Preventive Medicine 51 (2010) 320324

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Preventive Medicine
j o u r n a l h o m e p a g e : w w w. e l s e v i e r. c o m / l o c a t e / y p m e d

Skin cancer risk factors among primary school children: Investigations in Western Hungary
Katalin Fehr a,,1, Maria Cecilia Cercato b,1, Ida Prantner c, Zsuzsanna Dombi c, Bernadett Burkali a, Judit Paller a, Valerio Ramazzotti b, Isabella Sperduti d, Edit Ndasi c, Katalin Parragi a, Ildik Menyhrt a, Pier Giorgio Natali e, Istvn Ember c
a

Western-Transdanubian Regional Institute of National Public Health and Medical Ofcers' Service, Gyr, Hungary H-9024 Gyr, Jsika u. 16 Department of Epidemiology, Regina Elena Italian National Cancer Institute, Rome, Italy I-00144 Rome, Via Elio Chianesi 53 c Department of Public Health and Preventive Medicine, University of Pcs, Pcs, Hungary H-7624 Pcs, Szigeti t 12 d Biostatistics, Regina Elena Italian National Cancer Institute, Rome, Italy I-00144 Rome, Via Elio Chianesi 53 e Laboratory of Immunology, Regina Elena Italian National Cancer Institute, Rome, Italy I-00144 Rome, Via Elio Chianesi 53
b

a r t i c l e

i n f o

a b s t r a c t
Objective. To evaluate the factors associated with sunburns and with sun protection practice in Hungarian primary school children. Method. We investigated children's (the median age: 8, range 5 to 12 years) and parents' assessment of sun sensitivity and sun protection characteristics in cities Gyr and Zalaegerszeg (Hungary) in 2004. This cross-sectional study was part of a programme intended to increase children's and parents' awareness of harmful effects of excessive sunbathing. Analyses were based on 1804 multiple choice questionnaires. Results. At multivariate analysis a signicant association between sunburns and fairness of complexion, freckles, use of sunscreens and T-shirts, and higher school-class level was observed. Sunburn was inversely associated with hat-wearing. Parents were more likely to apply sunscreen to children with light eyes and to the younger ones, to protect fair skinned children with T-shirts; to protect males and children with fair skin and light eyes with hats. Conclusion. Since environmental factors play an important role in the development of skin cancer, morbidity could be reduced by primary prevention. Sun protection habits should therefore be taught early in life, and parents' behaviour adapted. Phenotype is not only related to sunburns but it also appears to inuence parents' sun safety behaviour. 2010 Elsevier Inc. All rights reserved.

Available online 14 July 2010 Keywords: Skin cancer Melanoma Prevention Children Risk factors Hungary

Introduction The incidence of different skin cancer types, such as melanoma, in young and middle-aged people is increasing worldwide (Garbe and Leiter, 2009; Gaudi and Ksler 2003; Ries et al., 2000). As for the mortality rates, after increasing during the 1970s and 1980s in the United States of America and in Europe, in the 1990s a levelling off was observed in many countries (Garbe and Leiter, 2009). Moreover mortality for melanoma started to decline in recent cohorts in Australia, North America, UK and Sweden, where specic skin cancer prevention campaigns were more stressed (Severi et al., 2002). Epidemiological studies emphasize the role of the geographical location; the pole to equator gradient of melanoma incidence and consequences of migration are also well-documented (Armstrong and

Corresponding author. Fax: + 36 96 418068. E-mail address: feher.katalin@nydr.antsz.hu (K. Fehr). 1 Contributed equally to this work. 0091-7435/$ see front matter 2010 Elsevier Inc. All rights reserved. doi:10.1016/j.ypmed.2010.07.002

Kricker, 2001; Conti et al., 1994; Khlat et al., 1992; MacKie et al., 2002; Parkin et al., 1997; Remontet et al., 2003). Since there is no signicant difference in solar radiation among the different regions, geographical location and migration have no discernible effect on melanoma incidence in Hungary. The disease is the 7th and 6th most frequent cancer among women and men, the incidence is continuously increasing. The National Cancer Register of Hungary recorded 1117 new malignant melanoma cases in 2001 (600 females and 517 males), which mainly affected the 5075-year-old population (Gaudi and Ksler, 2002). The malignant melanoma death rate was 3.19 per 100000 in the same year, the mortality rate is higher in men than in women (Gaudi and Ksler, 2002, 2003). Using the European standard population as reference, the age-standardised death rate was 1.95 in women and 3.74 in men per 100000 population (European mortality database, 2009). Due to the increase in incidence and mortality rate, melanoma must be considered a severe public health issue also in Hungary. Among the Caucasians, fair skin-type characteristics, presence of freckles and number of moles are well known melanoma constitutional

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risk factors (Bliss et al., 1995; Gandini et al., 2005a,b). Intermittent sun exposure and history of sunburns in childhood and adulthood signicantly increase the risk; furthermore the risk increases with the number of sunburns (Autier, 2004; Gandini et al., 2005a,b; Veierod et al., 2003). Excessive sunbathing and sunburns sustained in childhood signicantly increase the risk of developing melanoma later in life (Autier, 2004; Veierod et al., 2003). Melanoma is an aggressive tumour with unfavourable prognosis if diagnosed at an advanced stage; therefore, effective prevention and early diagnosis are key factors in decreasing morbidity and mortality (Somlai, 2003). According to studies, skin cancer is largely preventable by public education and behaviour change (Hill et al., 1992). Moreover, healthy habits established in childhood may be sustained throughout life, thus sun protection habits should begin early in life, be taught as part of routine preventive health care and in school settings (Geller et al., 2003; Marks, 1987; O'Riordan et al., 2003). This cross-sectional study is part of an international project, coordinated by the Regina Elena Cancer Institute, Rome, Italy with the participation of other European and non-European countries, investigating sun sensitivity factors and sun protection practice in primary school children. The programme aims children and their parents to bring notice to the harmful effects of excessive sunbathing. The results in samples from Spanish and Italian children are already available (Cercato et al., 2008; Ramazzotti et al., 2009). The aim of this study is to evaluate the factors associated with sunburns, and with sun protection practice in Hungarian school-age children.
Methods During the school-year 2003/2004, 2530 children attending the 1st4th grades in the primary schools of two cities of the Western-Transdanubian Region in Hungary (Gyr, Zalaegerszeg) were surveyed. 19 schools were selected and cluster sampling was used. The median age was 8 (range 512) years. At the beginning of the school-year parents were informed about the aim and the phases of the project. They were asked to sign informed consent forms and to ll in the questionnaire with their children handed by their teachers and to return it within two weeks. No instructions concerning how to ll in the questionnaire were given. We considered the parent as the one reporting, taking the young age of the child into account, and the parents' signature was mandatory in considering the data from the questionnaire valid. Out of the 2530 questionnaires distributed, 1837 (72.6%) were returned completely or partially lled in. 33 children were excluded as information regarding their class grade was missing and the remaining 1804 were analysed. The questionnaire consisted of multiple choice questions addressing common risk factors for melanoma: skin, hair and eye colour, tendency in tanning and sun burning, number of moles present on the left forearm, presence of freckles and lifetime sunburns. Intense sunburns (experienced blistering) were separately recorded. The mole count on the left forearm was chosen, because there is evidence suggesting that the number of moles present on one part of the body fairly accurately estimates the total number of moles on the whole body (Farinas-Alvarez et al., 1999). Regular use of sun protection measures (sunscreens, hats, T-shirts, and sunglasses) and demographic variables (age, sex, and residence) were also collected. Data from the respondents were entered in a database and forwarded to the Regina Elena Cancer Institute to be processed. At the end of the school-year each child received a letter outlining the recommendations to be adopted during sun exposure according to current guidelines (using sunscreens, wearing sunglasses, hats and T-shirts, avoiding sunbathing during the midday hours: 11 am to 3 pm during daylight saving time) (McKinlay et al., 2002). Data handling was in accordance with Act LXIII of 1992 on the Protection of Personal Data and Public Access to Data of Public Interest of Hungary. Statistical analysis In this study the history of sunburns represents the indicator of exposure to sun damage. Children reporting at least one experience of sunburn were considered to be positive. The class grade was chosen as a valid proxy of age and as an indicator of a child's educational level. Eye colour was recoded into light

(green/blue) and dark (brown/black). The Odds Ratio (OR) and their relative 95% Condence Intervals (95% CI) were computed through univariate and multivariate logistic regression models to evaluate the association of sunburns with constitutional factors and with sun protection practices; the association between sun protection practices and children characteristics was also assessed. The multivariate logistic regression model was developed using stepwise regression (forward selection) with predictive variables that were signicant in the univariate analyses. The cut-off p-value to enter in or to be removed from models was set between 0.10 and 0.15. Multiple Correspondence Analysis (MCA), a descriptive/exploratory technique designed to analyse simple two-way and multi-way tables, was used to identify high-risk prole according to the distribution of sun sensitivity constitutional characteristics and to sun protection behaviour. The results provide information which is similar in nature to those produced by factor analysis techniques, and they make it possible to explore the structure of the categorical variables included in the table. The most common kind of table of this type is the two-way frequency cross-tabulation table (Greenacre, 1984; Lebart et al., 1984). This representation aims to visualize the similarities and/or differences of proles simultaneously, identifying those dimensions which contain the majority of data variability. The position of the points in the MCA graph is informative. Categories plotting close to each other are statistically related and have patterns of relative frequencies. This association is statistically valuable (Lebart's statistic) when the points are located far from the origin of the graph which represents a mean, uninformative prole. The data were analysed by using the SPSS version 13 (SPSS, Inc., Chicago, IL).

Results Tables 1 and 2 show the characteristics of the study population. Fairness of complexion is a common feature: light eyes, fair hair (red, fair/light brown) and fair skin represent 47%, 66% and 42% of cases, respectively. Sun exposure is frequently reported: the majority of children usually spent their summer holiday outside the city at the waterfront (64%) or in the mountains (17%) and 93% of the participants reported to get sun-tanned at the end of the summer. Although 67% of the whole samples reported do not easily get sunburnt, 56% of it reporting previous sunburns with blisters in 8% of cases. Sun protection practices adopted include sunscreens (90%), T-shirts (75%), hat (63%) and sunglasses (50%). When exploring the relationship between sun sensitivity characteristics related to pigmentation and sun protective measures using Multiple Correspondence Analysis (MCA) four groups corresponding to two risk levels were clearly dened; more in detail, a close association among the characteristics dening a high-risk constitutional prole (fair skin, eyes, hair colour, presence of freckles and of nevi) as well as among those dening a high-risk behavioural prole (not using sunscreen, T-shirt, hat, and sunglasses) was observed (Fig. 1). Through univariate and multivariate logistic regression models we evaluated determinants of sunburns. At univariate analysis a signicant direct association was observed between sunburns and light eyes (OR: 1.52; 95% CI: 1.261.83), fair hair (red vs. dark, OR: 4.39; 95% CI: 1.2615.34; fair/light brown vs. dark, OR: 1.34; 95% CI: 1.101.63), fair skin (fair vs. medium-dark, OR: 2.00; 95% CI: 1.652.43) presence of freckles (OR: 2,22; 95% CI: 1.742.83), presence of nevi (OR: 1.37; 95% CI: 1.121.68), use of sunscreens (OR: 1.39; 95% CI: 1.021.88) and of T-shirt (OR: 1.44; 95% CI: 1.151.79) and school-class level (OR: 1.29; 95% CI: 1.191.40). Wearing hats was inversely associated with sunburns (OR: 0.81; 95% CI: 0.660.99), while no association was found for gender, area of residence (city vs. countryside), type of holiday and tendency to tan. Multivariate analysis conrms that fair skin, light eyes, freckles and higher school-class level were factors predicting sunburns; moreover the use of sunscreens and T-shirt was also directly associated with history of sunburns, while wearing hat showed a protective effect (Table 3). When examining determinants of sun protective behaviour (to apply sunscreen; to wear T-shirt, hat, sunglasses) at multivariate analysis including in the model skin, eye and hair colour, presence of freckles, presence of nevi, gender and class grade, parents were more

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Table 1 General and constitutional characteristics of the 1804 primary school children in Hungary (school-year 2003/2004). General characteristics Sex Male Female School Class 1 2 3 4 na (%) 908 (50.3) 896 (49.7) 812 320 320 352 (45%) (17.7) (17.7) (19.6) Constitutional characteristics Eye colour Brown Black Blue or Green Hair Colour Red Fair/light brown Dark brown/black Skin Fair Medium Dark Number of moles 0 15 N5 Freckles Yes No na (%) 914 (50.8) 33 (1.8) 851 (47.3) 17 (0.9) 1176 (65.4) 605 (33.6) 758 (42.2) 1000 (55.6) 39 (2.2) 547 (31.2) 1046 (59.6) 161 (9.2) 385 (21.6) 1395 (78.4)

n = Sample size; the sum may not add up to the total because of some missing values. Fig. 1. Multiple correspondence analysis plot showing constitutional and behavioural risk proles of the primary school children in Hungary (school-year 2003/2004).

likely to apply sunscreen to the children with light eyes and to the younger ones; to protect the fair skinned children with a T-shirt and to protect the children with fair skin, light eyes and the males with a hat (Table 4). As to concern wearing sunglasses it is more frequently reported among the females and the older ones. Furthermore, parents protect more frequently the females with sunscreens and children with nevi with a T-shirt, but the differences do not reach the statistically signicance. Taking into account that wearing hat is the only protective measure inversely related with sunburns, we explored the relationship between this practice and the other ones. Chi-square results showed that children wearing hats are also more likely to use sunscreens (p b 0.0001), to wear T-shirt (p b 0.0001) and sunglasses (p b 0.0001), compared to children who do not (data not shown). Discussion Over the last few decades a signicant increase in the number of patients suffering from skin cancer was reported worldwide (Gaudi and Ksler, 2003; Garbe and Leiter, 2009; Ries et al., 2000). Early diagnosis and effective prevention may play an important role in decreasing the morbidity and the mortality rate for melanoma

(Somlai, 2003). The U.S. Task Force on Community Preventive Services found that education and policy approaches to increasing sun protection behaviour were effective when implemented in primary schools (Saraiya et al., 2004). In Australia, where a national public health skin cancer prevention program has been conducted for 20 years a decrease in skin cancer incidence and mortality rate has been reported (Marks, 1999). This study is a part of an international programme aimed to protect children from the risks related to excessive sun exposure. The questionnaire allowed dening the constitutional and behavioural risk proles in West-Hungarian children. Strengths of the study include the relatively large sample, the response rate and the novelty of providing sun protection habits from a selected population for which limited or no evidence exists. Some limitations must also be considered: the bias involved in the self and parents' assessment method, the absence of a measurable indicator of sun exposure damage and the selection of the most relevant and simple items to detect. In facts, questions investigating the timing of

Table 3 Multivariate analysis: predictors of sunburns in Hungarian school-age children (schoolyear 2003/2004). Variable Skin Fair Medium/dark Eyes Light Dark Freckles Yes No Class grade Sunscreen Yes No T-shirt Yes No Hat Yes No n (total = 1528) 638 890 724 804 342 1186 1528 1382 146 1118 410 943 585 OR (CI 95%) 1.87 (1.492.35) 1 1.24 (0.991.54) 1 1.64 (1.252.14) 1 1.31 (1.201.44) 1.46 (1.012.11) 1 1.33 (1.051.69) 1 0.70 (0.560.88) 1 p-value b 0.0001

Table 2 Sun exposure characteristics of the 1804 primary school children in Hungary (schoolyear 2003/2004). Sun Exposure Characteristics Lifetime sunburns Yes No Tendency to sunburnt Yes No Sunscreen Yes No Hat Yes No Holidays At the seaside/lake In the mountains In town
a

na (%) 1010 (56.1) 790 (43.9) 587 (32.7) 1208 (67.3) 1608 (89.6) 186 (10.4) 1060 (63.5) 610 (36.5) 1144 (64.3) 305 (17.2) 329 (18.5)

na (%) Blisters Yes 146 (8.2) No 1633 (91.8) Sun-tanned Yes 1665 (93.5) No 116 (6.5) T-Shirt Yes 1275 (74.9) No 428 (25.1) Sunglasses Yes 817 (50.2) No 809 (49.8)

0.05

b 0.0001 b 0.0001 0.04

0.02

0.002

n = Sample size; the sum may not add up to the total because of some missing values.

OR, Odds Ratio; CI, Condence Interval; n, sample size.

K. Fehr et al. / Preventive Medicine 51 (2010) 320324 Table 4 Multivariate analysis: predictors of sun protective behaviour in Hungarian school-age children (school-year 2003/2004). Variable Sunscreen OR (95% CI) School class Sex Male Female Skin Medium/dark Fair Eyes Dark Light Nevi No Yes OR, Odds Ratio; CI, Condence Interval; n, sample size. 0.74 (0.650.85) 1.00 1.36 (0.981.87) 1.00 1.36 (0.951.95) 1.00 1.54 (1.102.18) 0.06 p-value b 0.0001 T-shirt OR (95% CI) p-value Hat OR (95% CI) p-value Sunglasses OR (95% CI) 1.21 (1.111.32) 1.33a (1.081.63) 1.00 b 0.0001 1.00 1.71 (1.402.10)

323

p-value b 0.0001

b 0.0001

0.09

1.00 2.03 (1.602.58)

b 0.0001

1.00 1.34 (1.081.66) 1.00 1.28 (1.031.58)

0.009

0.01

0.02

1.00 1.23 (0.971.57)

0.09

sun exposure, the frequency and suitability of sunscreen application, as well as items concerning the family (socioeconomic status, educational level, melanoma family history) were excluded. The results are relevant because they highlight that melanoma risk factors (fairness of eye, hair and skin colour, presence of nevi and experience of sunburns) are common in the investigated children population. As reported by other studies, the study pointed out that constitutional characteristics such as fair complexion, presence of freckles and older age were factors predicting sunburns (Balato et al., 2007; Cercato et al., 2008; Dixon et al., 1999; Ramazzotti et al., 2009; Severi et al., 2002; Stinco et al., 2005). These ndings conrm the evidence of the higher susceptibility of fair skinned individuals and highlight a decline in sun protection practices in older children, probably due to reduced parental control. Concerning to behavioural characteristics, the results show that applying sunscreen and wearing T-shirt regularly are factors directly associated with history of sunburns, while wearing hat is inversely related. This study takes into account the limitation of the cross-sectional survey that does not provide information on the timing and the sites of sunburns (do sunburns predated the use of sunscreen/T-shirt? What part of the body has been overexposed to sunburns?). These data suggest that, except for the group characterized by appropriate use of hat, parents are more inclined to use protective tools rather than limit their children's sun exposure; these data are consistent with the results of other investigations (Robinson and Rademaker, 1998; Stinco et al., 2005). A systematic review of the evidence linking sunscreens use to sun exposure duration found that intentional sun exposure tends to be longer when a sunscreen is used or when SPF (sun protection factor) increases (Autier et al., 1999, 2007). Moreover, in order for sunscreens to be effective they need to be properly applied (e.g. re-applying sunscreens in every two hours and after bathing) (McKinlay et al., 2002; Odio et al., 1994). In addition, wearing T-shirt also could extend the length of the intentional sun exposure, but it is not sufcient to protect all parts of the body (head, forearms, and lower limbs). The decreased risk of sunburns observed in those hat-wearing children who are also more likely to use the other protective measures, suggests that this practice is an index of an appropriate protective behaviour, probably based on sun avoidance. The parents' knowledge of hat-wearing children seems to be adequate and their children's hat-use to be conscious and effective. However, given that sun safety habits were not effective in our population, we explored the determinants of sun protection practices.

Data show that parents are more likely to protect children at higher risk of skin damage: the younger and the fair-coloured ones. Furthermore, gender-related behaviour was also observed: females were more frequently protected by sunscreen and males by hat, independently from complexion and age. Finally, sunglasses were mainly adopted by females and by older children; this data are in agreement with the results of our previous published studies conducted among European children and suggest a fashion motivated behaviour more than a protective one (Cercato et al., 2008). Data of our investigations highlight the importance of improving sun safety. A comparative analysis of sun sensitivity factors and determinants of sun protection behaviour of different countries will be shortly presented. Conclusion Even though Hungary is not surrounded by water, spending holidays at the waterfront, where health damaging effects of solar radiation are enhanced is very popular among primary school children. Due to public health education and advertisements, the majority of children already use some kind of sun protection, mainly sunscreen and T-shirt. However, the high rate of subjects referring sunburn experience evidences that sun protection habit is not effective. In several other epidemiological studies investigating children's sun exposure in different countries, overall conclusions are that despite the evidence of the parents' knowledge about the risk related to sunburns, the sun protection practices adopted for their children are generally not appropriate (Balato et al., 2007; Bourke and Graham-Brown, 1995; Dixon et al., 1999; Robinson and Rademaker, 1998; Severi et al., 2002; Stinco et al., 2005). Determinants of parents' behaviour need therefore to be further investigated to improve children's sun protection.

Conict of interest statement The authors declare that there are no conicts of interest.

Acknowledgments Dr. E. Conti who prematurely died, made decisive contributions to the study.

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