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  Volume 95
Numero 6
novembre-dicembre 2009 		I documenti sono in formato PDF, consultabili utilizzando Acrobat Reader
 
Strong seasonality in the diagnosis of skin melanoma in Italy: the Italian Network of Cancer Registries (AIRTUM) study

Emanuele Crocetti, Stefano Guzzinati, Eugenio Paci, Fabio Falcini, Roberto Zanetti, Marina Vercelli, Ivan Rashid, Vincenzo De Lisi, Antonio Russo, Susanna Vitarelli, Stefano Ferretti, Lucia Mangone, Rosaria Cesaraccio, Rosario Tumino, Susanna Busco, Carlotta Buzzoni
1Registro Tumori Toscano, Unità di Epidemiologia Clinica e Descrittiva, ISPO, Florence;
2Registro Tumori del Veneto, Istituto Oncologico Veneto, IRCCS, Padua; 3Registro Tumori della Romagna, IRST, Meldola (FC); 4Registro Tumori del Piemonte, Ospedale S. Giovanni Antica Sede, Turin; 5Registro Tumori Regione Liguria c/o SS Epidemiologia Descrittiva IST Genoa, Dipartimento di Scienze della Salute, Università di Genova, Genoa; 6Registro Tumori della Provincia di Modena, Policlinico, Modena; 7Registro Tumori della Provincia di Parma, Ospedale di Parma, Parma;
8Registro Tumori Milano, ASL Città di Milano, Servizio di Epidemiologia, Milan; 9Registro Tumori della Provincia di Macerata, Università di Camerino, Camerino (MC); 10Registro Tumori della Provincia di Ferrara, Istituto di Anatomia Patologica, Ferrara; 11Registro Tumori della Provincia di Reggio Emilia, Azienda USL di Reggio Emilia; 12Registro Tumori della Provincia di Sassari, Centro di Osservazione Epidemiologica, Sassari; 13Registro Tumori di Ragusa, Ospedale Maria Paternò Arezzo, Ragusa; 14Registro Tumori di popolazione della provincia di Latina, Azienda USL Latina, Latina;
15Italian Association of Cancer Registries data-bank, Florence, Italy

Key words: diagnosis, melanoma, population-based, seasonality.

abstract

Aim. To evaluate seasonality in the diagnosis of cutaneous melanoma in Italy.
Methods. A total of 16,284 invasive (and 1,235 in situ) cutaneous melanomas incident from 1978 to 2002 in 14 cancer registries belonging to the Italian Network of Cancer Registries (AIRTUM) was analyzed. We used the Walter and Elwood test to evaluate seasonality. The monthly distribution of diagnosis was evaluated for sex, skin site, melanoma morphology and period of diagnosis.
Results. The overall monthly diagnosis of invasive melanoma showed a statistically significant excess around the month of June. The same pattern was present for males and females, across age-groups and periods of time. All skin sites showed a cycling trend, melanoma of the head and neck peaked around April, all the others peaked around June. As regards morphologic types, a cyclic trend was evident for superficial-spreading melanomas (peak around July), for not-specified melanomas (June) and for other histotypes (June). Diagnosis of in situ melanoma peaked in September.
Conclusions. The present study showed that also in Italy melanoma diagnosis has a seasonal trend, with the peak in early summer. It seemed that summer UV exposure, acting both as a late promoter of malignant melanoma development and also increasing the visibility of pigmented skin lesion, may be relevant to explain such a peak.

Introduction
Seasonality in cutaneous malignant melanoma (MM) diagnosis has been documented in several western countries, usually with a summertime peak1-10. The reasons for such seasonality are still unclear, even though several possible explanations have been suggested. A possible effect of public campaigns for early detection usually carried out during spring-summer has been emphasized5. Increased patient awareness and self-detection of suspected lesions due to summer clothing have also been documented5, and even a short-term promoting effect of UV exposure has been suggested5. Although the amplitude of seasonality seems to increase with decreasing latitude7, sparse data are available for Mediterranean countries7,11-12.
To contribute to this issue, we analyzed data from a pool of Italian population-based cancer registries.

Materials and methods
Data were retrieved from the Italian Network of Cancer Registries (AIRTUM – www.registri-tumori.it) data base, which collects data from Italian general and specialized population-based cancer registries13. The present study focused on cutaneous MM diagnosed from 1978 to 2002. Overall, 16,284 invasive MM were included in the study. In situ MM (n = 1,235) were analyzed separately. For the present study, data from the following registries were used: Tuscany (incidence data from 1985 to 2002), Parma (1978-2002), Reggio Emilia (1996-2002), Modena (1988-2002), Ferrara (1991-2002), Sassari (1992-2002), Veneto (1987-2001), Torino (1985-2001), Milano (1999-2002), Latina (1990-2000), Macerata (1991-2000), Genova (1987-2000), Romagna (1986-2002) and Ragusa (1985-2002). Overall, the registries included in the study covered a population of about 10,730,000 inhabitants, which represented 18.8% of the total resident Italian population.
Histologic verification was available for 97.0% of MM (range among registries, 86.4-100%), and the mean incidence of cases known from death certificate only was 0.4% (range among registries, 0-0.9%).
Seasonality was evaluated by means of the Walter and Elwood test for seasonality of a binary outcome with a variable population at risk14 implemented in the routine ‘seast’ of the software Stata (www.stata.com). The Walter and Elwood test adjusts for a varying population at risk14. The option ‘exact’, which forces the test to adjust for variable month length, was applied. The test considers observations in each sector (month) arising as moments around a unit circle, with the data corresponding to sector midpoints. The test assumes that within a year there are 12 periods (months) and that in each period n events occur from a population at risk of a certain size. Data may be represented as placed around a unit circle at points corresponding to the periods. The test produces two measures: α as the measure of the amplitude of the cyclic variation, and Θ which gives the direction of the maximum rate14. For the latter measure, single months are in counterclockwise position in the circle and correspond to the following mean angle: January 15°, February 45°, March 75°, April 105° and so on up to December 345°.
The monthly distribution of diagnosis was evaluated for invasive MM for: sex (males and females); site (head & neck, upper limb, lower limb, trunk, other, and not specified); morphology (superficial-spreading melanoma (ICDO-3 code = SSM), nodular melanoma, melanoma on malignant lentigo, acral lentiginous melanoma, other, not otherwise specified); period of diagnosis (1978-1982, 1983-1987, 1988-1992, 1993-1997, 1998-2002).

Results
The overall monthly diagnosis of invasive MM showed a statistically significant excess from the cyclic variation with the maximum around the month of June (represented by Θ values between 150 and 180) (Figure 1 and Table 1). The same pattern was present for males and females (Table 1). No differences from this early summer peak were evidenced either across age groups or across periods of time of diagnosis, except for 1978-1982, for which very few cases were available (Table 1). According to the site of MM onset, all main sites showed a cyclic trend: MM of the head and neck peaked around April, all the others peaked around June (Table 1).






Sex and site-specific results were similar to the mean value for both sexes together for upper limb (males Θ = 182.3, P = 0.02, females Θ = 176.7, P <0.001) and for lower limb (Θ = 181.0, P = 0.036, females Θ = 191.2, P <0.001), slightly different for head and neck (males Θ = 90.8, P <0.001, females Θ = 108.6, P <0.001) and especially for trunk (males Θ = 162.2, P <0.001, females Θ = 138.3, P <0.001), which showed an anticipated peak in May for females.
As regards MM morphologic types, a cyclic trend was evident for superficial-spreading melanomas (peak around July), for not otherwise specified melanomas (June) and for other histotypes (June), whereas no statistically significant cyclic trend was evidenced for nodular, acral, or lentigo melanomas.
The excess in June and July did not fill up the deficit in August. In fact, the mean incidence rate of the period June-August was significantly higher (1.09 cases/100,000 subjects/year; 95% CI, 1.05-1.12) than that of the other months (0.85; 95% CI, 0.83-0.87).
The analysis was carried out separately for 1,235 in situ MM. For these tumors, a statistically significant cyclic trend peaking in October was documented. Only some of the Registries contributed with in situ MM. To exclude a possible selection bias, for registries that provided in situ MM we repeated the analysis also for invasive MM, and again the summer peak was evidenced (data not shown).

Discussion
The present descriptive study, carried out on a huge population-based case series, confirmed that also in Italy there was seasonality in the diagnosis of MM, with a peak of new diagnoses around June. This summer peak was present for males and females and through all the analyzed age groups. As evidenced in the US, there was a substantial seasonal variation in the diagnosis of almost all morphology types, except for nodular MM3.
The peak in early summer was not explained as a consequence of an anticipated medical attendance before a holiday period. In Italy, in August there is the modal value of holidays, and in this month also most of the health services reduce their activity. The peak of diagnosis in early summer is much greater than the loss in August, and other explanations than just a ‘holiday effect’ need to be considered.
The effect of public campaigns for MM early detection (e.g., http://www.skincancerday.it) was one of the proposed explanations for this summer peak. The effect should have been enhanced during recent years according to the diffusion of such public health campaigns usually performed at the beginning of summer5. However, although these campaigns have increased over time, the summer peak was evidenced in the 80’s, when the popularity and attention on skin MM and its early diagnosis was less than today.
In other studies, the early diagnosis effect was supported by a higher percentage of thinner MM7-8 and by a better survival for MM diagnosed in summer than for those detected in other seasons8. Unfortunately, information on Breslow thickness and Clark level was not available in the present case series, and no evaluation of the relationship between seasonality and stage at diagnosis was possible. However, early diagnosis should be effective for both invasive and not yet invasive MM, but the summer peak was not documented for in situ MM15, which on the contrary showed a peak of diagnosis in Autumn. Therefore, it seems that different explanations seem to work for invasive and in situ MM15.
Increased patient awareness and self-detection of suspected lesions due to summer clothing has also been considered relevant among the possible explanations for the summer peak in diagnosis10. Data on site of MM were also analyzed for gender, assuming a difference in summer clothing and in the willingness to get a tan and to sunbathe between males and females. Although better visibility with less clothing during spring and early summer may be important, present data analyzed for subsites and gender did not confirm such an explanation. In fact, all the skin subsites, except for head and neck, showed the same summer peak. On the contrary, we would have expected a more evident effect for usually unexposed body sites (e.g., trunk) and also some differences between males and females (e.g., for lower limbs).
Another possible explanation of the summer peak may include the effect of intense sun exposure on the visibility, and consequently on the detectability of a melanocytic proliferation. An increased pigmentation in melanocytic nevi after intense UV exposure has been documented16-17 as the proliferation and activation of epidermal melanocytes16. Therefore, intense sun exposure that occurred in summer may alert the patient himself or the physician about a pigmented lesion. If this was the case, and if a quite long exposure was necessary, then detectability of suspicious lesions would be more likely to occur at the end rather than at the beginning summer. On the one hand, this was true only for in situ MM, which peaked in October. On the other hand, a short-term UV-induced darkening effect may contribute to explain the peak of invasive MM.
Among the other possible explanations for the summer peak in MM diagnosis, there was also the possible effect of UV radiation as a promoting factor for the progression of MM during the late stages of development of the disease5,9. This hypothesis would also be in accord with the peak evidenced for invasive but not for in situ MM.
In conclusion, the present study confirmed that also in Italy MM diagnosis had a seasonal trend, with the peak in early summer. Presumably, seasonality is multifactorial in a disease which has been demonstrated to be pathogenetically heterogeneous. Among the other possible explanations, it seemed that summer UV exposure – acting both as a late promoter of MM development and also increasing the visibility of pigmented skin lesion – may be relevant to explain such a peak.

References
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 2. Swerdlow AJ: Seasonality of presentation of cutaneous melanoma, squamous cell cancer and basal cell cancer in the Oxford Region. Br J Cancer, 52: 893-900, 1985.
 3. Schwartz SM, Armstrong BK, Weiss NS: Seasonal variation in the incidence of cutaneous malignant melanoma: an analysis by body site and histologic types. Am J Epidemiol, 126: 104-111, 1987.
 4. Braun MM, Tucker MA, Devesa SS, Hoover RN: Seasonal variation in frequency of diagnosis of cutaneous malignant melanoma. Melanoma Res, 4: 235-241, 1994.
 5. Lambe M, Blomqvist P, Bellocco R: Seasonal variation in the diagnosis of cancer: a study based on national cancer registration in Sweden. Br J Cancer, 88: 1358-1360, 2003.
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 8. Boniol M, Armstrong BK, Doré J-F: Variation in incidence and fatality of melanoma by season of diagnosis in New South Wales, Australia. Cancer Epidemiol Biomarkers Prev, 15: 524-528, 2006.
 9. Scotto J, Nam JM: Skin melanoma and seasonal pattern. Am J Epidemiol, 111: 309-314, 1980.
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13. AIRTUM Working group: Italian cancer figures – report 2006. Incidence, mortality and estimates. Epidemiol Prev 30, 2006 suppl 2.
14. Walter SD, Elwood JM: A test for the seasonality of events with a variable population at risk. Br J Prevent Soc Med, 29: 18-21, 1975.
15. Akslen LA, Hartveit F: Cutaneous melanoma – season and invasion? A preliminary report. Acta Derm Venereol, 68: 390-394, 1988.
16. Tronnier M, Smolle J, Wolff HH: Ultraviolet irradiation induces acute changes in melanocytic nevi. J Invest Dermatol, 104: 475-478, 1995.
17. Stanganelli I, Rafanelli S, Bucchi L: Seasonal prevalence of digital epiluminescence microscopy patterns in acquired melanocytic nevi. J Am Acad Dermatol, 34: 460-464, 1996.



 
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