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Acta Oncologica, 2010; 49: 665–672
ORIGINAL ARTICLE
Trends in the survival of patients diagnosed with malignant melanoma of the skin in the Nordic countries 1964 – 2003 followed up to the end of 2006
LAUFEY TRYGGVAD Ó TTIR 1,2 , METTE GISLUM 3 , TIMO HAKULINEN 4 , Å SA KLINT 5 , GERDA ENGHOLM 3 , HANS H. STORM 3 & FREDDIE BRAY 6,7
1 Icelandic Cancer Registry, Icelandic Cancer Society, Reykjavik, Iceland, 2 Department of Medicine, University of Iceland, Reykjavik, Iceland, 3 Department of Cancer Prevention and Documentation, Danish Cancer Society, Copenhagen, Denmark, 4 Finnish Cancer Registry, Helsinki, Finland, 5 Swedish Cancer Registry, National Board of Health and Welfare, Stockholm, Sweden, 6 Department of Clinical- and Registry-based Research, Cancer Registry of Norway, Oslo, Norway and 7 Department of Biostatistics, Institute of Basic Medical Sciences, University of Oslo, Norway
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Abstract A previous Nordic study showed a marked and steady increase in the age-adjusted 5-year relative survival of skin melanoma patients diagnosed during the period 1958 through 1987. Males had considerably poorer survival than females. Material and methods . Using the NORDCAN database, we studied relative survival and excess mortality of patients diagnosed with melanoma of the skin in the Nordic countries 1964 – 2003 followed up to the end of 2006. These were contrasted with concomitant trends in incidence and mortality. Results . The overall incidence of melanoma almost quadrupled, but there was considerable variation in the trends in the fi ve countries. Mortality was low but doubled during the study period. Survival ratios increased steadily to between 80% and 90% for patients diagnosed in 1999 – 2003. Swedish patients had consistently higher survival, whereas Danish patients had the highest excess death rates the fi rst three months after diag-nosis up until 1990, but thereafter, rates reached a similar low level to that observed in the other Nordic countries. The survival of Nordic women is still higher than that of men, but the difference has diminished, while the mortality rates among men are becoming increasingly higher relative to those for women among individuals 50 years and older. In younger indi-viduals, mortality rates are similar in the two sexes, and declining. Conclusions. Nordic patient survival following melanoma diagnosis is generally high and has been steadily increasing in the last decades. Differences in incidence between the fi ve countries are more pronounced than the differences in survival. The strong upward trends in incidence and survival may mainly be the result of extensive changes in sunbathing habits or other UV exposure and, more recently, of an increasing awareness by the medical community and the public concerning early detection of melanoma of the skin.
Malignant melanoma of the skin (melanoma) was a rare disease in the Nordic countries 50 years ago, but the incidence has risen dramatically over time, and currently comprises 4% of all cancers in the Nordic countries and almost 2% of all cancer deaths. In 1999 – 2003, an average of 4 500 incident cancers were diagnosed yearly and nearly 1 000 deaths occurred due to melanoma [1]. The main known environmental risk factor is intermittent exposure to ultraviolet (UV) radiation, but the effects of UV radiation are highly dependent on skin type, and to a certain extent on inherited mutations [2,3]. Higher socioeconomic groups have higher incidence and
ISSN 0284-186X print/ISSN 1651-226X online © 2010 Informa UK Ltd. (InfDOI: 10.3109/02841861003702528
Correspondence: Laufey Tryggvad ó ttir, Icelandic Cancer Registry, Icelandic CanFax: � 354 5401910. E-mail: [email protected]
(Received 14 January 2010; accepted 12 February 2010)
higher survival ratios than lower socioeconomic groups [4].
The most important prognostic factors for mela-noma patients are lymph node involvement and/or metastatic spread as well as the thickness of the lesion. Other important factors are gender, presence or absence of ulceration, age at diagnosis, and the anatomical location of the tumour [5]. The most common location among women is at the extremi-ties, a location that is associated with higher survival ratios than the more typical locations among males, i.e. on the trunk, head and neck. Women have generally higher survival than men, but this cannot be explained
orma Healthcare, Taylor & Francis AS)
cer Society, PO Box 5420, IS-125 Reykjavik, Iceland. Tel: � 354 5401900.
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entirely by the higher incidence of extremity location, lower stage at diagnosis or other more favorable primary tumour characteristics as compared with men [6 – 8].
The survival of European melanoma patients is generally high and does not vary greatly. Nordic patients have slightly higher 5-year survival than the European mean, which was 83% in the EURO-CARE-4 study [9]. A previous Nordic study showed a marked and steady improvement in the age-standardised 5-year relative survival of patients diagnosed during the period 1958 through 1987, with little variation between the Nordic countries, especially towards the end of the period [10].The aim of the present study is to describe, compare and interpret the Nordic trends in melanoma with respect to incidence, mortality and relative survival in patients diagnosed between 1964 and 2003, as well as exam-ine excess mortality due to this cancer according to time elapsed from diagnosis.
Material and methods
Melanoma of the skin is here defi ned as ICD-10 code C43. The data source and methods are described in detail in an earlier article in this issue [11]. In brief, the NORDCAN database contains comparable data on cancer incidence and mortality in the Nordic countries; data are delivered by the national cancer registries, with follow-up information on death or emigration for each cancer patient available up to and including 2006. We calculated sex-specifi c 5-year relative survival for each of the diagnostic groups in each country for eight 5-year periods from 1964 – 1968 to 1999 – 2003. For the last 5-year period, the hybrid method was used. Country-specifi c population mor-tality rates were used for calculating the expected survival. Age-standardisation of survival used the weights of the International Cancer Survival Standard (ICSS) cancer patient populations [12]. We present age-standardised (World) incidence and mortality rates, 5-year relative survival, and excess mortality rates for the follow-up periods of within one month, one to three months and two to fi ve years following diagnosis, as well as age-specifi c 5-year relative survival by country, sex and 5-year period.
Results
Incidence and mortality
There was great variation in incidence between the fi ve Nordic countries, especially among females. All countries experienced in the 40-year period an almost fourfold increase, resulting in an age-standardised incidence in the period 1999 – 2003, ranging between 9.0 (per 100 000, Finland) and 14.5 (Norway) among
men, and between 7.8 (Finland) and 19.8 (Iceland) among women. The relative increase was similar among men and women. Until the end of the 1980s, Iceland and Finland had the lowest incidence among both sexes, since then however, rapid increases in rates were observed in Iceland (Figure 1). Norwegian men had the highest incidence rates across the entire period, while Icelandic women surpassed their Nor-wegian counterparts circa 1997 to exhibit the highest ranked incidence. In Norway, incidence has not increased among either sex since 1990.
Mortality was low and more stable over time than incidence. However, there was a doubling of rates during the observation period, with the largest increase in Icelandic and Norwegian men. The mor-tality was highest among Norwegian men during the entire period, whereas Finnish and Icelandic men had the lowest rates. In 2003 mortality rates ranged from 2.0 (Iceland) to 3.9 (Norway) per 100 000 among men and from 1.0 (Finland) to 2.5 (Norway) per 100 000 among women. Even though incidence was similar in men and women throughout the period, all-ages mortality was higher among men and the sex-specifi c differences increased steadily with time.
Survival
The relative survival ratios of Nordic patients diag-nosed with melanoma were high and have been steadily increasing. For the last period of diagnosis (1999 – 2003) the survival ratios ranged between 78% and 93% among men and between 88% and 92% in women (Figure 1 and Table I). Swedish patients have consistently had the highest survival ratios over calendar time, whereas Finnish and Danish patients have had the lowest survival. Due to the small num-bers of Icelandic patients, it was not possible to esti-mate survival ratios until the most recent years, and these are diffi cult to interpret given the underlying random variation. Women had higher age-standardised 5-year relative survival ratios than men, but as the ratios among men increased relatively more, the sex-specifi c differences diminished with time.
In the earlier periods, Denmark had a much higher excess death rate during the fi rst three month after diagnosis, more notable for men than for women, but in the mid-1990s Denmark reached a level simi-lar to the other Nordic countries (Figure 2). Sweden and Iceland had the lowest excess mortality during the fi rst three months. The excess death rates became very similar across countries two to fi ve years after diagnosis. Over the entire study period, a reduction in excess death rates during the fi rst three months was observed in all countries, and a reduction was also apparent, albeit to a lesser extent, in the longer
Nordic survival following malignant melanoma of the skin 667
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Figure 1. Trends in age-standardised (World) incidence and mortality rates per 100 000 and age-standardised (ICSS) 5-year relative survival for malignant melanoma of the skin by sex and country. Nordic cancer survival study 1964 – 2003.
668 L. Tryggvad ó ttir et al.
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N RS (CI) N RS (CI) N RS (CI) N RS (CI) N RS (CI)
Men 1964–1968 445 40 (35–46) 297 40 (34–47) 7 ∗ 453 47 (42–53) 941 58 (54–62)1969–1973 561 50 (45–56) 412 43 (37–50) 7 ∗ 660 54 (49–59) 1254 60 (57–63)1974–1978 852 59 (55–63) 556 58 (53–63) 13 ∗ 920 65 (61–69) 1708 67 (65–70)1979–1983 1050 65 (62–69) 756 68 (63–72) 25 ∗ 1162 68 (65–72) 2161 73 (71–76)1984–1988 1333 69 (65–72) 1086 74 (70–77) 20 ∗ 1478 71 (69–74) 2903 76 (74–78)1989–1993 1667 72 (69–75) 1199 79 (76–82) 29 ∗ 2050 76 (74–78) 3393 84 (82–85)1994–1998 2036 78 (76–81) 1434 77 (74–80) 63 72 (61–85) 2245 78 (76–80) 3804 84 (83–86)1999–2003 2439 80 (78–82) 1701 82 (80–85) 90 93 (89–98) 2359 78 (77–80) 4256 86 (85–88) Women 1964–1968 756 66 (62–71) 369 55 (50–61) 17 ∗ 533 73 (68–78) 1066 76 (73–80)1969–1973 866 69 (66–73) 499 63 (58–69) 17 ∗ 715 73 (69–77) 1528 77 (74–79)1974–1978 1204 75 (72–78) 682 73 (69–77) 30 82 (72–93) 1170 82 (79–85) 1951 81 (79–83)1979–1983 1522 80 (78–83) 936 80 (77–83) 40 82 (72–93) 1466 82 (80–85) 2403 85 (83–86)1984–1988 1810 82 (80–85) 1170 85 (82–87) 40 84 (76–92) 1932 86 (84–88) 3000 88 (86–89)1989–1993 2224 85 (83–87) 1251 83 (81–86) 60 84 (76–92) 2340 89 (88–91) 3523 90 (89–91)1994–1998 2577 88 (86–90) 1406 86 (84–88) 94 91 (85–97) 2471 89 (87–90) 3942 92 (91–93)1999–2003 3013 90 (89–91) 1684 89 (87–90) 161 91 (85–97) 2633 88 (87–90) 4273 92 (91–93)
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Figure 2. Trends in age-standardised (ICSS) excess death rates per 100 person years for malignant melanoma of the skin by sex, country, and time since diagnosis in Nordic cancer survival study 1964 – 2003.
Table I. Trends in survival for malignant melanoma of the skin by sex and country. Number of tumours (N) included and the 5-year age-standardised (ICSS) relative survival in percent with 95% confi dence intervals (RS (CI)). Nordic cancer survival study 1964 – 2003.
Numbers in italics indicate that two or more cells had to be combined to get suffi cient number of patients to calculate survival. ∗ Too few patients to calculate survival, see reference [11].
Nordic survival following malignant melanoma of the skin 669
Men Women
Age 0–49 50–59 60–69 70–79 80–89 90 � 0–49 50–59 60–69 70–79 80–89 90 �
Denmark 1964–1968 48 38 35 37 34 ∗ 73 64 66 64 41 ∗ 1969–1973 50 53 47 53 46 ∗ 78 77 63 54 58 01974–1978 67 50 55 54 63 ∗ 81 77 75 60 70 01979–1983 73 65 64 54 56 0 88 83 80 69 60 291984–1988 76 69 68 60 47 0 88 83 87 72 67 401989–1993 81 74 61 68 59 101 91 90 84 78 60 451994–1998 86 83 77 64 64 0 94 87 88 83 72 681999–2003 87 83 80 68 66 46 93 91 87 89 78 57 Finland 1964–1968 47 39 43 40 0 ∗ 65 71 50 47 0 ∗ 1969–1973 46 52 33 39 43 ∗ 69 68 57 61 48 ∗ 1974–1978 61 65 53 60 31 ∗ 84 80 68 62 34 ∗ 1979–1983 71 75 71 64 30 ∗ 90 80 76 74 54 591984–1988 79 80 66 72 57 75 92 87 82 76 70 01989–1993 82 78 77 78 78 70 91 88 80 75 61 01994–1998 82 80 78 65 64 110 92 88 84 82 68 511999–2003 87 85 81 75 74 62 94 91 89 83 69 104 Iceland 1964–1968 75 75 75 26 ∗ ∗ 81 69 66 40 ∗ ∗ 1969–1973 75 75 75 26 ∗ ∗ 81 69 66 40 ∗ ∗ 1974–1978 56 56 56 ∗ 79 ∗ 101 95 64 57 63 ∗ 1979–1983 56 56 56 ∗ 79 ∗ 101 95 64 57 63 ∗ 1984–1988 74 74 74 45 ∗ ∗ 95 71 81 106 20 ∗ 1989–1993 74 74 74 45 ∗ ∗ 95 71 81 106 20 ∗ 1994–1998 81 81 81 48 29 ∗ 97 86 92 92 70 ∗ 1999–2003 97 97 97 88 69 ∗ 97 86 92 92 70 ∗ Norway 1964–1968 61 40 42 25 59 ∗ 79 74 72 66 58 01969–1973 62 55 49 44 44 0 83 74 71 65 42 ∗ 1974–1978 76 72 68 41 29 0 89 85 80 74 62 431979–1983 73 72 64 56 74 0 91 85 79 72 63 1281984–1988 81 75 70 61 41 158 92 89 85 77 69 761989–1993 84 81 77 63 47 31 94 90 91 83 75 521994–1998 86 77 80 72 51 74 95 92 86 82 76 871999–2003 85 79 78 69 67 81 93 92 86 79 80 95 Sweden 1964–1968 65 58 55 53 42 0 84 76 73 64 77 01969–1973 71 65 60 43 23 0 88 83 72 61 51 881974–1978 78 72 65 48 54 83 87 85 78 73 66 851979–1983 78 75 72 66 62 0 89 86 86 78 68 381984–1988 85 78 74 68 51 120 92 89 89 83 68 371989–1993 88 87 81 81 67 76 96 91 89 86 70 871994–1998 89 88 85 79 61 38 96 94 91 88 75 701999–2003 91 87 86 81 73 37 95 93 91 87 83 64
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term in rates. The excess deaths per 100 person years were consistently higher among men than women,an observation noted soon after diagnosis, and one that was still seen 2-5 years after diagnosis. As shown in Table II the 5-year age-specifi c relative survival was highest in the youngest group and declined with advancing age in all countries throughout the period, but increase was seen in all age-groups over time.
In Figure 3, the incidence and mortality trends (on a logarithmic scale) are shown separately for individuals below age 50 years, and 50 years and older. There have been considerably more pro-nounced changes in the older group with time, where the incidence in males and females has at least qua-drupled and mortality doubled in both sexes. This contrasts with the trends in the younger group; the increase in incidence was threefold in both sexes
Table II. Trends in 5-year age-specifi c relative survival in percent after malignant melanoma of the skin by sex and country. Nordic cancer survival study 1964 – 2003.
Numbers in italics indicate that two or more cells had to be combined to get suffi cient number of patients to calculate survival. ∗ Too few patients to calculate survival, see reference [11].
670 L. Tryggvad ó ttir et al.
Nordic countries, Melanoma of skinASR (World) age (0–49)
Nordic countries, Melanoma of skinASR (World) age (50–85+)
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while the mortality slightly decreased in men and women since circa 1989.Discussion
In this large population-based study we found that the incidence of malignant melanoma in the Nordic countries almost quadrupled and the mortality doubled between 1964 and 2003, and was highest in Norwegian men. Relative survival improved markedly and is currently between 80% and 90%. It has remained consistently higher in women than men over time, although the differences have diminished.
The survival of melanoma patients has also been increasing for several decades in Australia, the US and in a number of European populations, a fi nding which has been mainly attributed to the raised pub-lic awareness due to educational programmes focus-ing not only on primary prevention, but also on the importance of skin examination in order to detect potential changes in moles (melanocytic naevi) and bringing them to the attention of doctors or derma-tologists. This has led to increased diagnostic activity and earlier diagnosis in those countries [13,14].
Advances in the treatment of malignant cutane-ous melanoma are likely to explain a much smaller part of the worldwide increased survival, as no dra-matic changes have occurred. The standard treat-ment consists of a wide local excision, with or without sentinel lymph node biopsy, based on thickness of the lesion [15]. However, a small frac-tion of the increase may be attributed to advances
in treatment, such as sentinel node biopsy and adju-vant treatment [16] and some of the increase may be due to lead time bias occurring when an earlier diag-nosis does not affect the timing of death, and length bias which occurs because of an increasing inclusion of indolent cancers that would never have been life threatening [17].
Swedish patients had consistently the highest survival ratios relative to the other Nordic countries during the entire study period. It is likely that an important role is played by the establishment of the Swedish Mela-noma Study Group in 1976, which had the objective of creating national guidelines for melanoma diagno-sis, treatment and follow-up [18] and also by the establishment of public educational programmes in Sweden [19]. However, the reasons behind the sur-vival also being highest in Sweden before the onset of those programmes are not obvious. The Swedish Can-cer Registry does not register death certifi cate-initi-ated cases, but it is likely that this could only explain a small amount of the survival differences observed between Sweden and the other Nordic countries, since skin melanoma is rarely seen to be death-certif-icate initiated in the other Nordic countries.
The excess mortality in Denmark during the fi rst months after diagnosis was well above that of the other countries, most notably among males, until around year 1990; thereafter excess death rates had reached a level similar to the other countries. The excess mortality has declined considerably in all countries during the past 40 years, especially within the fi rst three months following diagnosis.
Figure 3. Trends in Nordic age-standardised (World) incidence and mortality rates per 100 000 by sex and by ages below and above 50 years. Nordic cancer survival study 1964 – 2003.
Nordic survival following malignant melanoma of the skin 671
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The most dramatic changes in incidence were observed in Iceland, a geographical area that has a low background UV radiation due to the northern latitude and frequent cloud cover. The increase is most notable from the late-1980s, and among women. This may partly result from a very high prevalence of sun bed use in Iceland, as well as a large increase in travel abroad to southern areas during the past four decades and partly because of increased diagnos-tic activity due to a nationwide cancer prevention programme which came into action in 1990 [20].
There were only minor differences between the sexes in the overall incidence in the Nordic coun-tries throughout the period, but the mortality was higher among men and the sex-specifi c differences increased steadily with time. However, this was only seen in diagnoses at ages 50 and older, and the increase in mortality was also confi ned to this group. In the younger age groups there has been a slight decrease in mortality among both sexes since circa 1989. This favorable development among the young is noteworthy, especially since a relatively high pro-portion of deaths among melanoma patients occurs under 50 years of age because of a relatively low age at diagnosis. Among Nordic persons who died from melanoma in 1999 – 2003, about 14% were younger than 50 years (compared to 5% under 50 years when considering deaths from all types of cancer taken together [1]).
Contrasting mortality trends in younger and older age groups have previously been reported from other populations [21,22] and have been attributed to stronger infl uence on the younger generations of the educational programmes aiming at increased awareness of the precursors of malignant melanoma [21,23, 24].
Not enough is known about similar educational programmes in the Nordic countries except for Sweden [19]. However, it is likely that the interna-tionally raised knowledge has also led to increased awareness among health professionals and the public in all the Nordic countries, but probably with con-siderable variations between countries in extent and timing.
A limitation of this study is the lack of informa-tion on stage and thickness of the tumours, as well as the body location. However, we found that the relative proportion of superfi cial spreading melano-mas has been increasing during the study period, although to a different extent within countries (data not shown), which could indicate that the incidence increase may be associated with a relative increase of thin melanomas. The median melanoma thickness decreased signifi cantly in Sweden between 1976 and 1987 [19], and in 1990 – 1999 [18]. It has been shown that a public education campaign in Scotland in 1985 was followed by a reduction in the absolute
number of thick tumours as well as melanoma-related mortality [25].
Increased awareness among both the public and health professionals is likely to be strongly associated with the survival improvements during the past 20 – 30 years in the Nordic countries, but information is lack-ing. It is of great importance to study in detail the current status, and if possible to what extent the awareness has changed with time, and compare with the detailed sex- and age-specifi c changes with time in relative survival, incidence and mortality, accord-ing to thickness and body location of the tumours.
It can be concluded that Nordic patient survival following melanoma diagnosis is generally high and has been steadily increasing in the last decades. Dif-ferences in incidence between the fi ve countries are more pronounced than the differences in survival. Improved understanding is needed of the forces behind those changes and of the status of the public knowledge about naevi, skin cancer and melanoma in the Nordic countries, in order to be better able to prevent further deaths from malignant melanoma.
Acknowledgements
The Nordic Cancer Union (NCU) has fi nancially supported the development of the NORDCAN data-base and programme, as well as the survival analyses in this project.
Declaration of interest: The authors report no confl icts of interest. The authors alone are respon-sible for the content and writing of the paper.
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