Morbidity and mortality in gynecological cancers among first- and second-generation immigrants in Sweden

Morbidity and mortality in gynecological cancers amongfirst- and second-generation immigrants in Sweden

Seyed Mohsen Mousavi1,2, Kristina Sundquist3 and Kari Hemminki1,3

1 Division of Molecular Genetic Epidemiology, German Cancer Research Center (DKFZ), Heidelberg, Germany2 Cancer Institute, Tehran University of Medical Sciences, Tehran, Iran3 Center for Primary Health Care Research, Lund University, Malmo, Sweden

We studied the effect of new environment on the risk in and mortality of gynecological cancers in first- and second-generation

immigrants in Sweden. We used the nationwide Swedish Family-Cancer Database to calculate standardized incidence/mortality

ratios (SIRs/SMRs) of cervical, endometrial and ovarian cancers among immigrants in comparison to the native Swedes. Risk

of cervical cancer increased among first-generation immigrants with Danish (SIR 5 1.64), Norwegian (1.33), former

Yugoslavian (1.21) and East European (1.35) origins, whereas this risk decreased among Finns (0.88) and Asians (SIRs varies

from 0.11 in Iranians to 0.54 in East Asians). Risk of endometrial (SIRs varies from 0.28 in Africans to 0.86 in Finns) and

ovarian (SIRs varies from 0.23 in Chileans to 0.82 in Finns) cancers decreased in first-generation immigrants. The overall

gynecological cancer risk for the second-generation immigrants, independent of the birth region, was almost similar to that

obtained for the first generations. The birth region-specific SMRs of gynecological cancers in first- and second-generation

immigrants co-varied with the SIRs. Risk of gynecological cancers among the first-generation immigrants is similar to that in

their original countries, except for cervical cancer among Africans and endometrial cancer among North Americans and East

Europeans. Our findings show that risk and mortality of gynecological cancers observed in the first-generation immigrants

remain in the second generation. We conclude that the risk and protective factors of gynecological cancers are preserved

upon immigration and through generations, suggesting a role for behavioral factors or familial aggregation in the etiology of

these diseases.

The distribution of gynecological cancers is widely affected bygeographical variations. The highest rates for cervical cancer(>30/100,000) have been reported from the South and WestAfrica and Latin America, while the lowest rates (<5/100,000)are reported from Northeast Africa and West Asia. NorthAmericans and East Europeans have the highest endometrialcancer rates (>15/100,000), whereas Africans have the lowestrates (<2/100,000). The highest ovarian cancer rates (>10/100,000) have been reported from Eastern Europe, and thelowest from Africa (<2/100,000).1 Cervical, endometrial andovarian cancer incidence rates are 7.4, 13.8 and 9.0 per100,000 person years in Sweden, respectively.2 The world mor-

tality to incidence ratios of gynecological cancers are 55–61%.3

Human papillomavirus (HPV) infection, obesity and repro-ductive factors are the most important environmental risk fac-tors of gynecological cancers.4 However, a familial aggregationfor gynecological cancers has also been reported.5–9

There are limited and controversial epidemiological dataconcerning whether immigration may cause significantchanges in the risk and mortality of gynecological cancers.10–17

For example, a persistent high cervical cancer risk wasreported among North African immigrants in Israel,15

whereas, in contrast, a study on Korean immigrants in theUnited States showed a decreased risk of cervical and anincreased risk of endometrial cancers.17 It has been reportedthat East African immigrants in England and Wales experi-enced decreased cervical and ovarian cancer mortality ratescompared to English and Welsh natives.11 Contrarily, a studyon Japanese immigrants in Brazil showed increased mortalityof cervical and endometrial cancers.12 Surprisingly, anotherstudy of immigrants in Australia and Canada showed anincreased ovarian cancer mortality amongst the majority ofimmigrant groups.13

Sweden is an excellent country to study cancer in immi-grants because of its uniform cancer registration, health caresystem and a large number of immigrants (>1.8 millionimmigrants).18 Previous studies on immigrants in Sweden,based on data from the Swedish Cancer Registry, reportedrisk of gynecological cancers only among foreign-born

Key words: cancer, cervix, endometrial, immigrants, mortality, ovary,

risk, Sweden

Grant sponsors: The German Cancer Research Center (DKFZ),

Deutsche Krebshilfe, The Swedish Cancer Society, The Swedish

Council for Working Life and Social Research, EU FP7/2007-2013

Grant 260715

DOI: 10.1002/ijc.26395

History: Received 17 Jun 2011; Accepted 22 Aug 2011; Online 26

Aug 2011

Correspondence to: Seyed Mohsen Mousavi, German Cancer

Research Center (DKFZ), Division of Molecular Genetic

Epidemiology, C050, Im Neuenheimer Feld 580, 69120 Heidelberg,

Germany, Tel.: þ49-6221-42-1805, Fax: þ49-6221-42-1810,

E-mail: [email protected]

Epidemiology

Int. J. Cancer: 000, 000–000 (2011) VC 2011 UICC

International Journal of Cancer

IJC

women between 1968 and 200419,20 and our previous reportson first- and second-generation immigrants to Sweden alsosuffered from a small number of gynecological cancercases.21,22 Furthermore, to our knowledge, there are no stud-ies investigating changes in mortality rate of gynecologicalcancer in second-generation immigrants. Therefore in thepresent report, we focused on the risk and mortality of gyne-cological cancers in the first- and second-generation immi-grants in Sweden using a longer follow-up time (from 1958to 2008), a larger number of cases (N ¼ 8,015) and a largernumber of deaths (2,010) in comparison with previousstudies.19–22

Material and MethodsWe used the updated version of the Swedish Family-CancerDatabase (FCD), which is a sub-dataset of the MigMed data-base run by Center for Primary Health Care Research atLund University. The FCD contains information from themultigenerational registries, the national censuses, the Swed-ish Cancer Registry and the death notifications.23 Data oncancers in FCD is tagged with codes from the seventh revi-sion of the International Classification of Disease (ICD-7)(http://www.wolfbane.com/icd/index.html) including codes171, 172 and 175 for cervical, endometrial (corpus uteri) andovarian cancers, respectively. The Swedish Cancer Registry isbased on compulsory reports of diagnosed cancer cases, witha nearly 100% national coverage.2 The underlying cause ofdeath is available from the Swedish Cause of Death Registryon the basis of ICD classification of diseases; however ICDcodes varied through the last decades. Death codes for cervi-cal, endometrial, and ovarian cancers were 171, 172/174, and175 from 1958 to 1968 (ICD-7), followed by 180, 182, and183 from 1969 to 1996 (ICD-8/9) and then C53, C54/C55,and C56 (ICD-10), respectively.

The FCD provides data on the birth country and the dateof immigration to Sweden for each individual.23 We definedthe first-generation immigrants as those who were born out-side Sweden with no identified parents in the database,whereas information on parents was available for the secondgeneration in the database. Second-generation immigrants arenormally classified as being born in the host country. Forthis study, we defined second-generation immigrants, how-ever, as Swedish born or foreign born. The country of birthwas classified based on the geographical regions and the pop-ulation size. As about one third of gynecological cancer casesand related deaths events in second-generation immigrantswere among those who were originally from Nordic coun-tries, second-generation immigrants were classified into twosubgroups of ‘‘selected Nordic countries’’ and ‘‘other immi-grants’’ based on incidence and mortality of gynecologicalcancers in the NORDCAN database to maximize the possiblenumber of cancer cases and deaths.24 Classification of sec-ond-generation immigrants provided the maximum numberof cases and deaths in relation with the mother’s country ofbirth.

Like our previous studies,25–27 we calculated standardizedincidence ratios (SIRs) and standardized mortality ratios(SMRs) as the ratio of observed to expected number of casesand deaths. The expected number of cases and deaths werecalculated in 5-year age groups and in 10-year intervals forthe years between 1958 and 2008. The native Swedes wereselected as the reference population.28 Additionally, the ageat first-child birth (<20, 20–24, 25–29, 30þ) and the numberof childbirths (0, 1, 2, 3, 4þ) were included in the adjustmentto eliminate the effect of reproductive factors on gynecologi-cal cancer risk.4,29 The effect of time in Sweden was testedfor two groups based on the time since immigration <20years and �20 years.23 Confidence intervals (95% CI) werecalculated, assuming a Poisson distribution. SAS software ver-sion 9.2 was used for the data analysis (SAS Institute, Cary,NC).

ResultsThe FCD included 20,575 cases and 5,885 deaths of cervicalcancer in Swedes, and 1,943 cases and 517 deaths in first-generation immigrants (Table 1). The median ages at immi-gration and diagnosis of cervical cancer were 33 and 47years. In comparison with Swedes, a lower cervical cancerrisk was observed among Iranians (SIR ¼ 0.11), Iraqis (0.19)and Asian Arabs (0.28), while Danes (1.64), Norwegians(1.33), former Yugoslavians (1.21) and other East Europeans(1.35) had a higher risk. An increased cervical cancer mortal-ity was seen among Danes (SMR ¼ 1.77) followed by Norwe-gians (1.58).

We observed 31,947 cases and 4,755 deaths of endometrialcancer in Swedes, and 2,582 cases and 320 deaths in first-generation immigrants. The median ages at immigration anddiagnosis of endometrial cancer were 31 and 62 years. Therisk of endometrial cancer was decreased almost in all immi-grant groups (SIRs ranging from 0.28 in Africans to 0.86 inFinns). Notably, first-generation immigrants had neither anincreased endometrial cancer risk nor a significant differencein the mortality of this cancer.

Our data also included 25,464 cases and 13,894 deaths ofovarian cancer in Swedes, and 2,003 cases and 1,020 deathsin first-generation immigrants. The median ages at immigra-tion and diagnosis of ovarian cancer were 31 and 57 years.The risk of ovarian cancer was decreased almost in all immi-grant groups (SIRs ranging from 0.23 in Chileans to 0.82 inFinns). The ovarian cancer mortality was decreased amongFins (SMR ¼ 0.81), former Yugoslavians (0.69), Turks (0.25),Iranians (0.19), Chileans (0.23) and Latin Americans (0.41).

The gynecological cancer risk among first-generationimmigrants did not significantly vary after adjusting forreproductive factors (data not shown). For example, adecreased cervical cancer risk was observed among Iranians(0.11), Iraqis (0.21) and Asian Arabs (0.28), whereas Danes(1.63), Norwegians (1.32) and other East Europeans (1.35)had an increased risk. SIR for endometrial and ovarian can-cers was decreased almost in all immigrant groups ranging

Epidemiology

2 Gynecological cancers in immigrants


Table

1.Personyears

atrisk,ageatim

migration/d

iagnosis,

standardizedincidence/m

ortality

ratios(SIRs/SMRs*)forcervical,endometrialandovariancancers

amongfirst-generationim

migrants

toSwedenfrom

1958

to2008

Birth

region

Numberof

cohort

follow-up

Person

years

Cervicalcancer

Endometrialcancer

Ovariancancer

Median

ageat

NSIR

395%

CI

Death

SMR3

95%

CI

Median

ageat

NSIR

95%

CI

Death

SMR

95%

CI

Median

ageat

NSIR

95%

CI

Death

SMR

95%

CI

I1DX2

IDX

IDX

Sweden

4,460,352

157,306,953

NA

48.2

20,575

1.00

5,885

1.00

NA

63.4

31,947

1.00

4,755

1.00

NA

59.9

25,464

1.00

13,894

1.00

Finland

138,864

3,872,574

29

48.7

566

0.88

0.81

0.95

164

0.93

0.79

1.08

26

61.3

956

0.86

0.80

0.91

120

0.88

0.73

1.06

27

57.9

699

0.82

0.76

0.88

354

0.81

0.73

0.90

Denmark

30,238

610,178

33

46.9

193

1.64

1.42

1.89

61

1.77

1.36

2.28

31

60.8

189

0.93

0.80

1.07

18

0.64

0.38

1.02

34

59.8

169

1.12

0.96

1.30

93

1.12

0.90

1.37

Norway

41,213

953,966

34

49.7

253

1.33

1.17

1.51

90

1.58

1.27

1.94

35

64.1

274

0.84

0.75

0.95

43

0.91

0.66

1.23

34

56.8

257

1.06

0.93

1.20

139

1.02

0.86

1.21

Baltic

country

11,838

238,834

40

57.7

70

1.20

0.93

1.52

28

1.37

0.91

1.97

39

67.9

110

1.06

0.87

1.28

17

0.92

0.53

1.47

39

62

55

0.70

0.53

0.92

40

0.83

0.59

1.13

Germ

any

33,780

826,262

32

47.7

151

0.96

0.82

1.13

38

0.80

0.57

1.10

27

64.5

277

0.94

0.83

1.06

38

0.93

0.66

1.28

31

60.4

195

0.92

0.79

1.05

114

0.96

0.79

1.16

Benelux

6,310

95,020

32

41.4

21

1.29

0.80

1.97

30.72

0.15

2.11

29

62.8

23

0.95

0.60

1.42

51.60

0.52

3.73

35

70

14

0.74

0.41

1.25

90.92

0.42

1.75

UK

9,421

146,286

28

43.7

18

0.77

0.46

1.22

40.74

0.20

1.90

38

62.8

20

0.66

0.41

1.03

20.55

0.07

1.97

35

56.1

27

1.07

0.70

1.55

16

1.30

0.74

2.11

Poland

33,840

601,244

33

45

107

1.16

0.95

1.40

18

0.85

0.50

1.34

35

56.8

120

0.92

0.76

1.10

14

0.96

0.53

1.61

34

53.3

107

0.99

0.81

1.20

52

1.01

0.75

1.32

Russia

13,007

187,542

35

49

24

0.71

0.46

1.06

60.65

0.24

1.41

39

67.3

42

0.81

0.59

1.10

50.65

0.21

1.53

37

52

27

0.66

0.44

0.96

19

0.86

0.52

1.35

Form

erYugoslavia

54,394

941,555

34

42.8

157

1.21

1.03

1.41

26

0.96

0.62

1.40

37

60.3

159

0.79

0.67

0.92

14

0.68

0.37

1.14

34

53

124

0.79

0.66

0.94

50

0.69

0.51

0.91

OtherEastern

Europe

22,878

443,348

33

45.3

100

1.35

1.10

1.64

27

1.40

0.93

2.04

34

61.3

107

0.88

0.72

1.07

11

0.74

0.37

1.32

32

55.3

86

0.92

0.74

1.14

46

0.96

0.70

1.28

Greece

7,574

160,208

32

48.5

70.31

0.12

0.63

029

56.3

16

0.43

0.25

0.70

20.53

0.06

1.93

33

48.5

10

0.34

0.16

0.62

10.07

0.00

0.41

Southern

Europe

14,184

216,558

34

44.3

28

0.80

0.53

1.15

60.71

0.26

1.54

30

62.8

36

0.72

0.50

0.99

71.15

0.46

2.37

31

57

31

0.78

0.53

1.11

15

0.76

0.42

1.25

OtherEurope

7,021

108,064

31

47

14

0.97

0.53

1.63

51.83

0.59

4.26

32

61.1

10

0.65

0.31

1.20

21.33

0.16

4.81

39

46.6

12

0.86

0.44

1.50

30.50

0.10

1.47

Turkey

13,727

246,084

31

47.8

19

0.60

0.36

0.94

30.48

0.10

1.40

38

56.6

14

0.33

0.18

0.55

20.44

0.05

1.58

30

44.6

90.26

0.12

0.49

40.25

0.07

0.65

Iraq

31,510

248,326

42

45.4

60.19

0.07

0.42

047

58

33

1.13

0.78

1.59

31.03

0.21

3.01

42

46.8

15

0.59

0.33

0.97

60.59

0.21

1.27

Iran

22,339

339,636

42

51.8

50.11

0.04

0.27

10.14

0.00

0.78

41

53.8

26

0.60

0.39

0.87

10.24

0.01

1.36

35

48

18

0.45

0.27

0.71

30.19

0.04

0.54

AsianArabcountries

16,684

234,482

49

53.7

80.28

0.12

0.55

036

59

15

0.54

0.30

0.90

10.38

0.01

2.10

45

52.5

16

0.64

0.37

1.04

60.59

0.22

1.29

IndianSubcontinent

16,692

295,747

39

48.8

90.47

0.21

0.89

51.84

0.60

4.29

33

67.1

90.68

0.31

1.30

21.60

0.19

5.79

27

39.6

90.61

0.28

1.16

20.38

0.05

1.37

Southeast

Asia

34,109

381,444

29

40.9

59

1.31

1.00

1.69

71.09

0.44

2.25

33

50.5

24

0.82

0.52

1.22

20.78

0.09

2.80

30

44.2

20

0.62

0.38

0.96

70.60

0.24

1.23

East

Asia

24,814

344,387

31

36.3

15

0.54

0.30

0.89

40.94

0.25

2.40

38

52.5

13

0.58

0.31

0.99

031

45

20

0.90

0.55

1.39

50.57

0.18

1.32

OtherAsia

9,397

59,734

42

44.2

70.97

0.39

2.00

11.00

0.03

5.60

48

54.6

50.80

0.26

1.87

040

41.3

91.63

0.75

3.10

20.92

0.11

3.33

NorthAmerica

13,759

227,553

43

57.8

37

0.84

0.59

1.15

12

0.92

0.48

1.61

41

65.7

63

0.96

0.74

1.23

10

0.94

0.45

1.73

39

62.1

41

0.78

0.56

1.06

21

0.71

0.44

1.08

Chile

10,698

220,360

35

49.1

33

1.21

0.83

1.70

40.77

0.21

1.98

38

54.6

18

0.51

0.30

0.81

034

49.9

70.23

0.09

0.48

30.23

0.05

0.68

LatinAmerica

20,827

302,516

32

40.7

24

0.74

0.47

1.10

20.36

0.04

1.30

36

62.8

15

0.48

0.27

0.79

10.33

0.01

1.87

31

53.8

15

0.50

0.28

0.83

50.41

0.13

0.96

Africa

35,473

393,319

29

38

12

0.26

0.13

0.45

20.32

0.04

1.15

31

54.8

80.28

0.12

0.54

021

43.1

11

0.35

0.18

0.63

50.44

0.14

1.03

Allim

migrants

674,591

12,695,227

33

47.3

1,943

0.97

0.93

1.02

517

1.02

0.94

1.11

31

61.6

2,582

0.84

0.81

0.87

320

0.83

0.74

0.92

31

56.8

2,003

0.83

0.80

0.87

1,020

0.83

0.78

0.88

*SignificantSIRsandSMRs:

95%

CIdoesnotinclude1.00.Th

eSIRswere

adjustedby5-yearagegroupsandtimeperiods(10-yearbandsfrom

1958to

2008).

1I¼

immigration.2DX¼

diagnosis.

3Bold

types:

95%

CIdoesnot

include1.00.

from 0.26 in Africans to 0.87 in Finns and from 0.23 in Chil-eans to 0.82 in Finns.

Furthermore, no significant trend was observed for gyne-cological cancer risk in first-generation immigrants withregard to time in Sweden (Table 2). For example, anincreased cervical cancer risk was observed among Norwe-gians who had resided in Sweden for less than 20 years (SIR¼ 1.35), whereas the risk remained high among those whohad resided for more than 20 years (1.29). The same patternwas seen for endometrial and ovarian cancer risk trend bythe variable time in Sweden.

We analyzed cancer risk and mortality for daughters ofthe first-generation immigrants by taking daughters’ andmothers’ birth region into account and also by including agegroups, time periods, age at first-child birth and number ofchildbirths in the adjustment. Table 3 shows the results for‘‘selected Nordic countries’’ and ‘‘other immigrants.’’ Theoverall gynecological cancer risk and mortalities for ‘‘daugh-ters,’’ independent to the birth region, co-varied withobserved risk and mortality in ‘‘mothers.’’ Daughters of Dan-ish and Norwegian immigrants had a cervical cancer risk of1.27 when born in Sweden compared with a risk of 1.44 fortheir mothers. Cervical cancer risk decreased among foreign-born (0.77) and Swedish-born (0.86) daughters of immigrantsfrom other origin are in line with a risk of 0.88 among moth-ers from other origin. Daughters of Foreign-born Nordic(0.86) and other Swedish-born immigrants (0.88) had adecreased risk of endometrial cancer in line with thedecreased risk in their mothers. Risk of ovarian cancer signif-icantly decreased only among Swedish-born daughters incomparison with that in their mothers. There was no signifi-cant difference in mortality of cervical and endometrial can-cers among any group of daughters, however Finnish-born(0.71) and Swedish-born (0.70) daughters had a decrease inmortality in line with the decreased mortality of Finnishmothers (0.81).

DiscussionThe large number of immigrant women (>900,000) from anationwide database and a 50-year follow-up (12.7 millionperson years),23 allowed us to estimate population-based riskand mortality of gynecological cancers for first- and second-generation immigrants to Sweden. Our findings on first-gen-eration immigrants showed an increase in cervical cancer riskamong Danes, Norwegians, former Yugoslavians and EastEuropeans, while Finns and most Asians experienceddecreased risk. The risk of endometrial and ovarian cancerswas decreased in almost all first-generation immigrants. Ourdata showed that the overall risk of gynecological cancers infirst-generation immigrants remained the same in the secondgenerations, however the birth region-specific SMRs of gyne-cological cancers co-varied with the SIRs.

Although, cervical cancer is proportionately the mostcommon cancer among women in many African countries,1

surprisingly, in first-generation Africans it significantly

showed a decreased risk in our study. However, it has beenreported that cervical cancer might be linked to a low-socioe-conomic status,30 SIRs were not adjusted for socioeconomicstatus in our study because a major proportion of immigrantscame to Sweden after 1990 (about 620,000 immigrants); andthat was the latest date that the socioeconomic data wasavailable from the FCD.

Risk of cervical cancer has been reported to be high inDenmark.24,31 This study is in line with our previous reporton Nordic immigrants to Sweden32 that showed an increasedrisk of cervical cancer among Danish first-generation immi-grants, which is suggested to be due to persistent sexualbehaviors upon migration. Differences in the prevalence ofHPV infection between the population of origin and the hostpopulation may explain the role of sexual behaviors.22 Forinstance, the prevalence of HPV in Danish residents withnormal cytology of cervix had been reported to be somethree times higher than in Swedes.33

Southeast Asian immigrants in the United States havebeen shown to have a nearly fivefold increased risk of cervi-cal cancer compared to Hispanic women.34 We also found anincreased risk, but not significant (SIR ¼ 1.31; 95% CI ¼1.00–1.69) for Southeast Asian first-generation immigrants.Asians (except those from Southeast) had, however, decreasedcervical cancer risk. This is in agreement with a study con-ducted on Middle Eastern immigrants in California35 and isalso consistent with the report of Cancer Incidence in FiveContinents (CI5).1 Our findings are in line with previousstudies, all suggest that risk of cervical cancer among first-generation immigrants follows the risk of birth country.1

North Americans and East Europeans have a higher endo-metrial cancer rates than Swedes.1 Unexpectedly, we foundno increased risk among first-generation immigrants fromthese areas. North American and East European countriesharbor multiethnic and multicultural societies and as immi-grants are self-selected groups, therefore samples from suchcountries might not represent the population of country oforigin.36 However, the observed risk of endometrial canceramong other first-generation immigrants in our study is inagreement with the report of CI5.1

It has been observed that the age at immigration wasalmost three decades earlier than the age at diagnosis of en-dometrial cancer. In addition, the decreased risk of endome-trial cancer among first-generation immigrants was independ-ent with time in Sweden. Hence, our findings of endometrialcancer risk among first-generation immigrants, which do notconverge to the risk in the host country, even after around30 years residency in Sweden, may indicate that protectivefactors against endometrial cancer have been preserved uponmigration.

It has been found that obesity is associated with anincreased risk of endometrial cancer through increasingperipheral production of estrogen.37 A previous study onimmigrants in Sweden showed that Finnish, former Yugosla-vian and Southern European women had a significantly higher

Epidemiology



Table

2.Standardizedincidence

ratios(SIRs*)forcervical,endometrialandovariancancers

amongfirst-generationim

migrants

toSwedenbylength

ofstay

Cervicalcancer

Endometrialcancer

Ovariancancer

Length

ofstay<

20

years

Length

ofstay�

20

years

Length

ofstay<

20

years

Length

ofstay�

20

years

Length

ofstay<

20

years

Length

ofstay�

20

years

Birth

region

NSIR

95%

CI

NSIR

95%

CI

NSIR

95%

CI

NSIR

95%

CI

NSIR

95%

CI

NSIR

95%

CI

Finland

304

0.85

0.76

0.95

262

0.91

0.80

1.02

141

0.78

0.66

0.92

815

0.87

0.81

0.93

192

0.84

0.73

0.97

507

0.81

0.74

0.89

Denmark

134

1.85

1.55

2.20

59

1.31

1.00

1.69

54

1.18

0.89

1.54

135

0.86

0.72

1.02

54

1.09

0.82

1.43

115

1.14

0.94

1.36

Norway

160

1.35

1.15

1.57

93

1.29

1.05

1.59

69

0.83

0.64

1.05

205

0.85

0.74

0.97

103

1.22

1.00

1.48

154

0.97

0.82

1.14

Baltic

country

41

1.11

0.79

1.50

29

1.36

0.91

1.95

30

0.95

0.64

1.35

80

1.11

0.88

1.38

21

0.69

0.43

1.06

34

0.71

0.49

1.00

Germ

any

104

1.20

0.98

1.45

47

0.67

0.49

0.90

40

0.80

0.57

1.08

238

0.97

0.85

1.10

61

1.10

0.84

1.41

135

0.86

0.72

1.02

Benelux

19

1.70

1.02

2.65

20.39

0.05

1.41

50.84

0.27

1.97

18

0.98

0.58

1.55

30.43

0.09

1.25

11

0.93

0.47

1.67

UK

11

0.63

0.32

1.13

71.17

0.47

2.41

60.59

0.22

1.29

14

0.70

0.38

1.18

14

1.17

0.64

1.96

13

0.98

0.52

1.67

Poland

82

1.21

0.96

1.50

25

1.02

0.66

1.51

44

0.87

0.63

1.17

76

0.95

0.75

1.19

56

1.02

0.77

1.32

51

0.96

0.72

1.26

Russia

19

0.76

0.46

1.18

50.58

0.19

1.34

13

0.58

0.31

0.98

29

1.00

0.67

1.44

18

0.84

0.50

1.32

90.47

0.21

0.89

Form

erYugoslavia

129

1.28

1.07

1.52

28

0.96

0.64

1.39

76

0.73

0.58

0.92

83

0.84

0.67

1.05

79

0.85

0.67

1.06

45

0.70

0.51

0.93

OtherEastern

Europe

70

1.38

1.07

1.74

30

1.29

0.87

1.84

32

0.83

0.57

1.17

75

0.91

0.71

1.14

42

1.05

0.76

1.42

44

0.83

0.60

1.11

Greece

50.33

0.11

0.77

20.26

0.03

0.95

30.31

0.06

0.92

13

0.47

0.25

0.80

60.50

0.18

1.10

40.23

0.06

0.58

Southern

Europe

22

0.89

0.56

1.35

60.57

0.21

1.24

10

0.80

0.39

1.48

26

0.69

0.45

1.01

11

0.72

0.36

1.29

20

0.82

0.50

1.27

OtherEurope

10

0.88

0.42

1.62

41.30

0.35

3.32

10.17

0.00

0.97

90.94

0.43

1.78

10

1.32

0.64

2.44

20.31

0.04

1.12

Turkey

13

0.54

0.29

0.92

60.80

0.29

1.75

60.28

0.10

0.61

80.37

0.16

0.73

70.33

0.13

0.69

20.14

0.02

0.51

Iraq

60.20

0.07

0.43

030

1.08

0.73

1.55

31.92

0.40

5.60

14

0.57

0.31

0.96

10.90

0.02

4.99

Iran

50.12

0.04

0.29

021

0.55

0.34

0.84

50.89

0.29

2.07

14

0.39

0.21

0.66

40.94

0.26

2.41

AsianArabcountries

60.23

0.08

0.50

20.77

0.09

2.80

80.38

0.16

0.74

71.11

0.45

2.29

15

0.73

0.41

1.20

10.23

0.01

1.27

IndianSubcontinent

60.44

0.16

0.97

30.53

0.11

1.54

09

1.48

0.68

2.80

70.75

0.30

1.55

20.37

0.04

1.33

Southeast

Asia

52

1.30

0.97

1.70

71.41

0.57

2.90

16

0.85

0.49

1.38

80.76

0.33

1.49

15

0.62

0.34

1.01

50.64

0.21

1.50

East

Asia

11

0.57

0.28

1.02

40.48

0.13

1.22

70.59

0.24

1.22

60.57

0.21

1.24

13

0.93

0.49

1.59

70.85

0.34

1.76

OtherAsia

70.98

0.39

2.02

05

0.84

0.27

1.96

09

1.69

0.77

3.20

0

NorthAmerica

27

0.82

0.54

1.20

10

0.86

0.41

1.59

21

0.86

0.53

1.31

42

1.02

0.73

1.37

18

0.71

0.42

1.12

23

0.85

0.54

1.27

Chile

27

1.18

0.78

1.72

61.36

0.50

2.97

12

0.54

0.28

0.95

60.46

0.17

1.01

60.27

0.10

0.60

10.12

0.00

0.65

LatinAmerica

21

0.78

0.49

1.20

30.53

0.11

1.55

70.41

0.17

0.85

80.55

0.24

1.09

80.41

0.18

0.80

70.69

0.28

1.43

Africa

12

0.29

0.15

0.50

04

0.20

0.06

0.52

40.43

0.12

1.09

50.21

0.07

0.49

60.83

0.31

1.81

Allim

migrants

1,303

0.99

0.93

1.04

640

0.95

0.88

1.03

661

0.75

0.69

0.81

1,922

0.88

0.84

0.92

801

0.84

0.78

0.90

1,203

0.83

0.78

0.88

Bold

types:

95%

CIdoesnotinclude1.00.

*SignificantSIRsandSMRs:

95%


eSIRswere

adjustedby5-yearagegroupsandtimeperiods(10-yearbandsfrom

1958to

2008).

Epidemiology

Mousavi et al. 5


Table

3.Standardizedincidence/m

ortality

ratios(SIRs/SMRs*)forcervical,endometrialandovariancancers

amongim

migrantmothers

anddaughters

1to

Sweden

Incidence

Mortality

Mother

Foreign-born

daughter

Swedish-born

daughter

Mother

Foreign-born

daughter

Swedish-born

daughter

Birth

region

NSIR

95%

CI

NSIR

95%

CI

NSIR

95%

CI

NSMR

95%

CI

NSMR

95%

CI

NSMR

95%

CI

Cervicalcancer

SelectedNordic

countries2

446

1.44

1.31

1.58

29

1.09

0.73

1.27

128

1.27

1.06

1.36

151

1.64

1.39

1.93

41.20

0.33

1.95

15

1.21

0.67

1.51

Otherim

migrants

1,497

0.88

0.84

0.93

166

0.77

0.66

0.82

266

0.86

0.76

0.91

366

0.89

0.80

0.98

27

1.06

0.70

1.25

35

1.02

0.71

1.17

Allim

migrants

1,943

0.97

0.93

1.01

197

0.81

0.70

0.86

394

0.96

0.87

1.00

517

1.02

0.94

1.12

31

1.07

0.73

1.25

50

1.07

0.79

1.20

Endometrialcancer

SelectedNordic

countries

1,419

0.87

0.83

0.92

83

0.86

0.69

0.94

164

0.95

0.81

1.01

181

0.87

0.74

1.00

70.87

0.35

1.23

13

0.91

0.49

1.17

Otherim

migrants

1,164

0.77

0.73

0.82

89

1.22

0.98

1.33

79

0.88

0.70

0.96

139

0.74

0.62

0.87

81.24

0.54

1.72

50.66

0.21

1.01

Allim

migrants

2,583

0.82

0.79

0.86

173

1.00

0.86

1.06

243

0.93

0.81

0.97

320

0.81

0.72

0.90

15

1.01

0.56

1.27

18

0.83

0.49

1.01

Ovariancancer

SelectedNordic

countries

699

0.82

0.76

0.89

85

1.02

0.82

1.11

96

0.78

0.63

0.84

354

0.81

0.73

0.90

20

0.71

0.43

0.86

26

0.70

0.46

0.83

Otherim

migrants

1,305

0.80

0.76

0.85

126

1.14

0.95

1.22

168

0.83

0.71

0.89

666

0.81

0.75

0.87

32

0.92

0.63

1.07

50

0.77

0.57

0.87

Allim

migrants

2,004

0.81

0.77

0.85

216

1.10

0.96

1.16

264

0.81

0.72

0.85

1,020

0.81

0.76

0.86

54

0.84

0.63

0.95

76

0.75

0.59

0.82

Bold

types:

95%

CIdoesnotinclude1.00.

*SignificantSIRs:

95%


eSIRswere

adjustedby5-yearagegroups,

timeperiods(10-yearbandsfrom

1958to

2008),ageatfirst-ch

ildbirth

(<20,20–24,25–29,30þ)

andnumberofch

ildbirth

(0,1,2,3,4þ)

.1Im

migrantmothers

anddaughters:First-andsecond-generationim

migrants.2SelectedNordic

countries:

Cervicalcancer:Denmark

andNorway.

Endometrialcancer:Finland,Denmark

andNorway.

Ovariancancer:Finland.

Epidemiology



percentage of body fat compared to their Swedish peers,38

whereas we observed a decreased risk of endometrial canceramong the immigrants. However, it must be noticed that dataon obesity was unavailable to us. Obesity is associated withreproductive factors to some extent, although the risk of endo-metrial cancer did not significantly vary when it was adjustedfor reproductive factors.

Use of hormone replacement therapy (HRT) during 1970smight be an explanation for the higher risk of endometrialcancer in Swedish women compared to first-generationimmigrants.39 A similar finding was reported in our previousstudy on breast cancer risk,40 which has almost similar pre-dispositions suggesting that HRT use might be a contributingfactor to relatively higher risk of endometrial cancer inSwedes than that in first-generation immigrants.

Overall, the observed decrease in risk of ovarian canceramong first-generation immigrants is in agreement with thereport of CI5 suggesting that the risk of ovarian cancer infirst-generation immigrants followed the risk in birth coun-tries.1 Hence, one may conclude that protective factorsagainst ovarian cancer have been conserved upon immigra-tion. Our data showed that first-generation African immi-grants had a decreased risk of ovarian cancer which is inconsistence with a study conducted in England and Wales(from 1970 to 1985).11 This might be due to high fertilityrates in the African population and also partly due to low-fertility rate in the host population.4 However, when weadjusted the risk for reproductive factors, there was nochange in ovarian cancer risk. Additionally, our previousstudy on breast cancer risk with almost similar risk factors toovarian cancer, showed a decreased risk of breast cancer inAfrican immigrants.41

Geographical variations in mortality rate of cervical cancerin Nordic countries are mainly caused by two major factorsincluding sexual behaviors and well-organized cervical cancerscreening program.42 The observed increased mortality ofcervical cancer among Danes and Norwegians in our study isconsistent with the report of NORDCAN24 that shows first, abirth cohort effect of first-generation immigrants who movedbefore 1970s, second, a large variation in the attendance rateby county and third, a difference in participation rate by eth-nicities in the cervical cancer screening program in Swe-den.43,44 For instance, cervical cancer screening attendancerate was reported to vary from 85% in Vasterbotten to 25%in Malmo.43 Furthermore, a similar study on cervical cancer

screening program in Sweden from 1993 to 2005 showed aparticipation rate of 47% for Danes and 44% for Norwegianscompared to 62% in native Swedes.44

We found no significant difference mortality for endome-trial cancer that may be due to small numbers of endometrialcancer deaths available. Our data showed a decreased mortal-ity of ovarian cancer among first-generation immigrants,which is inconsistent with a study of immigrants in Australiaand Canada. This study reported a shift in mortality of ovar-ian cancer to the level of host countries, particularly in immi-grants originating from low-risk countries.13 Incomplete datafrom birth countries, a small number of deaths, a limited pe-riod of follow-up (1984–1988) and aggregated immigrantgroups (first- and second-generation immigrants were com-bined) may explain differences between the findings of thesetwo studies.

Our data showed that the observed risk and mortality ofgynecological cancers among first-generation immigrantsremained the same in the second generations, independentto the birth region of the second-generation immigrants,although some studies showed that integration in the cultureof host country, i.e., ‘‘acculturation’’ might partly accountfor the observed changes in risk of cancers among the sec-ond-generation immigrants.45,46 Our findings suggested thatthe risk and/or protective factors of gynecological cancers,mainly behavioral factors, might not vary upon generations.It is possible that familial aggregation of gynecological can-cer play a role in causation of these cancers after immigra-tion.5–9

In summary, the risk of gynecological cancers in first-gen-eration immigrants follows the risk of cancer in the countryof origin, except for cervical cancer among Africans and en-dometrial cancer among North Americans and East Euro-peans. The risk and mortality of cervical, endometrial andovarian cancers in first-generation immigrants remained thesame in the second generation, which may indicate that riskand protective factors of these cancers, mainly behavioral fac-tors, are preserved upon immigration and through the gener-ations or present a role of familial aggregation in the etiologyof these diseases. Further studies are required to confirm therole of behavioral factors or familial aggregation in the etiol-ogy of gynecological cancers.

AcknowledgementThe authors thankMiss Parisa Roudgari for English proofreading.

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Epidemiology



Documents

Morbidity and mortality in gynecological cancers among first- and second-generation immigrants in Sweden