Non-melanoma skin cancer among ethnic German immigrants (resettler) from the former Soviet Union: a cohort study from 1990 to 2007
Archives of Public Health volume 80, Article number: 85 (2022)
UV radiation is a significant risk factor for non-melanoma skin cancer (NMSC). Ethnic Germans (resettlers) who immigrated to Germany from the former Soviet Union may have had a relatively high UV light exposure and thus a higher risk of developing NMSC. We compared the incidence of NMSC in a resettler cohort with the general population of the Saarland (Federal state of Germany) in relation to tumour location.
All new NMSC cases (resettler cohort and total population) between 1990 and 2007 were retrieved from the Saarland cancer registry and classified according to sex, histology, and location. The classification used for tumour location approximated the previous UV exposure. Age-standardized incidence rates (ASR) for the general population and standardized incidence ratios (SIR) for resettlers compared to the general population were calculated and modelled using Poisson regression.
Sex-specific overall SIR indicated a significant increase in female resettlers (SIR 1.31 (95% CI 1.02–1.67)) which can mostly be attributed to an increased incidence of squamous cell carcinoma. The regression analysis showed that among resettlers the risk of developing tumours in UV-exposed skin areas was 2.16 (95% CI 1.35–3.45) higher compared to the general population.
Female resettlers have a higher risk to be diagnosed with NMSC than the general German population. Based on the observed distribution of tumour location, it is suspected that UV exposure contributed significantly to this risk.
Non-melanoma skin cancer (NMSC) is the most common type of cancer in humans. However, the term NMSC is not clearly defined. It represents a group of cutaneous malignancies including basal cell carcinomas (BCC), cutaneous squamous cell carcinomas (SCC) and some other types (inter alia extramammary Paget's disease, Merkel cell carcinoma, skin adnexal carcinomas). In Germany, about 230,000 people developed NMSC in 2016 . BCC is a slowly destructive and infiltrative tumour that metastasises very rarely. With an incidence of approximately 200 new cases per 100,000 people in 2013, it was the most common skin cancer entity in Germany . SCC represent the second most common non-melanoma skin cancer showing an indolent clinical course. This type of skin neoplasia begins typically with a premalignant lesion – actinic keratosis. Metastases of SCC were observed in a prospective study with a frequency of 4% within 43 months . Tumours other than BCC/SCC represent a small inhomogeneous group of skin neoplasms with different and not always clear aetiology.
The most important risk factor for the development of BCC and SCC is ultraviolet (UV) radiation exposure. UV radiation is considered an obligate carcinogen for humans . In the case of BCC, it is assumed that intermittent irradiation, especially in childhood, but also intensive tanning in the context of leisure activities is decisive [5,6,7,8]. In the case of SCC, the cumulative dose over a lifetime is of particular importance . The meaning of UV exposure for the tumours other than BCC/SCC depends on entity and is presumably of subordinate importance.
According to the Federal Statistical Office, approximately 25.5% of the German population has a migration background . Of these, the so-called Aussiedler (resettlers) with their own migration experience represent the second largest group (approx. 2.6% of the total German population) . Resettlers are immigrants of German descent who came from states of the former Eastern Bloc. Until 1989 they mostly came from Poland and Romania, however their majority immigrated from the states of the former Soviet Union after 1990, mainly from Kazakhstan and the Russian Federation . In previous studies, it has been shown, that resettler have higher risk in comparison to the general German population to develop stomach cancer and lung cancer but a lowered risk for breast cancer [12, 13].
NMSC is the most common form of cancer and is of particular importance for public health. In this study, we investigated the incidence of NMSC in ethnic Germans from the former Soviet Union in comparison to the general German population. Of specific interest are UV-exposed tumours, as there could be an increased risk among resettlers due to a higher UV exposure in their countries of origin.
Within the framework of a retrospective register-based study, we investigated the occurrence of NMSC in a cohort of resettlers in comparison to the total population of the Saarland (Federal state of Germany). The cohort consists of 18,619 resettlers (approximately 64% all resettlers) who immigrated to the Saarland between the years 1990 and 2005 from countries of the former Soviet Union. The dataset was directly obtained from all local reception centres and contained name, date of birth, issue date of a German passport as an approximation for date of migration, sex, country of birth and first city of residence .
The observation period started with the date of migration, which was determined by the date of issue of the German passport [12, 15]. To avoid bias due to the introduction of skin cancer screening in Germany, December 31, 2007, was defined as the end of follow-up for the present study.
The regional registration authorities were asked about the vital status and out-migration from the study area (Saarland), which were considered to be the end of follow-up for the study.
Data on skin cancer incidence (every first NMSC-case per person) were provided by the Saarland cancer registry. The identification of the resettler cohort among the Saarland population was done with the help of a computer-assisted record linkage procedure by the comparison of name components and their phonetic codes as well as information on sex, date of birth, and place of residence . All cases of skin cancer of the total Saarland population including resettler cohort were coded according to the International Statistical Classification of Diseases and Related Health Problems 9th Revision (ICD-9) and the morphological code of the International Classification of Disease for Oncology 2nd Revision (ICD-O 2). Histological types were coded as BCC, SCC and Other using the ICD-O 2 classification. UV light exposure was approximated by tumour location using the ICD-9 classification (see Table 1) [6, 16].
Person-years of time under risk for the resettler cohort were calculated separately for both sexes, calendar years and 5-year age groups.
Age-standardised incidence rates (ASR) of the Saarland population were calculated based on the mid-year population and the European Standard Population  for the following categories, separately by sex and calendar year: all skin cancers, histological type (BCC, SCC, Other), approximated UV light exposure (UV-exposed, UV-unexposed, Unknown). Standardised incidence ratios (SIR) were calculated for resettlers in comparison to the Saarland population for the same categories as well as by sex and two time periods (1990–1998, 1999–2007). For this purpose, the number of skin cancer cases observed among the resettlers was divided by the expected number, which results from the age- and calendar year-specific Saarland rates and the person-years of the cohort. Exact 95% confidence intervals (95% CI) were calculated for ASR and SIR [18, 19].
Finally, the SIR was modelled using Poisson regression to examine independent effects. The observed number of diagnoses served as the dependent variable, the expected number as the offset and standard errors were scaled using Pearson's chi-square. Independent variables were calendar year (continuous as year minus 1990), sex, histological type, and approximated UV radiation exposure. All statistical analyses were performed using Stata 15.1 IC (Copyright 1985–2017 StataCorp LLC, StataCorp, 4905 Lakeway Drive, College Station, Texas 77,845 USA).
The cohort of resettlers consists of 18,619 persons, of whom 8,976 were men and 9,643 women. During the observation period it accumulated 177,644.2 person-years with a mean observation time of 9.5 years. A total of 18,575 new cases of skin cancer were identified in the Saarland during the same period, of which 51.5% were in men. Among resettlers, 43.3% of the 120 diagnoses were among men (see Table 2). The mean age at diagnosis was 69 years in the general population and 68 years in resettlers. Overall, 80.5% of all skin cancer diagnoses were BCC and 17.4% SCC. Among resettlers, it was 75.8% and 23,3%, respectively. The approximated UV exposure status (tumour location) showed an unequal distribution between resettlers and the general population. Rather UV-exposed tumours represented 66.7% of the diagnoses in the Saarland population (22.9% unexposed, 10.4% unknown) and 76.7% (14.2% unexposed, 9.2% unknown) in resettlers.
Figure 1 shows the temporal development of ASR of Saarland population according to approximated UV exposure (tumour location) and sex for the general population of the Saarland. The ASR per 100,000 persons is relatively stable over the observation period (year 2007) with 58.6 (95% CI 57.2–59.9) for men and 37.1 (95% CI 36.1–38.0) for women for UV-exposed locations. For comparison, ASRs of UV-exposed locations among resettlers (estimated by means of SIR) were 61.4 (95% CI 40.6–82.2) for men and 57.9 (95% CI 42.3–73.5) for women.
For total NMSC, the standardised incidence ratios (SIR) comparing resettlers to the general population were not increased (see Table 3), but when looking sex-specifically, there was an increase for female resettlers (1.31 (95% CI 1.02–1.67)), especially in the first period (1990–1998). When separated according to the approximated UV exposure status, there was again a higher SIR for women. When separated by histological type, higher SIR were also found for SCC among both sexes together and among women.
Table 4 presents the independent variables influencing the SIR modelled by Poisson regression. All independent variables show a significant (p < 0.05) association with the SIR. On UV-exposed skin areas, the SIR was independently increased by a factor of 2.16 (95% CI 1.35–3.45) compared to non-exposed skin areas. Furthermore, it should be emphasised that the SIR decreases every year.
In the present study, we investigated the incidence of non-melanoma skin cancer among resettlers from the former Soviet Union with a special focus on tumour location and previous UV exposure. It is shown that skin cancer developed more frequently in UV-exposed skin areas of female resettlers compared to the female general population. Accordingly, there was also a higher proportion of squamous cell carcinomas. Over time skin cancer incidence decreased among resettlers while rates of the general population remained largely stable.
Factors that significantly determine individual UV exposure are skin type, geographical location of residence, leisure time behaviour and occupational exposure. With regard to skin type, there are no known differences between resettlers and Germans; both are assigned to the Caucasian skin type .
Historically, resettlers immigrated mainly from Kazakhstan and the Russian Federation, and there mainly from Siberia. In Kazakhstan, the climate is strictly continental and the UV index in Astana (now Nur-Sultan, the capital of Kazakhstan) is 6–7 (high) during June and July [21, 22]. However, Astana is located more in the northern part of Kazakhstan. Cities in southern Kazakhstan, such as Almaty (former capital of the Kazakh Soviet Socialist Republic) show a UV index in July between 8–10 (very high) up to 11 (extreme) . In addition to time of year and day, the UV index depends mainly on latitude and is directly associated with the risk of NMSC [23,24,25]. The most frequent tumour localisations of BCC and SCC were reported in the head and neck region among Astana residents . As for climatic conditions in Russia, it is not possible to generalise due to the size of the country. One of the most important settlement regions of ethnic Germans in Russia are areas around the city of Omsk and the Altai region in Siberia, which are located around 54° and 60° north latitude, respectively. There, a UV index of max. 7 (high) is reached . By comparison, the average value for the UV index in July 2019 in the city of Wiesbaden (the closest measuring station with a documented UV index history for the Saarland) was 6 (high) .
In the former Soviet Union, public life usually took place outdoors in the summer with limited leisure activities and crowded living conditions. In addition, work in one's own garden was common as an important place to grow food due to the lack of goods in stores. Furthermore, in Soviet times, forced labour in fields was also part of everyday life in the Asian republics for schoolchildren, students, and state employees [28, 29]. The work usually took place at harvest time in the fall over a period of several weeks. Those affected at times lived in tent camps and worked outside every day, regardless of weather conditions. Outdoor sports activities probably played a subordinate role in this cohort. In Germany, 67% of resettlers did not engage in regular physical activity according to a survey . In general, we lack reliable information regarding NMSC incidence in the Union of Soviet Socialist Republics (USSR). Although cancer registration is available since seventies  most data is not accessible and not available for ethnic Germans.
Slightly more than half of the ethnic German immigrants completed vocational training in their countries of origin in the agricultural sector or in other skilled trades, which are often practiced outdoors. On the other hand, a relatively large number of ethnic German women have higher educational qualifications, which are presumably more likely to be practiced indoors (29% versus 30% of women without a migrant background) . It can be noted that a European style of dress was also propagated and maintained in Islamic regions such as Kazakhstan . Furthermore, it can be assumed that the dangers of excessive UV exposure were largely unknown in the Soviet population and thus preventive measures were neglected [33, 34].
For non-UV-exposed skin areas, no differences in incidence were observed between resettlers and the general German population, suggesting that there are no other risk factors for resettlers. The observed convergence of disease incidence over time could be partially explained by medical underuse in the country of origin and direct access to medical care in Germany after immigration. However, a survey showed that despite direct access to the German health care system, resettlers tend not to participate in offered preventive and screening examinations [35, 36]. Studies have shown that cancer and cardiovascular disease rates of migrants adapt to rates of the host country [37,38,39].
The strengths of our study include the representative resettler cohort with an observation period of 18 years and complete follow-up for more than 95%, as well as the high quality of the Saarland Cancer Registry data [40,41,42]. However, we want to highlight that cancer registry data reflect the number of diagnosed cases and not necessarily the true incidence in a population. Therefore, NMSC incidence might be underestimated in particular before the introduction of skin cancer screening .
In contrast, the classification according to UV exposure represents a limitation, as this could only be approximated using tumour location. Concentrated in the first years of observation, in approximately 10% of the diagnoses, the tumour location was indicated as unknown (ICD-9: 173.9). A further classification into strongly, moderately, weakly and or UV unexposed locations was also waived with in this study due to the limited number of observations. The lack of individual UV exposure also hinders the observation of differences due to gender and fashion. However, viewed over a lifetime, it is predominantly the head and neck area that is exposed to UV radiation [6, 16]. Lacking individual information such as details on the region of origin, occupation and leisure time activity should also be noted.
Further, our analyses do not take in account the length of stay in Germany. However, immigration pattern of resettler show that the vast majority immigrated between 1990 and 1995 leading to high correlation of calendar year and length of stay.
Finally, we did not calculate ASR for resettler cohort in addition to the indirect SIR due to the relatively low number of cases.
In summary, we were able to show that resettlers from the former Soviet Union carried an increased risk of developing non-melanoma skin cancer. Based on the distribution of the tumour sites, it can be assumed that a stronger UV exposure in the countries of origin contributed significantly to the increased risk. The combination of increased risk and possible underuse due to non-participation in screening and early detection programs, may result in an increased risk profile. Future studies should include the period after the introduction of skin cancer screening to show whether specific services are needed for the group of resettlers.
Availability of data and materials
Data of this study are not open access, but we encourage other researchers to contact us and apply for data access based on collaborating projects. Please, contact Volker Winkler (email@example.com) or Evgenia Markeeva-Ilisevic (E.Markeeva@stud.uni-heidelberg.de) to apply for possible collaborations.
Age-standardized incidence rates
Basal cell carcinoma
International Classification of Disease for Oncology 2nd Revision
Non-melanoma skin cancer
Squamous cell carcinoma
Standardized incidence ratios
Kaatsch P, Spix C, Katalinic A, Hentschel S, Luttmann S, Waldeyer-Sauerland M, et al. Bericht zum Krebsgeschehen in Deutschland 2016. Berlin: Robert Koch Institut; 2016.
Gesellschaft der epidemiologischen Krebsregister in Deutschland und Zentrum für Krebsregisterdaten im Robert Koch-Institut. Krebs in Deutschland für 2013/2014 Berlin 2017.
Brantsch KD, Meisner C, Schonfisch B, Trilling B, Wehner-Caroli J, Rocken M, et al. Analysis of risk factors determining prognosis of cutaneous squamous-cell carcinoma: a prospective study. Lancet Oncol. 2008;9(8):713–20.
El Ghissassi F, Baan R, Straif K, Grosse Y, Secretan B, Bouvard V, et al. A review of human carcinogens–part D: radiation. Lancet Oncol. 2009;10(8):751–2.
Gallagher RP, Hill GB, Bajdik CD, Fincham S, Coldman AJ, McLean DI, et al. Sunlight exposure, pigmentary factors, and risk of nonmelanocytic skin cancer I Basal cell carcinoma. Arch Dermatol. 1995;131(2):157–63.
Kricker A, Armstrong BK, English DR, Heenan PJ. A dose-response curve for sun exposure and basal cell carcinoma. Int J Cancer. 1995;60(4):482–8.
Kricker A, Armstrong BK, English DR, Heenan PJ. Does intermittent sun exposure cause basal cell carcinoma? a case-control study in Western Australia. Int J Cancer. 1995;60(4):489–94.
Rosso S, Zanetti R, Martinez C, Tormo MJ, Schraub S, Sancho-Garnier H, et al. The multicentre south European study “Helios”. II: Different sun exposure patterns in the aetiology of basal cell and squamous cell carcinomas of the skin. Br J Cancer. 1996;73(11):1447–54.
Statistisches Bundesamt. Pressemitteilung Nr. 463 vom 1. Oktober 2021 2021 Available from: https://www.destatis.de/DE/Presse/Pressemitteilungen/2021/10/PD21_463_125.html;jsessionid=BE2B078C0CA8809DAA732736FA9D80FC.live711.
Konar Ö, Kreienbrink A, Gieloff A, Rühl S: Migrationsbericht der Bundesregierung 2016/2017. In. Edited by Bundesministerium des Innern. Berlin; 2019.
Worbs S, Bund E, Kohls M, von Babka Gostomski C. (Spät-)Aussiedler in Deutschland. Eine Analyse aktueller Daten und Forschungsergebnisse. Nürnberg: Bundesamt für Migration und Flüchtlinge; 2013.
Winkler V, Holleczek B, Stegmaier C, Becher H. Cancer incidence in ethnic German migrants from the former soviet union in comparison to the host population. Cancer Epidemiol. 2014;38(1):22–7.
Lindblad A, Kaucher S, Jaehn P, Kajüter H, Holleczek B, Lissner L, et al. The incidence of intestinal gastric cancer among resettlers in Germany-do resettlers remain at an elevated risk in comparison to the general population? Int J Environ Res Public Health. 2020;17(24):9215.
Winkler V, Kaucher S, Deckert A, Leier V, Holleczek B, Meisinger C, et al. Aussiedler Mortality (AMOR): cohort studies on ethnic German migrants from the Former Soviet Union. BMJ Open. 2019;9(2):e024865.
Winkler V. Specific aspects of the health profile in ethnic German migrants from the Former Soviet Union. Heidelberg: Heidelberg University; 2008.
Raasch B, Maclennan R, Wronski I, Robertson I. Body site specific incidence of basal and squamous cell carcinoma in an exposed population, Townsville Australia. Mutat Res. 1998;422(1):101–6.
Statistisches Bundesamt. Bevölkerung: Bundesländer, Stichtag, Altersjahre (table number 12411–0012) Wiesbaden: Statistisches Bundesamt; 2020 [Available from: https://www-genesis.destatis.de/genesis//online?operation=table&code=12411-0012&bypass=true&levelindex=1&levelid=1600172106780#abreadcrumb.
Fay MP, Feuer EJ. Confidence intervals for directly standardized rates: a method based on the gamma distribution. Stat Med. 1997;16(7):791–801.
Breslow NE, Day NE. Rates and rate standardization. In: Cancer IAfRo, editor. Statistical methods in cancer research: volume II-the design and analysis of cohort studies. Lyon: IARC Scientific Publications; 1987. p. 48–79.
McLoone P, McLoone P, Imanbayev K, Norval M. The incidence and body site of skin cancers in the population groups of Astana, Kazakhstan. Health Science Reports. 2018;1(7):e51.
CIA's Office of Public Affairs. The world factbook explore all countries: Kazakhstan Washington, DC2021 [Available from: https://www.cia.gov/the-world-factbook/countries/kazakhstan.
Kazhydromed. Monthly newsletter of the forecasts of the index of ultraviolet radiation: Ministry of ecology geology and natural resources of the Republic of Kazahstan; 2020 Available from: https://www.kazhydromet.kz/en/ecology/ezhenedelnyy-byulleten-prognozov-indeksa-ultrafioletovoy-radiacii.
Wei-Passanese EX, Han J, Lin W, Li T, Laden F, Qureshi AA. Geographical variation in residence and risk of multiple nonmelanoma skin cancers in US women and men. Photochem Photobiol. 2012;88(2):483–9.
Rivas M, Araya MC, Caba F, Rojas E, Calaf GM. Ultraviolet light exposure influences skin cancer in association with latitude. Oncol Rep. 2011;25(4):1153–9.
Fioletov V, Kerr JB, Fergusson A. The UV index: definition, distribution and factors affecting it. Can J Public Health. 2010;101(4):I5-9.
Чyбapoвa HE, Ждaнoвa EЮ. Ультpaфиoлeтoвыe pecypcы пpи яcнoм нeбe нa тeppитopии Poccии. Becтник Mocкoвcкoгo yнивepcитeтa. 2012;5:9–19.
Bundesamt für Strahlenschutz (BfS). Geoportal 2020 Available from: https://www.imis.bfs.de/geoportal/.
Keller S. The puzzle of manual harvest in Uzbekistan: economics, status and labour in the Khrushchev era. Central Asian Survey. 2015;34(3):296–309.
Zanca RG. Life in a Muslim Uzbek village : cotton farming after Communism. Belmont, Calif.: Wadsworth Pub. Co.; 2011.
Kuhrs E, Winkler V, Becher H. Risk factors for cardiovascular and cerebrovascular diseases among ethnic Germans from the former Soviet Union: results of a nested case-control study. BMC Public Health. 2012;12:190.
Karpov AB, Zuev AV, Takhalov RM, Kostrykina EV, Samoilova YUA. Morbidity rate dynamics of malignant epithelial skin neoplasms among the population of an industrial center in Western Siberia. Klinicheskaya Dermatologiya i Venerologiya. 2011;9(6):30–5.
Boden R. Sowjetische Außenpolitik und Islam. Jahrbuch für Historische Kommunismusforschung 2009: 149–62.
Seité S, Del Marmol V, Moyal D, Friedman AJ. Public primary and secondary skin cancer prevention, perceptions and knowledge: an international cross-sectional survey. J Eur Acad Dermatol Venereol. 2017;31(5):815–20.
Boлгин B.H., Coкoлoвa T.B., Cтpaнaдкo E.Ф., Лaмoткин И.A., M.B. C. Клиникo-эпидeмиoлoгичecкиe ocoбeннocти тeчeния бaзaльнo-клeтoчнoгo paкa кoжи y лиц пoжилoгo вoзpacтa Aльмaнax клиничecкoй мeдицины. 2006:28–31.
Aparicio ML, Doring A, Mielck A, Holle R. Differences between Eastern European immigrants of German origin and the rest of the German population in health status, health care use and health behaviour: a comparative study using data from the KORA-Survey 2000. Soz Praventivmed. 2005;50(2):107–18.
Starker A, Hövener C, Rommel A. Utilization of preventive care among migrants and non-migrants in Germany: results from the representative cross-sectional study “German health interview and examination survey for adults (DEGS1).” Arch Public Health. 2021;79(1):86.
Ott JJ, Paltiel AM, Winkler V, Becher H. The impact of duration of residence on cause-specific mortality: a cohort study of migrants from the former soviet union residing in Israel and Germany. Health Place. 2010;16(1):79–84.
Stirbu I, Kunst AE, Vlems FA, Visser O, Bos V, Deville W, et al. Cancer mortality rates among first and second generation migrants in the Netherlands: convergence toward the rates of the native Dutch population. Int J Cancer. 2006;119(11):2665–72.
Gray L, Harding S, Reid A. Evidence of divergence with duration of residence in circulatory disease mortality in migrants to Australia. Eur J Public Health. 2007;17(6):550–4.
Kaatsch P, Spix C, Katalinic A, Hentschel S. Krebs in Deutschland 2007/2008. Robert Koch-Institut; 2012. p. 136.
Brenner H, Stegmaier C, Ziegler H. Estimating completeness of cancer registration in Saarland/Germany with capture-recapture methods. Eur J Cancer. 1994;30(11):1659–63.
Winkler V, Ott JJ, Holleczek B, Stegmaier C, Becher H. Cancer profile of migrants from the former soviet union in Germany: incidence and mortality. Cancer Causes Control. 2009;20(10):1873–9.
Breitbart EW, Waldmann A, Nolte S, Capellaro M, Greinert R, Volkmer B, et al. Systematic skin cancer screening in Northern Germany. J Am Acad Dermatol. 2012;66(2):201–11.
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Markeeva-Ilisevic, E., Holleczek, B., Becher, H. et al. Non-melanoma skin cancer among ethnic German immigrants (resettler) from the former Soviet Union: a cohort study from 1990 to 2007. Arch Public Health 80, 85 (2022). https://doi.org/10.1186/s13690-022-00842-1
- Non-melanoma skin cancer
- Basal cell carcinoma
- Squamous cell carcinoma
- UV radiation