to 83%) and 72% (61% to 83%), respectively. These increases were statistically significant for females only and borderline significant for young males. Ten-year relative survival rates also increased substantially for females, reaching significance for the age group <60 years (Figure 2).Figure 2.Trends in 5- and 10-year relative survival 1980–2002, Eindhoven Cancer Registry region, by sex and age group, with 95% confidence intervals (RS, relative survival. **The number of men surviving >5 years was too small to calculate 10-year relative survival rates in the period 1980–1989).The multivariate analyses showed that, taking into account tumour-specific characteristics such as body site, histogenetic subtype and Breslow thickness, the survival of melanoma patients has improved over the years (Table 3). For every more recent year of diagnosis, the hazard ratio of dying decreased with 4% compared with the previous year. These analyses also show that being male or having a melanoma on the trunk, having a NM or a melanoma with higher Breslow thickness significantly increased the hazard of death (Table 3).Table 3.Results of the multivariate Cox regression analyses for melanoma patients diagnosed between 1993 and 2002 in the population-based Eindhoven Cancer RegistryVariableHR(95% CI)Year of diagnosis    Continuous (increasing)0.96(0.92–1.00)Age    Continuous1.05(1.04–1.05)Sex    Female (ref)1.00    Male2.00(1.60–2.49)Site    Arms (ref)1.00    Trunk1.52(1.10–2.10)    Head and neck1.34(0.94–1.91)    Legs1.14(0.82–1.60)Histogenetic subtype    SSM (ref)1.00    NM2.01(1.51–2.68)    LMM0.78(0.33–1.81)    Other1.65(1.28–2.13)Breslow thickness    Continuous1.14(1.11–1.17)HR, hazard ratio; CI, confidence interval; SSM, superficial spreading melanoma; NM, nodular melanoma; LMM, lentigo maligna melanoma.discussionWe reported up-to-date population-based survival rates of melanoma patients diagnosed in the southeastern Netherlands. Despite the absence of major improvements in melanoma treatment [19, 20], survival rates have improved substantially over the past two decades, except for elderly men. It is unclear why elderly men did not benefit from the improvements that were accomplished for the other groups, although it is known that females and younger males are more sensitive for sun-safe messages [21] and therefore, melanomas are probably detected earlier in this group. These improvements in survival rates are surprising as marked increases in incidence were still seen in the melanomas with high Breslow thickness and NM. Earlier detection seemed to have occurred among females, where there were no significant increases in the group of melanomas with a Breslow thickness of ≥4.0 mm, whereas strong increases were observed in this category among males. Contrary to the United States, where Welch et al. [22] observed that the increases in incidence was largely the result of increased diagnostic scrutiny rather than real increases in the disease, the increases in melanoma incidence in the ECR population were not confined to early-stage cancer and mortality did increase [23].Relative survival estimates were always higher than crude survival statistics, due to the fact that the crude survival rates are corrected by the background mortality of the population. This is clearly illustrated in the case of head and neck melanomas, and melanomas occurring in people aged ≥60 years, where we observed differences of >20 per cent units. This phenomenon is caused by the fact that these are populations of elderly patients, in which the background mortality is high, hence, mortality due to melanoma only contributes a small part to the overall mortality.The observed survival rates are higher than most reported by other studies, especially for females [1–4, 24]. This is mostly due to the fact that we used more recent data and a method which produces more up-to-date estimates of survival [8, 16, 17]. Most other studies used traditional methods to calculate melanoma survival rates, resulting in estimates that represent survival rates of previous generations of melanoma patients, rather than the most current estimates. The available, but mostly outdated, population-based data on melanoma survival showed substantial differences in survival between countries [4] with marked improvement of 5-year survival rates over time [1, 3]. The most recently reported European average 5-year relative survival for melanoma patients diagnosed between 1990 and 1994 was 85% for women and 75% for men [4]. Five-year relative survival rates for Australians diagnosed with melanoma between 1992 and 1997 were 90% for males and 94.6% for females [25]. Surveillance, Epidemiology and End Results (SEER) statistics (United States) for whites diagnosed with melanoma between 1996 and 2002 were 90.3% (males) and 93.4% (females) [26]. Most European population-based studies used traditional methods for survival analysis; 5-year crude survival estimates being between 85% and 87% for women and 80% for men [2, 3], the most recent 5-year relative survival rates come from Yorkshire, England, and were 81.5% for women and 70% for men [7]. Five-year crude survival rates in the cohort used by the American Joint Committee on Cancer were only 73% and in the SEER registry 89% [27]. The American Joint Committee on Cancer (AJCC) melanoma staging system was designed to determine criteria to be used in the tumour–node–metastasis classification and stage grouping. The criteria were meant to be ‘relevant to current clinical practice’, ‘regularly incorporated in clinical trials’ and the required data should be ‘sufficiently easy for tumour registrars to identify in medical records to code staging information’ [28]. The staging system was tested in the AJCC cohort which included patients diagnosed as early as 1940 and used cohort analysis to estimate survival rates [24]. Moreover, the AJCC cohort was not population-based but rather influenced by varying referral patterns and clinical trial entry criteria to tertiary medical centers and cooperative groups. These features might have skewed the patients distribution overall compared with the general population [24]. These characteristics of the AJCC cohort and analyses cause the presented survival rates to be largely outdated and not representative of the general population. In this study, we presented population-based data of all patients diagnosed in the ECR region. The survival rates predicted by the AJCC were already proven to underestimate survival in the USA population [27], as they are now proven to do for this Dutch population.Although women had higher incidence rates of melanoma than males, their survival rates were significantly better: ∼20% higher 5- and 10-year relative survival rates than men. This gender difference in survival has been reported previously and is currently not well understood [1–7]. Part of the difference was probably due to the fact that compared with men women were younger at diagnosis and were more often diagnosed with thin melanomas and of the SSM type [29]. However, even melanomas of the same Breslow thickness and histopathological subtype and trunk and head and neck melanomas exhibited better relative survival rates for females than males. The multivariate analysis showed that, after correcting for all these factors, the hazard of death for male melanoma patients was significantly higher than for women. Therefore, besides a younger age, better stage at diagnosis and more favourable histogenetic subtypes, other factors are likely to be responsible for this superior survival of women. This phenomenon deserves further investigation.Most [6, 24, 30], but not all [5], previous studies showed a worse survival for patients with trunk melanomas. In this study, absolute and relative survival rates of patients with trunk melanomas were not significantly worse compared with survival of patients with melanomas on other body sites. However, after taking all available prognostic factors into account simultaneously in the multivariate analyses, trunk melanomas had a significantly increased hazard ratio.NMs had a worse survival rates than SSM among males only, the reason for this remains unclear. It probably has to do with more favourable other tumour characteristics among women. In multivariate analyses, NMs showed an increased hazard ratio. Few other studies reported survival rates by histogenetic subtype, usually being worse for nodular than for SSMs [5, 7].Unfortunately, no information was available on ulceration, which is an important prognostic factor. Should we have been able to include ulceration into the multivariate models, the results would likely have changed towards an important effect of ulceration and a somewhat less strong effect of Breslow thickness alone.In conclusion, survival of melanoma in the south-east of The Netherlands has improved over the past decades, mainly in the 1980s. Especially for women with thin melanomas, the prospects are very good. Secondary prevention activities seem to have been effective for females only. Ways should be found to better reach the elderly males, because in this group many life-years can theoretically be gained by improving early detection.The authors would like to thank the ECR for the data collection and data disposition. 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