Cancer risks in second-generation immigrants to Sweden



We used the nationwide Swedish Family-Cancer Database to analyze cancer risks in Sweden-born descendants of immigrants from European and North American countries. Our study included close to 600,000 0–66-year-old descendants of an immigrant father or mother. We calculated standardized incidence ratios (SIRs) and 95% confidence intervals (CIs) for 17 cancer sites using native Swedes as a reference. All cancer was marginally below the Swedish incidence in offspring of immigrant origin. Decreased SIRs were observed for breast cancer among Norwegian descendants, melanoma among descendants of Hungarian fathers and ovarian and bladder cancer among descendents of Finnish mothers, all consistent with the difference in cancer incidence between Swedes and the indigenous populations. Cervical cancer was increased in daughters of Danish men, whereas thyroid cancer and non-Hodgkin's lymphoma were in excess in offspring of parents of Yugoslav and Asian descent. Even these results agreed with the high incidence rates in parents compared to Swedes, except that for non-Hodgkin's lymphoma other explanations are needed; these may be related to immune malfunction. Comparison of the results between the first- and the second-generation immigrants suggest that the first 2 decades of life are important in setting the pattern for cancer development in subsequent life. Birth in Sweden sets the Swedish pattern for cancer incidence, irrespective of the nationality of descent, while entering Sweden in the 20s is already too late to influence the environmentally imprinted program for the cancer destiny. © 2002 Wiley-Liss, Inc.

The classic migrant studies on Japanese immigrants to the USA and on European immigrants to Australia have been strong arguments for the predominant environmental etiology in cancer.1, 2 Since then, numerous other migrant studies have appeared from these geographic areas, from Israel, South America and some European countries.3–10 Common to these studies has been, with a few exceptions, that the incidence of cancer has moved to the level of the new host population in 1 or 2 generations.11–14 Although these studies on practically all main cancers and decreasing and increasing rates, leave little doubt about the overall importance of changing environmental factors in cancer, there are some features in migrant studies that have deserved limited attention, including movement of people between approximately the same socioeconomic backgrounds and between small geographic distances. Such movements, typical of inter-European migration, may entail relatively fast cultural mixing with the recipient population and uninterrupted contacts to the native population.15 Migrant studies may eventually be used to answer the questions about population differences in genetic susceptibility because of the differential distribution of genotypes in populations.16, 17 However, as such effects, if present, are likely to be small, their demonstration would be particularly demanding.

In Sweden, close to 1 million people, 10% of the population, is foreign born, having immigrated from a number of countries at various periods of time, reflecting epochs in world history. The numbers of the Sweden-born offspring of immigrants are shown in Table I. The Nordic countries (Denmark, Finland, Iceland, Norway and Sweden; Iceland will not be discussed further because of its small population) have had an open job market for decades and no limitations for travel or settlement within their borders. Sweden has been the largest economy in the region and has attracted a number of Nordic immigrants over the years. A large influx of Finns took place in the 1960s, making them the largest immigrant group. Sweden remained outside the Second World War and many Balts and Germans immigrated before and after the War. Hungarian and Czechoslovakian political turmoils caused waves of immigration from these countries to Sweden. Yugoslavs came in large numbers in the 1970s. The most recent immigration includes Chileans, Asians and Africans, but their Sweden-born offspring have barely reached adult age and only Asians are included in our study.

Table I. Population, Person-Years and SIRs for All Cancer in Descendants by Parental Birth Country
Parental birth countryBy father's birth countryBy mother's birth countryCompatriot parents
PopulationPerson-yearsMean follow-upOSIR95% CIPopulationPerson-yearsMean follow-upOSIR95% CIPopulationPerson-yearsMean follow-upOSIR95% CI
  1. Bold type: 95% CI does not include 1.00.

Nordic countries230,1394,809,695211,6460.940.90–0.99300,4286,858,674232,7580.950.92–0.99111,6932,193,362205770.890.82–0.96
Eastern Europe98,4451,892,991196880.980.91–1.0691,4431,598,578176181.000.92–1.0855,158888,094163161.000.89–1.11
Western Europe91,8331,891,747216560.980.91–1.0669,0271,586,968236510.990.92–1.0721,903439,089201330.890.74–1.05
North America13,644295,851222140.990.86–1.1411,693274,001232311.000.87–1.135814,409821.150.11–4.22
All descendants580,62210,199,154183,4600.960.92–0.99597,57111,322,294194,4730.970.94–0.99856,80016,639,284196,5520.970.94–0.99

We use the nationwide Swedish Family-Cancer Database, in which the birth country of each individual is recorded, to study cancer incidence among the Sweden-born offspring of immigrants from Europe and North America. It is of interest to compare data from second-generation immigrants to their parents, which is presented in the preceding article.18


The Swedish Family-Cancer Database was initially created in the middle of the 1990s by linking an administrative family register on all Swedish families to the Swedish Cancer Registry.19, 20 For each child, there are data on both parents at the time of birth. Each person has been assigned a unique technical identification number (which is different from the national identification number, “personal number”), allowing construction of families, for example, through the mother. The Database includes all persons born in Sweden after 1931 with their biological parents, totaling more than 10.2 million individuals. It was updated in the beginning of 2001 to include cancers from the nationwide Swedish Cancer Registry from 1958–1998. The Database is organized in 3.2 million families, with parents and offspring.

The completeness of cancer registration in the 1970s has been estimated to be more than 95% and is now considered to be close to 100%. The percentage of cytologically or histologically verified cases of gastric cancers has been close to 100%.21 The Swedish Cancer Registry is based on compulsory notification of cases.21 A 4-digit diagnostic code according to the 7th revision of the International Classification of Diseases (ICD-7) was used. The following ICD-7 codes were pooled: “leukemia,” codes 204–207 (leukemias), 208 (polycythemia vera) and 209 (myelofibrosis).

The parental information was classified according to the country of birth and the incidence of cancer was calculated for their 0–66-year-old offspring. “Eastern Europe” included the Czech Republic and all countries east of it; however, Greece was included with “Western Europe.” All tumor incidence rates were based on the data in the Family-Cancer Database. Follow-up was started at birth or January 1, 1961, whichever came latest. Follow-up was terminated on death, emigration or the closing date of the study, December 31, 1998. Standardized incidence ratios (SIRs) were calculated as the ratio of observed (O) to expected (E) number of cases. The expected numbers were calculated from 5-year-age-, sex-, 10-year-period-, region- (3 large cities, south Sweden and the rest) and tumor type-specific standard incidence rates. The incidence for all offspring in the Database was the standard rate. Confidence intervals (95% CI) were calculated assuming a Poisson distribution. Because the initial sex-specific analysis showed no gender-specific effects, data are given for both sexes together.


The offspring of the Swedish natives constituted by far the largest group of offspring in our study, about 6 million individuals and close to 160 million person-years (Table I). The offspring of Finns was the largest group of immigrant descent, including 213,000 persons with a Finnish mother. The number of offspring was about equal among immigrants from Eastern and Western Europe. Among them, Yugoslavs and Germans were the largest nationalities, each with more than 30,000 Sweden-born offspring. The total number of offspring born to compatriot marriages is also shown; close to 90,000 offspring from Finnish and 23,000 offspring from Yugoslav families were the largest groups. The total number of cancers recorded was 3,460 by fathers' and 4,473 by mothers' birth countries. The mean follow-up time gives an idea of the time since immigration of the families. The overall cancer rates were decreased for offspring of immigrant fathers (SIR 0.96), mothers (0.97) and compatriots (0.97). Among particular nationalities, offspring of the Finnish origin and of Norwegian compatriots showed decreased SIRs. There were no significantly increased risks. Below, we show the results on specific cancer sites with the country of origin. Offspring of compatriot marriages are only commented on if the SIRs are significant; for most cancer sites the numbers of cases were few.

Table II shows SIRs for offspring sex-specific cancers of breast, cervix and testis. Breast cancer was decreased among offspring of Norwegian mothers and increased among offspring of Rumanian fathers (SIR 4.15). Cervical cancer was increased in offspring of Danish fathers (1.75) or of 2 Danish parents (SIR 2.45, n = 12, 95% CI 1.26–4.29). Testis cancer was not increased in any of the immigrant groups; Denmark has the highest incidence in the world, but only sons of compatriot Danes showed any tendency for increase (SIR 1.79, n = 10, 0.85–3.30).

Table II. SIR for Breast, Cervix and Testis Cancer in Descendants by Parental Birth Country
Parental birth countryBreastCervixTestis
By father's birth countryBy mother's birth countryBy father's birth countryBy mother's birth countryBy father's birth countryBy mother's birth country
  1. Bold type: 95% CI does not include 1.00.

Nordic countries2220.910.80–1.044230.900.81–0.99991.200.97–1.461511.060.90–1.24940.950.77–1.171340.910.76–1.07
Eastern Europe960.960.78–1.171001.050.86–1.28290.890.59–1.27260.960.63–1.41431.130.82–1.52280.950.63–1.37
Western Europe931.070.86–1.311131.130.93–1.35301.020.69–1.45240.730.47–1.09380.990.70–1.35421.150.83–1.56
North America461.010.74–1.35551.090.82–1.42101.120.53–2.07111.160.58–2.0960.950.34–2.09111.830.91–3.28
All descendants4700.970.89–1.066990.960.89–1.041681.070.91–1.242141.000.87–1.141870.980.85–1.132210.980.85–1.12

Risks for colorectal and lung cancer and for melanoma are shown in Table III. Neither colorectal nor lung cancer showed changes in offspring of immigrants. Offspring of Hungarian fathers were protected against melanoma (SIR 0.32). Offspring of all foreign born fathers and mothers had decreased risk of melanoma with SIRs of 0.88 and 0.87, respectively.

Table III. SIR for Colorectal, Lung and Melanoma Cancer in Descendants by Parental Birth Country
Parental birth countryColorectalLungMelanoma
By father's birth countryBy mother's birth countryBy father's birth countryBy mother's birth countryBy father's birth countryBy mother's birth country
  1. Bold type: 95% CI does not include 1.00.

Nordic countries800.940.75–1.171380.910.77–1.08481.280.94–1.70841.120.89–1.391520.900.76–1.062480.900.79–1.02
Eastern Europe240.720.46–1.08240.800.51–1.19161.090.62–1.78120.810.42–1.42590.840.64–1.08510.870.65–1.14
Western Europe320.980.67–1.39381.110.78–1.52120.820.42–1.4480.470.20–0.93530.800.60–1.04560.810.61–1.05
North America161.140.65–1.85241.520.97–2.2691.070.49–2.0570.720.28–1.49251.370.89–2.03190.980.59–1.53
All descendants1590.930.79–1.082280.960.84–1.10871.130.91–1.401110.940.77–1.132940.880.78–0.993740.870.78–0.96

Data on nervous system, thyroid and endocrine tumors are collected in Table IV. Nervous system and nonthyroid endocrine tumors showed no change in offspring. Thyroid cancer was increased among Eastern Europeans, particularly among offspring of Yugoslav parents (SIR 2.70 from father and 3.81 from mother). All of the 8 affected offspring had both parents of Yugoslav origin (SIR 4.99, 2.13–9.89). Two of the offspring were siblings and these and another offspring were diagnosed with a medullary thyroid cancer. In both of these families, the mother also had a thyroid cancer, which were likely to be ascribed to the multiple endocrine neoplasia 2 syndrome. If these 3 hereditary cases were removed from analysis, the risk for thyroid cancer remained significant only for offspring whose both parents were Yugoslav (n = 5, SIR 4.83, 95% CI 1.53–11.37).

Table IV. SIR for Nervous System, Thyroid Gland and Endocrine Glands Cancer in Descendants by Parental Birth Country
Parental birth countryNervous systemThyroid glandEndocrine glands
By father's birth countryBy mother's birth countryBy father's birth countryBy mother's birth countryBy father's birth countryBy mother's birth country
  1. Bold type: 95% CI does not include 1.00.

Nordic countries2170.950.83–1.083310.990.89–1.11511.040.78–1.37911.160.93–1.42520.860.64–1.131081.070.88–1.30
Eastern Europe971.060.86–1.29911.140.92–1.40311.581.07–2.25281.721.14–2.49281.150.77–1.67170.810.47–1.29
Western Europe921.030.83–1.27771.020.81–1.28180.990.59–1.57180.990.59–1.57210.930.57–1.42170.740.43–1.19
North America251.480.95–2.18150.910.51–1.5120.400.04–1.4840.770.20–1.98101.410.67–2.6050.650.21–1.54
All descendants4840.970.89–1.065560.990.91–1.081071.120.92–1.351461.211.02–1.421200.980.81–1.171570.990.84–1.16

The risks of lymphohematopoietic malignancies for the second-generation immigrants are shown in Table V. Non-Hodgkin's lymphoma was increased in offspring of Yugoslav fathers (SIR 2.18), mothers (2.13) and compatriot parents (4.99, n = 8, 2.13–9.89). Offspring of Asian mothers were also at risk (1.74). For Hodgkin's disease or leukemia, no changes were noted.

Table V. SIR for Non-Hodgkin's Lymphoma, Hodgkin's Disease and Leukemia in Descendants by Parental Birth Country
Parental birth countryNon-Hodgkin's lymphomaHodgkin's diseaseLeukemia
By father's birth countryBy mother's birth countryBy father's birth countryBy mother's birth countryBy father's birth countryBy mother's birth country
  1. Bold type: 95% CI does not include 1.00.

Nordic countries690.900.70–1.141301.080.90–1.28560.840.64–1.09890.920.74–1.131250.870.73–1.041961.010.88–1.16
Eastern Europe391.260.89–1.72341.250.86–1.75250.960.62–1.42221.070.67–1.62480.810.60–1.08460.870.63–1.16
Western Europe311.030.70–1.46301.110.75–1.59331.260.87–1.77241.070.68–1.59490.860.63–1.13451.050.77–1.41
North America50.610.19–1.4360.690.25–1.5220.500.05–1.8371.870.74–3.8780.870.37–1.7391.090.49–2.08
All descendants1671.010.87–1.182231.130.98–1.281230.930.77–1.111521.010.86–1.193000.880.79–0.993521.000.89–1.11

For the remaining cancer sites, the number of cases from outside the Nordic countries was too small to allow analysis by parental birth country (Table VI). None of the sites (stomach, prostate and kidney) showed significant deviations in SIR. For ovarian and bladder cancer, daughters of Finnish mothers showed SIRs of 0.70 and 0.60, but these were not decreased in compatriot marriages.

Table VI. SIR for Stomach, Ovary, Prostate, Kidney and Urinary Bladder Cancer in Descendants by Parental Birth Region
ParentsBirth regionStomachOvaryProstateKidneyUrinary bladder
  1. Bold type: 95% CI does not include 1.00.

FatherNordic countries161.120.64–1.83450.860.63–1.16181.070.63–1.70441.050.76–1.41250.820.53–1.22
Eastern Europe50.910.29–2.14231.110.70–1.6771.530.60–3.16150.870.49–1.45151.300.73–2.15
Western Europe61.170.42–2.56160.850.48–1.3850.700.22–1.64171.030.60–1.65100.860.41–1.59
North America20.760.07–2.7870.900.36–1.8681.330.57–2.6310.190.00–1.0760.990.36–2.18
All descendants291.030.69–1.48950.920.74–1.13381.080.76–1.48890.910.73–1.12560.910.69–1.19
MotherNordic countries270.970.64–1.41730.780.61–0.98330.910.63–1.28550.820.62–1.07420.720.52–0.97
Eastern Europe40.780.20–2.02150.800.44–1.3250.910.29–2.15191.180.71–1.84121.090.56–1.91
Western Europe81.370.59–2.72150.740.41–1.23101.110.53–2.05151.050.58–1.73151.150.64–1.91
North America41.330.35–3.43131.530.81–2.6240.530.14–1.3850.870.27–2.0471.000.40–2.07
All descendants441.040.76–1.401190.830.69–0.99520.880.66–1.161070.920.75–1.11770.850.67–1.06


The sentinel finding in most migrant studies has been the adjustment of the cancer incidence in migrants to the level of the recipient population in 1 or 2 generations, depending on the rate of acculturation to the host country.12–14 The present results on the mainly inter-European migration not only agreed but also drove the point: The large differences in the first-generation immigrants shown in the preceding article almost completely disappeared in their Sweden-born second generation.18 In the first generation, 96 significant changes in SIR for sex- and country-specific sites were observed among the present nationalities compared to 10 in the present study (we denote “change” as any significant change in SIR for a “group,” i.e., male or female cancer site, counted separately, from a particular country). The fewer significant findings among the second-generation immigrants was not only due to the fewer number of cases but also to a true approach of the SIRs toward unity.

At 4 sites, a decrease of risk was observed: breast cancer (SIR 0.83) in descendants of Norwegian mothers, melanoma (SIR 0.32) in descendants of Hungarian fathers and ovarian (0.70) and bladder (0.60) cancer in descendants of Finnish mothers. All these matched significant protective effects in the first generation, the SIRs being 0.86 for breast cancer in Norwegian women, 0.50 for melanoma in Hungarian men, 0.80 for ovarian cancer and 0.69 for bladder cancer in Finnish immigrant women.18 Although these protective findings at these sites are consistent with some long-lasting environmental or even heritable effects, they are just a fraction of the 52 protective effects noted for the first-generation immigrants. Some remarkable but unfortunate changes have taken place for 18 national sex-specific groups for melanoma and 12 for prostate cancer where protection was observed in the first generation: Protection had disappeared for the second generation, except for Hungarian descendents.

The SIRs were increased for offspring of immigrants at 4 sites: breast cancer (4.15) for daughters of Rumanian men, cervical cancer (1.75) for daughters of Danish men, thyroid cancer in offspring of Yugoslav men (1.58), women (1.72) or compatriots (4.99) and non-Hodgkin's lymphoma in offspring of Yugoslav men (2.18), women (2.13) or compatriots (2.29) and of Asian mothers (1.74). These 6 country- and sex-specific increases can be compared to 44 increases in their parents.18 The second generation has been fortunate to overcome risks from stomach cancer in immigrants from 9 groups and that of lung cancer from 13 groups. The result on breast cancer is probably due to chance because of multiple comparisons. The incidence of cervical cancer is about 2 times higher in Denmark compared to Sweden and the result for Danish descendents may show cultural inheritance.22 For thyroid cancer, we found 2 immigrant families with multiple endocrine neoplasia 2, a highly penetrant condition that is usually recognized in families;23, 24 however, the SIR for thyroid cancer remained elevated even if the 3 affected children from these families were removed from analysis. Thyroid cancer was increased in the first-generation Yugoslav immigrants (SIR 1.64), thus with similar findings between the generations.18 By contrast, the parental data did not explain the consistent increase in non-Hodgkin's lymphoma in descendents of Yugoslav origin. According to the available reference literature, Yugoslavia is a low-risk area for non-Hodgkin's lymphoma.25, 26 Few previous migrant studies have considered lymphomas. However, lymphoma rates have been increased among South Asian migrants to England, including their English-born children and some Jewish groups moving to Israel.6, 27–29 Although the etiology of non-Hodgkin's lymphoma is unknown, it is likely to involve an aberrant immune response that has been linked to population mixing and undefined infections.30–33 Thus second-generation descendents of low-risk areas somehow do not appear to adjust to the high-risk environment of Sweden. This may also be relevant to the increasing incidence trends of non-Hodgkin's lymphoma in affluent countries.21, 34, 35

The main challenge to the current and future immigrant studies is whether it is possible to pinpoint the environmental factors that cause the change, either increasing or decreasing, in the incidence of cancer upon migration. Another challenge is to identify cancer rates that would truly differ between ethnic groups and thus suggest genetic factors predisposing to or protecting from cancer. Although humans are thought be genetically identical to more than 99.9%,36, 37 there are ethnic differences in genotypes that may or may not have an impact on the risk of cancer.16, 17 Such effects may be small and their demonstration would require unbiased epidemiologic studies of high statistical power.13, 14 If a genetic effect was present, it should be strongest in the first generation and in the second-generation offspring from compatriot marriages. The only neoplasms where such an interpretation may be tenable, based on the present data, were melanoma among Hungarian descendants, thyroid cancer among Yugoslav descendants and ovarian cancer among Finnish descendants. Skin pigmentation is a heritable trait associated with melanoma, but for the other sites no genetic hypothesis can be offered. For the majority of malignancies (lung, testicular, prostate, colorectal, nervous system, endocrine, stomach, kidney and bladder cancer, Hodgkin's disease and leukemia), no difference between the second-generation immigrants and native Swedes was found, suggesting that the differences in cancer incidence between Swedes and the indigenous populations are due to environmental effects.

In summary, the combined results of this and the preceding article18 followed the pattern noted for the previous migrant studies on indistinguishable incidence rates in the second-generation immigrant and host populations.13 The 96 sex- and country-specific significant differences among the first-generation immigrants had been reduced to 10 differences in the second generation. Most of these were consistent with the incidence rates in their parents. Comparison of the results between the first and second generations suggest that the first 2 decades of life are important in setting the pattern for cancer development in subsequent life. Birth in Sweden sets the Swedish pattern for cancer incidence, irrespective of the nationality of descent, whereas entering Sweden in the 20s is already too late to influence the environmentally imprinted program for the cancer destiny.


The Family-Cancer Database was created by linking registers maintained at Statistics Sweden and the Swedish Cancer Registry.