European Journal of Cancer Prevention:
Research Paper: Epidemiology
Cancer incidence among Turkish, Chilean, and North African first-generation immigrants in Sweden compared with residents in the countries of origin and native Swedes
Mousavi, Seyed Mohsena; Sundquist, Janb,c; Hemminki, Karia,b
aDivision of Molecular Genetic Epidemiology, German Cancer Research Center (DKFZ), Heidelberg, Germany
bCenter for Primary Care Research, Lund University, Malmö, Sweden
cStanford Prevention Research Center, Stanford University School of Medicine, Stanford, California, USA
Correspondence to Seyed Mohsen Mousavi, Division of Molecular Genetic Epidemiology, German Cancer Research Center (DKFZ), C050, Im Neuenheimer Feld 580, 69120 Heidelberg, Germany Tel: +49 622 142 1805; fax: +49 622 142 1810; e-mail: firstname.lastname@example.org
Received March 28, 2012
Accepted April 17, 2012
We compared the incidence of cancer among Turkish, Chilean, and North African (NA) first-generation immigrants with residents in their countries of origin and native Swedes. The Swedish Family-Cancer Database was used to calculate age-standardized incidence rates. We compared the age-standardized incidence rates for immigrants with those in the Cancer Incidence in Five Continents report. All-cancer rates were decreased in Turks (men) and Chileans and increased in NAs compared with the residents in their countries of origin. The rates of stomach cancer in Chileans and lung cancer in Turkish men were decreased, whereas Turkish women had an increased rate of lung cancer. Furthermore, the rate of prostate cancer in Turks and NAs and nervous system tumors in NA men and Turkish women were increased. Chileans had higher rates of stomach and testicular cancers and lower rates of colon cancer, nervous system tumors, and non-Hodgkin’s lymphoma compared with Swedes. Higher rates of male lung cancer and female thyroid cancer, and lower rates of male rectal and kidney cancers and nervous system tumors, and female stomach and colon cancers were observed among Turks compared with Swedes. The differences observed in all-cancer rates among immigrants were mostly attributable to decreased rates of stomach and lung cancers or an increased rate of prostate cancer after migration. We observed increased rates of colon, breast, and nervous system cancers after migration, whereas the rates of testicular, kidney and thyroid cancers, and non-Hodgkin’s lymphoma remained unchanged.
A total of 449 population-based cancer registries were in operation in the world by the year 2006 and they covered 21% of the global population (Parkin, 2006). However, the coverage differs regionally, with sparse registration in Asia (8% of the total population) and in Africa (11%). Even the quality of data differs, and when considering only the registries that match the inclusion criteria of the Cancer Incidence in Five Continents of IARC (CI5, latest volume IX from year 2007), the coverage shrinks (Curado et al., 2007; Ferlay et al., 2010). No more than 8% of the world population is covered, including only 4% of Asians and 1% of Africans. However, another window into the variations in cancer incidence may be immigrants who have entered a new country during adulthood (Parkin and Khlat, 1996; Hemminki et al., 2002, 2010a). Their cancer incidence tends to deviate from that in the host country, usually toward the rates in their country of origin, given that data are available from C15 or from extrapolated data assembled in GLOBOCAN (Ferlay et al., 2010).
Many immigrant groups in countries such as Sweden originate from regions with no cancer registration, and, hence, their cancer rates in the host country may provide rough estimates of the indigenous cancer rates (Parkin and Khlat, 1996). As an example of a successful estimation, we reported in 2002 that Chilean immigrants in Sweden had testicular cancer rates matching those in Danish immigrants and Danish natives, known to be among the highest in the world (Hemminki et al., 2002). Chile had no cancer registration but when the first regional rates were published in C15 in 2007, the high rates in Chile were confirmed. Our previous studies have shown, for example, high rates of liver and nasopharyngeal cancers in Southeast Asians and North Africans (NAs; Hemminki et al., 2010b; Mousavi et al., 2010d). The advantage of using incidence rates in the host country is that they are based on a uniform cancer registration system, not distinguishing natives and immigrants. The caveat is that immigrants are always a selected population whose cancer rates may deviate from the virtual mean rates in the country of origin (Parkin and Khlat, 1996).
In Sweden, immigrants account for some 15% of the population and they originate from almost all parts of the world (Hemminki et al., 2010a). The present aim was to compare the incidence of cancer in immigrants with the rates in their countries of origin and in Sweden. While selecting the immigrant populations for study, we considered the numbers of expected cancer cases, availability of population-based incidence data in the country of origin, and expected large differences in incidence compared with that among Swedes. Many European immigrant groups fulfill the first two conditions but not the third one, except in some special cases such as testicular cancer, which shows a high incidence among Danish immigrants comparable to that in their native counterparts and in contrast to that in Finnish immigrants and natives, who show a low incidence (Arnold et al., 2010; Hemminki et al., 2010c). Three immigrant groups fulfilled all the criteria: Turkish, covered by two cancer registries, Chileans, covered by one cancer registry, and NAs, covered by cancer registries in Algeria, Egypt, and Tunisia.
Participants and methods
We used the 2010 version of the Swedish Family-Cancer Database (FCD), which is a sub-dataset of the MigMed database run by the Center for Primary Health Care Research at Lund University. The FCD contains information from multigenerational registries, national censuses, the Swedish Cancer Registry, and death notifications (Hemminki et al., 2001, 2010a). Cancer data in the FCD are coded by the seventh revision of the International Classification of Disease (http://www.wolfbane.com/icd/index.html).
Native Swedes were defined as those who, along with their parents, were born in Sweden. First-generation immigrants were defined as those who were born in Turkey, Chile, or NA whose parents were not identified in the database. NA immigrants were classified as “Moroccans” and “other NAs” in the FCD. According to the FCD the populations were as follows: Turks (N=39 240), Chileans (16 358), and NAs (18 285). The available population-based dataset in the CI5 report covered Antalya (total population=1 392 172; year of cancer registry=1998–2002) and Izmir (3 353 446; 1998–2002), Turkey; Valdivia, Chile (632 394; 1998–2002); Setif, Algeria (1 365 488; 1998–2002); Gharbiah, Egypt (3 665 524; 1999–2002); and Sousse, Tunisia (494 800; 1998–2002; Curado et al., 2007).
The follow-up in the FCD covered the years 1988–2008, which overlapped with those in C15, 1998–2002. The start of the follow-up was defined as birth year, the date of immigration, or 1 January 1988, whichever was the latest. The end of the follow-up was defined as the date of cancer diagnosis, death or emigration, end of the last year of presence for the census, or the closing date of our study, 31 December 2008, whichever was the earliest.
We calculated age-standardized and sex-standardized incidence rates (ASRs per 100 000 person-years of the population at risk) for different types of cancers. The world population was used for standardization, as it is applied in CI5. The ASRs were adjusted by age (5-year bands), period (10-year bands from 1988 to 2008), and sex. The confidence interval (95% CI) for the ASRs was calculated by a Poisson approximation of the binomial variance of the age-specific incidence rate (Dos Santos Silva, 1999). Rate ratios (RRs) were calculated by dividing the ASRs in immigrants by the ASRs in native Swedes. The 95% confidence interval (CI) for the RRs was calculated by an approximate standard error for the logarithm of the RR (Dos Santos Silva, 1999). We presented cancers with a significant RR and at least 10 expected cases in one of the immigrant groups: stomach (immigrants=Chileans; RR=2.60), colon (Chileans; 0.39), rectum (Turks; 0.52), lung (Turks; 1.76), breast (Turks; 0.46), endometrium (Turks; 0.31), prostate (Turks; 0.50), testis (Chileans; 2.69), kidney (Turks; 0.56), nervous system tumors (Chileans; 0.46), thyroid (Turks; 2.38), and non-Hodgkin’s lymphoma (NHL; Chileans; 0.46). We compared the ASRs of Turkish, Chilean, and NA immigrants with those of the residents in their countries of origin on the basis of the CI5 report and with those of the native Swedes on the basis of the FCD. Nonoverlapping ASRs of immigrants compared with ASRs of residents in their countries of origin and Swedes were considered to show significant differences. The SAS software version 9.2 was used for the data analysis (SAS Institute Inc., Cary, North Carolina, USA).
We found 552 male and 374 female cancer cases in Turkish, 353 and 354 cases in Chilean, and 252 and 99 cases in NA immigrants, and 316 681 and 290 816 cases in Swedes, respectively (Table 1). Turkish men (ASR=190.0) had decreased all-cancer rates compared with the residents in Izmir (213.6), whereas Turkish women (130.7) showed no significant differences in the rates of cancer compared with residents in Antalya (125.8) and Izmir (124.5). Chilean men (183.8) and women (151.2) had decreased rates compared with Valdivia-resident men (242.4) and women (203.7). The NA men (ASR=190.9) and women (136.7) had increased rates compared with Algerian men (94.0) and women (84.7). Overall, all immigrants had lower rates compared with Swedish men (253.3) and women (230.1).
The ASRs for the selected cancers among men are shown in Tables 2 and 3. A decrease in the rate of stomach cancer was found among Chileans (17.6) compared with the residents in Valdivia (43.1). The NAs (13.5) had an increased rate of colon cancer compared with Algerians (3.0) and Egyptians (4.2). We found a decrease in the rate of lung cancer among Turks (35.2) compared with the residents in Izmir (74.5). All immigrants, except for Chileans, had an increased rate of prostate cancer (ASR ranging from 37.4 to 69.9) compared with the residents in countries of origin. Furthermore, NAs (8.7) had an increased rate of nervous system tumors compared with Algerians (0.7). Higher rates of lung cancer among Turks and testicular cancer among Chileans, and lower rates of colon cancer and NHL among Chileans and rectal and kidney cancers among Turks were observed compared with Swedes. We also found that Turks and Chileans had lower rates of nervous system tumors compared with Swedes.
Tables 4 and 5 show the ASRs for the selected cancers among women. A decrease in the rate of stomach cancer was found among Chileans (7.6) compared with the residents in Valdivia (16.0). Turks (10.7) had an increased rate of lung cancer compared with the residents in Antalya (4.8) and Izmir (5.9). An increased rate of breast cancer was observed among NAs (54.0) compared with Algerian (18.8) and Tunisian (29.8) residents. Furthermore, Turks (8.5) had an increased rate of nervous system tumors compared with the residents in Izmir (3.1). We also found lower rates of stomach cancer in Turks and Chileans, colorectal cancer in Turks, lung cancer in Chileans, breast cancer in Turks and NAs, and nervous system tumors in Chileans compared with Swedes, whereas a higher rate of thyroid cancer was observed in Turks.
Our study compared the rates of selected cancers among three populations: hosts (Swedes), immigrants, and residents (Turks, Chileans, and NAs). By applying a 95% CI for the ASRs, our study was able to find significant differences in the rates of cancer after migration. However, a small number of cases (specifically among NA immigrants), the short follow-up period, lack of information on the birth province of immigrants, and defining only two groups of NA immigrants in the FCD were some limitations of our study. Furthermore, the population-based cancer incidence data in Turkey, Chile, and NA countries were based on regional data and only covered less than 7% of the total population (Zanetti et al., 2010; Population Data, 2011). For example, the incidence rates for Turkey were obtained from Izmir and Antalya. Both of these areas are in West Turkey and their rates may not apply to all parts of Turkey.
Classical immigrant studies on cancers have shown that the rate of cancer among immigrants reaches the level of the host country within the first or the second generation (Parkin and Khlat, 1996). Unexpectedly, our data showed that Turkish immigrant men had a rate comparable to that of Antalya residents and a decreased rate compared with the residents in Izmir, whereas the Turkish immigrant women showed no differences in the rates of cancer compared with the residents in Antalya and Izmir. However, their cancer rates did not reach the level of Swedes during the period of study. Furthermore, we found a 30% decrease in the all-cancer rate among Chilean immigrants compared with the residents in Valdivia (Curado et al., 2007). Such a decrease in the cancer rate was reported among Chinese immigrant men in Canada compared with the residents of Shanghai (Luo et al., 2004). In general, NA residents have all-cancer rates ranging from one-third to half of those among Swedes (The National Board of Health and Welfare, 2009; Zanetti et al., 2010), whereas our data showed that the rates among NA immigrants were from half to two-thirds of those among the Swedes. This finding indicates an estimated increase of 30–50% in the cancer rate among NA immigrants compared with the NA residents. The analyses by cancer sites (Tables 2–5) show that the observed decreased all-cancer rates in Turkish (men) and Chilean immigrants were mostly attributable to the decreased rates of lung and stomach cancers, whereas the increased rate of NAs was mostly attributable to the increased rate in prostate cancer.
Previous studies have shown a decreased rate of stomach cancer after immigration, particularly among immigrants from high-risk countries. For example, Japanese immigrants to the USA and Chinese immigrants to Canada had up to 80% decrease in the rate of cancer compared with the residents in Japan and China (Kamineni et al., 1999; Luo et al., 2004). Furthermore, an ∼50% decrease in the rate was reported among Korean–Americans compared with the Korean residents (Lee et al., 2007). We also found an ∼50% decrease in the rate of stomach cancer among Chilean immigrants compared with the residents in Valdivia. In addition, the higher rate of stomach cancer among Chilean resident men and the lower rate among Turkish resident women compared with the Swedes remained unchanged after immigration. Hence, our result shows that the risk for stomach cancer may be modified after migration (Nilsson et al., 1993; Moradi et al., 1998; Kamineni et al., 1999; Suerbaum and Michetti, 2002; Ferlay et al., 2010; Mousavi et al., 2011d).
Studies on Korean immigrants to the USA and Iranian immigrants to Sweden showed an increased risk for colorectal cancer compared with that among the residents in Korea and Iran (Lee et al., 2007; Mousavi et al., 2010b). Our data also showed an increased rate of colon cancer among NA men compared with the residents in Algeria and Tunisia. These findings suggest a shift in the original lifestyle to a Westernized lifestyle. However, we found that the lower rates of colon cancer among Chilean men, rectal cancer among Turkish men, and colorectal cancer among Turkish women compared with the Swedes remained lower after immigration. This finding indicates that the preservation of original habits might be the main environmental exposure influencing the risk for colorectal cancer among these immigrants. Thus, immigrants might show different behaviors in lifestyle changes after migration, which depends on the age at immigration (Mousavi et al., 2011a).
Previous studies have found a decreased rate of 20–30% in lung cancer among male Chinese immigrants to Canada and among Japanese immigrants to the USA (Kamineni et al., 1999; Luo et al., 2004). We also found a 50% decreased rate of cancer among Turkish men compared with the residents in Izmir. In addition, our data showed that the higher lung cancer rate among Turkish resident men compared with the Swedes remained higher after migration. Although information on smoking was unavailable in our database, this observation may be indicative of a modification in the prevalence of smoking after migration (World Health Organization, 2002; Nierkens et al., 2006; Mousavi et al., 2011c). We also found that Turkish women had an increased rate of lung cancer compared with the residents in Antalya and Izmir. This finding might be because of a selection bias in the migrant population (Parkin and Khlat, 1996). However, integration within the culture of a host country and changes in smoking habits, for example Swedish women smoke as much as men, could partly account for the differences observed in the rates of lung cancer among Turkish immigrant women (World Health Organization, 2002; Delander et al., 2005; Blomstedt et al., 2007).
We found that the rate of prostate cancer among Turks and NAs was up to seven times greater than the rate for residents in Turkey and NA countries (Beiki et al., 2009). We have previously reported a rate ratio of 4.1 for prostate cancer among Iranian immigrants in Sweden compared with the Iranian residents (Mousavi et al., 2010b). In agreement with our findings, one study showed that the rate of prostate cancer among US Koreans was 3.5 times greater than that for the Korean residents (Lee et al., 2007). In contrast, another study reported that Asian Americans born outside the USA had a rate of prostate cancer similar to that in the population of their birthplace (Cook et al., 1999). We also found that the rate of prostate cancer in Chilean immigrants was not significantly different from that in the residents in Valdivia. Although we believe that immigrants may not be a representative sample of the total population of a country of origin, exposures to new environment and changes in lifestyles, more precisely food habits, may explain our observation (Kocturk-Runefors, 1990; Cook et al., 1999; Palloni and Morenoff, 2001; Boyle and Levin, 2008). Although there is controversy with regard to the prostate cancer screening program, the lack of this program in the countries of origin and improvement in diagnostic efforts using the prostate-specific antigen in Sweden since the late 1990s are probable reasons for these differences (Berglund et al., 2005; Kjellman et al., 2009).
We found an increased rate of breast cancer among NAs compared with Algerian and Tunisian residents, whereas Turks and Chileans showed no differences compared with the residents in Turkey and Valdivia. Previous studies have reported an increased rate of breast cancer among Iranian immigrants to Sweden and Korean immigrants to the USA compared with the residents in Iran and Korea (Lee et al., 2007; Mousavi et al., 2010b). Overall, all immigrants, except for Moroccans, had lower rates of breast cancer than the Swedes. Differences in population aging, reproductive factors, lifestyles, a positive family history, and diagnostic facilities could explain the differences observed in the rates of breast cancer among immigrants, hosts, and residents (Lagerlund et al., 2002; Andreeva et al., 2007; Hemminki et al., 2008; Hemminki et al., 2011a, 2011b, 2011c).
Our data showed that the higher rate of testicular cancer among Chilean residents compared with Swedes remained higher after migration. On the basis of our previous publication on first-generation and second-generation immigrants, early environmental exposures play a major role in the etiology of testicular cancer (Hemminki et al., 2010c). We also found that the lower rate of kidney cancer among Turkish residents compared with the Swedes remained lower after migration. However, further studies are required to define the role of a new environment in the etiology of this disease (Uitewaal et al., 2004; Boyle and Levin, 2008; Mousavi et al., 2010c).
We found an increased rate of nervous system tumors among NA men and Turkish women compared with the residents in their countries of origin. However, those immigrants showed no significant differences in the rate compared with Swedes. As in our previous report, the genetic background and/or childhood exposures may play a role in the etiology of this disease rather than exposures after migration (Mousavi et al., 2011b). We found no change in the rate of thyroid cancer and NHL after migration. We have reported previously that an iodine imbalance or childhood exposure to ionizing radiation may be associated with a high risk of thyroid cancer among Asian immigrants (Mousavi et al., 2010a). NHL shows a large international variation in the rates (Curado et al., 2007). For example, the variation in the rate of NHL was about three-fold among NA residents (Table 3). Although our knowledge of the potential risk factors for NHL is limited, current evidence points to immunological factors in childhood, which might remain unchanged after migration (Hemminki and Li, 2002; Boyle and Levin, 2008).
The change in the all-cancer rate after immigration is varied among different immigrant groups. The differences observed in all-cancer rates among immigrants were mostly attributable to decreased rates for stomach and lung cancers or an increased rate of prostate cancer after migration. We observed increased rates of colon, breast, and nervous system cancers after migration, whereas the rates of testicular, kidney, and thyroid cancers, and NHL, remained unchanged. The observed differences in the rates of colorectal, breast, testicular, kidney, nervous system, thyroid cancers, and NHL between immigrants and hosts may confirm the role of early childhood exposures or the preservation of original lifestyles in the etiology of these diseases.
This study was supported by Deutsche Krebshilfe, the Swedish Cancer Society, the Swedish Council for Working Life and Social Research, the Swedish Research Council, and EU FP7/2007–2013 grant 260715. The results of this project were presented at the EUNAM meeting in Ferrara, Italy, on 8 September 2011.
Conflicts of interest
There are no conflicts of interest.
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cancer; Chile; immigrants; incidence; North Africa; residents; Sweden; Turkey
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