The incidence and body site of skin cancers in the population groups of Astana, Kazakhstan

Abstract Background and aims Data on cutaneous malignant melanoma (CMM), squamous cell carcinoma of the skin (SCC), and basal cell carcinoma (BCC) in populations consisting of multi‐racial groups in the Commonwealth of Independent States are limited. Here, the main aim was to analyse the incidence and body site of these cancers in the population groups of Astana, Kazakhstan (2007‐2016). Methods Annual age standardised incidences and body sites of BCC, SCC, and CMM in Astana's population, divided into “Kazakhs and other Turkic/Asian” and “Russian and other European/Caucasian” groups, were calculated from histologically confirmed cases reported to Astana Oncology Centre. Results During the period January 2007 to October 2016, 647 skin cancers were diagnosed. The age and sex standardised incidence of BCC, SCC, and CMM increased significantly between 2007 to 2011 and 2012 to 2016. Higher incidences occurred in the Russian and other European/Caucasian group compared with the Kazakh and other Turkic/Asian group for the 3 skin cancers. BCC was the most common type of skin tumour, followed by SCC, and then CMM, in both population groups and sexes. The head/neck was the commonest site for BCC and SCC in all groups. For CMM, the most frequent site was the trunk in the Russian group and the head/neck in the Kazakh group. Conclusion The incidence of skin tumours in Astana rose over the past 10 years. Differences in skin phototypes and sun exposure/ protection behaviours may account for the more frequent occurrence of skin tumours in the Russian population group compared with the Kazakh population group.

where the population is multi-ethnic, containing a range of skin phototypes.
Kazakhstan is a former Soviet Republic that became independent following the dissolution of the Soviet Union in 1991. Its capital city was transferred to Astana in 1997. At the time of the 2009 census, Astana's population comprised 89.1% Kazakhs, 4.5% Russians, 0.9% Ukrainians, and 2.4% Uzbeks. 4 Since 2009, Astana's population increased by around 50%, and was 872 619 in 2016, 5 consisting of 75.5% Kazakhs, 15.3% Russians, 1.6% Ukrainians, 1.1% Uzbeks, 1% Germans, and several minority groups. 6 Astana has an extreme continental climate, with warm summers and long, cold winters. It can be as hot as +35°C in the summer, while in the winter temperatures as low as −35°C are not uncommon. The UV index ranges from 1 in the winter to 7 in July/August, and daily hours of sunshine vary from 3 in November/December to 11 in June/July. 7 Table 1 shows that 58.9% of cancers were found in women and 41.1% in men, with the majority in the Russian population (46.7%), followed by the Kazakh population (26.6%).

| Body site of CMM, BCC, and SCC in the population groups
The commonest body site for BCCs and SCCs was the head/neck in all population groups and in both males and females. For CMM, the most frequent body site was the head/neck in Kazakh and other Turkic/ Asians (34.4%) and the trunk in Russian and other European/Caucasians (35.6%). However, for each cancer, there was no statistically significant association between body site and national group (Table 3).

| Age standardised incidence of CMM, BCC, and SCC
During the study period, the age and sex standardised incidence rate

| Age standardised incidence of CMM, BCC, and SCC in the Russian and other European/Caucasian and Kazakh and other Turkic/Asian groups
The incidence of skin cancer among the Russian and other European/ Caucasian group during 2007 to 2011 was 81.0 per 100 000 for men and 57.3 for women. This was 1321% and 559% greater than that experienced by the Kazakh and other Turkic/Asian group, respectively, in whom the equivalent rates were 5.7 and 8.7 per 100 000 (Table 5). Rates were higher in the Russian and other European/Caucasian group for each cancer type, and the relative differential between European/Caucasian and Turkic/Asian was greater among men compared with women.

| DISCUSSION
This study has shown that there was a higher incidence of skin cancer The photo-protection offered by epidermal melanin is a possible factor explaining the differences in incidence between national groups. 10  and Japan, is also lower than in predominantly Caucasian populations in Europe, USA, and Australia. [11][12][13][14] Apart from phototype, other factors which may differ between the population groups include personal photo-protective measures, typical clothing, and outdoor/indoor occupations. These were not investigated in the present study.
As was found in Astana, BCC is the most common skin cancer in other Caucasian and Asian populations. 15,16 In Astana, the incidence of BCC was higher in Caucasian/European men than women. An increased incidence of BCC in males has previously been reported in European countries and may be due to higher sun exposure in men, who tend to have more outdoor work, expose a larger area of their skin, and are less likely to use sun protection than women. 1,17 Conversely, the incidence of BCC was higher in Kazakh and other Turkic/Asian females than in males, which may be due to differences in occupational or recreational exposures or sun protection practices or awareness. In agreement with other studies in Caucasian and Asian population groups, the head/neck was the most common site for BCC in both groups and sexes in Astana. 18,19 Similar to results in studies involving Caucasian, Chinese Asian, and Japanese populations, the second most common type of skin cancer in Astana was SCC. 1,15,16,19 The incidence of SCC in females was consistently higher than in males in Astana, which is the converse of that reported in several European countries. 1,20 The reasons for the higher incidence of SCC in women in Astana are not clear, but a study conducted in the Japanese population of Hawaii also demonstrated a higher incidence of BCC and SCC in females than males. 19 The authors proposed that cultural and occupational differences between men and women may be responsible.
CMM was the least frequent skin cancer in Astana; the age adjusted incidences were slightly higher in men than women for both population groups. This is similar to reports of slightly higher incidences of CMM in men than women for Caucasian and Asian population groups. 15,21 Conversely, in Japan, it has been reported that malignant melanoma occurs more frequently in females than males. 15 The most common body site for CMM in the Kazakh and other Turkic Asian group was the head and neck, whereas it was the trunk in the Caucasian/European group. However, when the population groups    22 Interestingly, the sole of the foot was the commonest body sites for CMM in Japan, with acral lentiginous melanoma being the most frequent subtype. 23 The difference in body site for CMM between Kazakh and Russian males in Astana may have been due to differences in the melanoma subtype; such information was not recorded in the cancer registry.
A limitation of our study is that it is based on a specialist oncology centre registry and not on a population-based cancer registry.
Therefore, the incidence of non-melanoma skin cancer is likely to underestimate the true incidence, as tumours may be treated topically without histological verification, treated privately, or not treated at all.
Differential use of health services over time and among different population groups may contribute to the rise in incidence rates and differences between groups. We could not assess how much of the rise in skin cancer incidence was due to changes in national composition, because population counts by age, sex, and national group were not available for the inter-census years 2012 to 2016. We were also limited to using projected population estimates for 2014 which makes the analysis less reliable for this time-period. A strength of the study is that it is one of the first to report skin cancer rates in a multinational transitional population during a period in which the population has rapidly expanded, partly due to an influx of Russian and other European groups.
The World Health Organisation has attributed the rising worldwide incidence of skin cancer to depletion of the ozone layer, and increasing outdoor activities and recreational exposures. 24,25 Thinning of the ozone layer has varied over the world, with most of it at polar latitudes: it has been insignificant over Kazakhstan, thus making ozone depletion as a local risk factor for skin cancer development unlikely. 26 It is more likely that exposure to solar ultraviolet radiation (UVR) lead-