Annals of Oncology Advance Access published online on March 5, 2008
Annals of Oncology, doi:10.1093/annonc/mdn025
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
Quantification of changes in breast cancer incidence and mortality since 1990 in 35 countries with Caucasian-majority populations
Data Analysis and Interpretation Group, Epidemiology Methods and Support Group, International Agency for Research on Cancer, Lyon, France
* Correspondence to: Dr P. Autier, International Agency for Research on Cancer, 150 Cours Albert Thomas, F-69372 Lyon Cedex 08, France. Tel: +33-472-73-81-63; Fax: +33-472-73-83-51; E-mail: autierp{at}iarc.fr
 |
Abstract |
|---|
 Top Abstract introductionmethodsresultsdiscussionfundingReferences |
|---|
Background: Since 1985 considerable changes have taken place in the early detection and treatment of breast cancer. We quantified breast cancer trends for 35 countries with populations mainly of European ancestry.
Methods: Incidence data were extracted from cancer registries and mortality data from World Health Organization database. Overall percentage change from 1990 to 2002 was quantified for all ages and for three different age-groups (35–49, 50–69 and 
70 years of age).
Results: The incidence percent change in women of all ages varied from 2.1% in Canada to 54.2% in Lithuania. Main increases in incidence were observed for women 50–69 years old, from 12.4% in Canada until 105.3% in Norway. Decreases in mortality of >20% were observed in nine countries. Mortality decreases were highest in women 35–49 years old and lowest in women 70 years. The magnitude of mortality decrease from 1990 to 2002 was not related to the mortality rate observed in 1990.
Conclusions: While increases in breast cancer incidence mainly concerned women 50 years, decreases in mortality were more marked in women 35–49 years old. Large disparities in changes in mortality rates probably reflect differences in detection of and management of breast cancer.
breast cancer, epidemiology, temporal trends
|
introduction |
|---|
|
TopAbstractintroductionmethodsresultsdiscussionfundingReferences |
|---|
Breast cancer is the most common cause of cancer death in women worldwide [1]. Since 1985 considerable changes in breast cancer detection and management have occurred [2] and end of the 1980s and in the 1990s decreases in breast cancer mortality started to be observed in western Europe, North America and Australia [3].
Periods during which breast cancer incidence or mortality data were available varied appreciably between countries, which made difficult the comparison of changes in incidence or mortality rates between countries. In years 2000s, incidence and mortality data from countries with populations mainly of European ancestry began to be available for relatively similar periods of time since 1990.
This paper quantifies and compares percentage changes in breast cancer incidence and mortality from 1990 to 2002 in 35 countries with Caucasian-majority populations for which mortality data are available since at least 1990, including Europe, North America, Australia, New Zealand and Israel.
|
methods |
|---|
|
TopAbstractintroductionmethodsresultsdiscussionfundingReferences |
|---|
data sources
Breast cancer mortality data were available for 35 countries, but breast cancer incidence data were available for 28 countries. In the seven countries with missing incidence data, there was no national nor subnational cancer registry with sufficient historical series. Incidence data were extracted from Cancer Incidence in five continent [4], EUROCIM database [5], NORDCAN database [6] and SEER database [7]. Registry data were passed through the multiple primary check program used by International Agency for Research on Cancer (IARC). Additional information was found in various national cancer registry reports available in the Internet [8–21]. The SEER definition of a ‘second primary’ cancer is more liberal than that used by the IARC: in SEER data, counting of second cancer cases is time dependent, and bilateral tumors are counted twice. Also classification of tumors can be made in more histological groups than in the IARC system, and two breast cancers occurring in the same patient may be counted as two different cancers according to SEER but as only one cancer according to IARC.
We extracted breast cancer mortality data of 35 countries with mainly European ancestry from the World Health Organization database [22] also available at IARC Web site [23]. Changes in the classification or in the codification process of death certificates may affect mortality trends. For instance, the change from International Classification of Diseases (ICD)-8 to ICD-10 in 1995 in Switzerland caused discontinuities in trends and the Swiss data before 1995 have been corrected accordingly [24]. In France, the effect of the introduction of the ICD-10 on mortality statistics has been studied [25] and mortality data before 2000 have been adjusted. A similar study was conducted in England and Wales [26] and corresponding data before 2000 and after 1993 have been corrected. Corrections for changes in classification brought only small changes to trends.
In the UK, incidence data were available for England (without Wales) and Scotland, but mortality data were available for England and Wales and for Scotland. For the sake of text clarity England with or without Wales on one hand and Scotland on the other hand, were considered as two countries.
Incidence and mortality data from Malta were not included in analysis because of small population size and short period of cancer registration.
statistical analysis
We computed the age-specific rates for each 5-year age-group and calendar year and estimated the age-standardized rate (ASR) of incidence and mortality rates per 100 000 person-years of all ages and for three different age-groups (35–49, 50–69 and 70 years of age), using the World Standard Population as defined by Segi [27].
For the majority of countries, incidence and mortality data were available until 2002 or later. We carried out estimations of trends until 2002 since this was the most recent year for which data were available for nearly all countries. For each country, annual percentage changes (APCs) and 95% confidence intervals (CIs) were quantified using log-linear regression for the period starting in 1990 until 2002 (APC). A trend was labeled as ‘significant’ if the 95% CI did not include zero. Overall percentage change (OPC) was calculated from 1990 to 2002 using the formula: OPC = ((1 + APC)number of years) – 1).
Incidence data were available until 2000 in Estonia and Germany, until 1999 in Switzerland and until 1997 in Italy, Spain, France and Canada. First year of available data was 1991 in Bulgaria and 1994 in Ireland. Mortality data were available until 1997 in Belgium and until 2001 in Denmark and Belarus. Available mortality data started in 1992 in Slovakia.
In these countries, we applied the APC estimated from the available data to the period 1990–2002, assuming that trends remained constant in the years without data. In Poland, mortality data were not available from 1996 to 1998, and in 1999, a change in classification in death certificates occurred. So, for this country, we used mortality data from 1990 to 1996 to estimate changes until 2002.
|
results |
|---|
|
TopAbstractintroductionmethodsresultsdiscussionfundingReferences |
|---|
Table 1 displays annual standardized rates for 1990 and for the last year of available data and detailed results on changes in breast cancer incidence and mortality from 1990 until 2002. For seven countries, only mortality data were available. Figure 1 summarizes changes in breast cancer incidence (27 countries) and mortality (33 countries) during 13 years from 1990 to 2002. Iceland and Luxembourg were not represented in Figure 1 because of instability in trends due to small population sizes.
|
|
changes in incidence and mortality rates since 1990
In women of all ages, incidence increased from 1990 to 2002 with an overall percent change from 2.1% in Canada to 54.2% in Lithuania. Women 35–49 years of age had the lowest increase in incidence, while women 50–69 years of age usually had the highest increases in incidence. In this age-group, 13-year increases of incidence between 25% and 49% were observed in 13 countries, increases between 50% and 99% were observed in 7 countries and the increase was 105.3% in Norway. In women 35–49 years old, the incidence decreased in Israel, United States and Canada, but the decline was significant only in the United States. Decreases in incidence were noticeable in seven countries for women 70 years old and more, with significant decrease in the United States and in Norway. These decreases in older women were always of much lower magnitude than the increase in incidence between 50 and 69 years old.
Changes in mortality were highly variable across countries. Among European countries, overall percent changes ranged from –30.5% (England and Wales) to +25.5% (Estonia). Decreases in mortality of >20% were observed in Australia, Austria, Canada, England and Wales, New Zealand, Scotland, Spain, Switzerland and the United States while decreases of <10% were observed in Belgium, Bulgaria, Denmark, Finland, France, Greece, Hungary and Poland. In all countries, there was a strong age gradient in mortality trends: mortality decreased more in the 35–49 age-group and decreased less in the 70+ age-group. The age differences in mortality changes were particularly marked in Eastern and Central European countries.
changes in incidence and mortality rates after 1990 according to rates in 1990
To assess whether there was a link between levels of incidence or mortality reached in 1990 and the subsequent magnitude of decrease or increase in breast cancer incidence or mortality, we represented in a same figure the level of incidence or mortality in 1990 and the OPC from 1990 to 2002.
The plot of change in incidence from 1990 to 2002 against the incidence rates in 1990 (Figure 2) indicates that the magnitude of increases in incidence from 1990 to 2002 was somewhat higher if incidence rates in 1990 were low.
|
For countries where all-age mortality in year 2000 was declining, we derived from Table 1 a plot of mortality from 1990 to 2002 against mortality rates in 1990 (Figure 3). Decreases in mortality were not much greater if mortality was high in 1990, and countries that had comparable mortality rates in 1990 showed highly variable changes in mortality during subsequent years. Among countries with highest mortality rates in 1990 (ASR
24 per 100 000 person-years), mortality dropped dramatically like in the UK (England and Wales, and Scotland). In contrast, mortality decreased only slightly in Belgium and Denmark. Among countries with intermediate mortality rates in 1990 (18/100 000 
ASR < 24/100 000), mortality decreased substantially in Australia, Canada, Switzerland, New Zealand and the United States. Decreases were low in France, Hungary and Slovakia. Among countries with relatively low mortality rates in 1990 (ASR < 18 per 100 000 person-years), mortality decreased substantially in Spain, while it decreased only moderately in Bulgaria, Finland and Greece. However, overall percent change from 1990 to 2002 corresponded to an average of the changes observed during this period. In this respect, in Finland, France, Spain, Norway, Germany and The Netherlands, sharper declines in mortality were noticeable at the end of the study period (data not shown) that probably announced greater decreases in mortality after 2002.
|
Figures 2 and 3 also indicate that mortality did not decrease more in countries with greater increases in incidence: in France, Denmark, Slovenia and Bulgaria, the incidence increased by 20% or more while the mortality decreased by <10%. In the United States, Canada and England, the incidence increased by <10% while the mortality decreased by 25% or more.
|
discussion |
|---|
|
TopAbstractintroductionmethodsresultsdiscussionfundingReferences |
|---|
This study is the first that compared temporal trends in breast incidence and mortality in 35 countries over a similar period of time. It shows striking differences in changes from 1990 to 2002 in breast cancer incidence and mortality between countries and between age-groups. Increases in incidence were lowest in 35–49 years old women and highest in women 50–69 years old. In contrast, decreases in mortality were highest in 35–49 years old women and lowest in women 70 years of age and more.
The six countries with lowest raise in incidence >13 years (Austria, England, The Netherlands, Scotland, United States and Canada) had quite large decline in mortality. In contrast, in a number of countries with substantial increases in incidence decreases in mortality remained relatively low. More specifically, the incidence in the 50–69 year group raised by 50% and more >13 years in Finland, Germany, Ireland and Norway, but the mortality dropped off only moderately in women 50 years of age and more.
The age difference in changes in incidence would be mainly due to mammography screening to the use of menopause hormone therapy (MHT) [28, 29]. However, MHT use was variable across countries. For instance, use was high in the United States, Switzerland and France but low in Italy [30], and thus the influence of MHT on breast cancer incidence may have been quite different from one country to another.
In most of the Central and eastern European countries, increases in incidence were among the highest observed, while mortality increased or decreased only moderately. Changes in reproductive factors and lifestyle after the rapid transition from centralized to market economy may have contributed to the strong increases in incidence. However, the few available published data do no provide obvious reasons for the increases in incidence. For instance, total energy intakes were lower in the 1990s than in the 1980s, but quality of consumed food products was apparently better [31–33]. New studies should have a closer look on reasons why breast cancer incidence is increasing in these countries. The increases in breast cancer mortality may proceed from the economical problems prevailing in most of these countries in the 1990s, limiting access to screening and to efficient treatments [34].
Downward changes in breast cancer mortality were more pronounced in younger women, followed by women 50–69 years old and then by women 70 years old and more. These contrasts were particularly marked in Central and eastern European countries. The sharp differences in mortality trends according to age could reflect a generational effect: younger women would be more breast cancer aware than older women and would also benefit from more medical attention [35–37].
In countries were breast cancer mortality decreased, the decline were highly variable and were not proportional to mortality levels observed in 1990. Probably these disparities in changes in breast cancer mortality reflect differences in detection and management of this condition. Profound restructuring of health care services involved in breast cancer detection, diagnosis and management occurred during the last 20 years in many countries, usually in the wake of mammography screening implementation [38–42]. Besides access to mammography screening and efficient treatments, it is probable that a part of the decrease in breast cancer mortality has been made by the increasing recognition that first, accuracy of screening was higher when done by radiologists used to read large numbers of mammograms [43, 44] and second, that outcome of cancer patients was better in high load, specialized cancer centers having multidisciplinary approaches [45–49].
|
funding |
|---|
|
TopAbstractintroductionmethodsresultsdiscussionfundingReferences |
|---|
European Commission (Directorate of SANCO Luxembourg, Grand Duchy of Luxembourg) for the European Network for Information in Cancer Epidemiology project; Canceropole Lyon Auvergne Rhone Alpes, France.
Received for publication October 31, 2007. Accepted for publication January 11, 2008.
|
References |
|---|
|
TopAbstractintroductionmethodsresultsdiscussionfundingReferences |
|---|
1. Ferlay J, Bray F, Pisani P, et al. GLOBOCAN 2002: Cancer Incidence, Mortality and Prevalence Worldwide. IARC Cancer Base No. 5, version 2.0, Lyon, France: IARC Press, 2004.
2. Veronesi U, Boyle P, Goldhirsch A, et al. Breast cancer. Lancet (2005) 365:1727–1741.[CrossRef][Web of Science][Medline]
3. Hermon C, Beral V. Breast cancer mortality rates are levelling off or beginning to decline in many western countries: analysis of time trends, age-cohort and age-period models of breast cancer mortality in 20 countries. Br J Cancer (1996) 73:955–960.[Web of Science][Medline]
4. Parkin DM, Whelan SL, Ferlay J, et al. Cancer Incidence in Five Continents, Vol. VIII. IARC Scientific Publications No. 155, Lyon, France IARC Press, 2002.
5. Eurocim Version 4.1. European Incidence Database, European Network of cancer registries Version 2.4. ICD-10 Entity Dictionary. Lyon, France: IARC Press, 2003.
6. Engholm G, Storm H, Ferlay J, et al. Cancer Incidence and Mortality in the Nordic Countries, Version 2.2. Copenhagen (2006) Denmark: Danish Cancer Society.
7. Surveillance, Epidemiology, and End Results (SEER) Program. Limited-Use Data (1973–2004) (2007) National Cancer Institute, DCCPS, Surveillance Research Program, Cancer Statistics Branch, USA.
8. Swedish Cancer Registry. http://www.socialstyrelsen.se/ (June 2006, date last accessed).
9. Ondrusova M, Plesko I, Safaei Diba C. Cancer Incidence in the Slovak Republic 2003 (2006) Bratislava, Slovakia: National Health Information Centre, 210.
10. Israel: Israel Cancer Registry. http://www.health.gov.il/icr (June 2006, date last accessed).
11. Lithuanian Cancer Registry: Cancer in Lithuania 2001–2002 (2005) Vilnius, Lithuania: Vilnus University Institute of Oncology,
12. Cancer Registry of Bulgaria. http://www.onco-bg.com (June 2006, date last accessed).
13. Cancer Registry of Norway. Cancer Incidence in Norway 2002. http://www.kreftregisteret.no (June 2006, date last accessed).
14. National Cancer Registry of Ireland. http://www.ncri.ie/ncri (June 2006, date last accessed).
15. Scottish Cancer registry. http://www.isdscotland.org (June 2006, date last accessed).
16. Association of Comprehensive Cancer Centres. Utrecht, The Netherlands. http://www.ikcnet.nl (June 2006, date last accessed).
17. Hertl K, Primic-Zakelj M, Zgajnar J, et al. Performance of opportunistic breast cancer screening in Slovenia. Neoplasma (2006) 53:237–241.[Medline]
18. Austria: Statistik Austria. http://www.statistik.at (June 2006, date last accessed).
19. England and Wales: National Statistics. http://www.statistics.gov.uk (June 2006, date last accessed).
20. Epidemiology of Malignant Tumors in the Czech Republic. National Cancer Registry of the Czech Republic. http://www.svod.cz (June 2006, date last accessed).
21. New Zealand Health Information Service. The New Zealand Cancer Register. http://www.nzhis.govt.nz/ (June 2006, date last accessed).
22. WHO Statistical Information System. World Health Organization, Geneva, Switzerland: http://www.who.int/whosis (20 July 2007, date last accessed).
23. International Agency for Cancer Research. (2007;) http://www.iarc.fr (20 July 2007, date last accessed).
24. Lutz JM, Pury P, Fioretta G, et al. The impact of coding process on observed cancer mortality trends in Switzerland. Eur J Cancer Prev (2004) 13:77–81.[CrossRef][Web of Science][Medline]
25. Pavillon G, Boileau J, Renaud G, et al. Conséquences des changements de codage des causes médicales de décès sur les données nationales de mortalité en France, à partir de l'année 2000. Bullettin Epidémiologique Hebdomadaire (2005) 4:13–16. [Article in French].
26. Brock A, Griffiths C, Rooney C. The effect of the introduction of ICD-10 on cancer mortality trends in England and Wales. Health Stat Q (2004) 23:7–17.[Medline]
27. Segi M. Cancer Mortality for Selected Sites in 24 Countries (1950–57). Tohoku University, Sendai, Japan: 1960;.
28. Jemal A, Ward E, Thun MJ. Recent trends in breast cancer incidence rates by age and tumors characteristics among US women. Breast Cancer Res (2007) 9(3):R28.[CrossRef][Medline]
29. Glass AG, Lacey JV, Carreon JD, Hoover RN. Combined role of menopause hormone therapy, screening mammography, and estrogen receptor status. J Natl Cancer Inst (2007) 99:1152–1161.
30. Jolleys JV, Olesen F. A comparative study of prescribing of hormone replacement therapy in USA and Europe. Maturitas (1996) 23:47–53.[CrossRef][Web of Science][Medline]
31. Ivanova L, Dimitrov P, Ovcharova D, et al. Economic transition and household food consumption: a study of Bulgaria from 1985 to 2002. Econ Hum Biol (2006) 4:383–397.[CrossRef][Web of Science][Medline]
32. Dofkova M, Kopriva V, Resova D, et al. The development of food consumption in the Czech Republic after 1989. Public Health Nutr (2001) 4:999–1003.[Web of Science][Medline]
33. Waskiewicz A, Piotrowski W, Sygnowska E, et al. Did favourable trends in food consumption observed in the 1984–2001 period contribute to the decrease in cardiovascular mortality?—Pol-MONICA Warsaw Project. Kardiol Pol (2006) 64:16–23.[Medline]
34. Kliukiene J, Andersen A. Survival of breast cancer patients in Lithuania and Norway, 1988–1992. Eur J Cancer (1998) 34:372–377.[CrossRef][Web of Science][Medline]
35. August DA, Rea T, Sondak VK. Age-related differences in breast cancer treatment. Ann Surg Oncol (1994) 1:45–52.[CrossRef][Web of Science][Medline]
36. Karjalainen S, Aareleid T, Hakulinen T, et al. Survival of female breast cancer patients in Finland and in Estonia: stage at diagnosis important determinant of the difference between countries. Soc Sci Med (1989) 28:233–238.[CrossRef][Web of Science][Medline]
37. Eaker S, Dickman PW, Bergkvist L, et al. Differences in management of older women influence breast cancer survival: results from a population-based database in Sweden. PLoS Med (2006) 3:e25.[CrossRef][Medline]
38. August DA, Carpenter LC, Harness JK, et al. Benefits of a multidisciplinary approach to breast care. J Surg Oncol (1993) 53:161–167.[Web of Science][Medline]
39. Monaghan P, Murray L, Donnelly M, et al. Breast cancer services—a population-based study of service reorganization. J Public Health (Oxf) (2005) 27:171–175.[CrossRef][Medline]
40. Zorbas H, Luxford K, Evans A, et al. Re: trends in the treatment of ductal carcinoma in situ of the breast. J Natl Cancer Inst (2004) 96:1258–1260.
41. Zorbas H, Barraclough B, Rainbird K, et al. Multidisciplinary care for women with early breast cancer in the Australian context: what does it mean? Med J Aust (2003) 179:528–531.[Web of Science][Medline]
42. Eaker S, Dickman PW, Hellstrom V, et al. Regional differences in breast cancer survival despite common guidelines. Cancer Epidemiol Biomarkers Prev (2005) 14:2914–2918.
43. Smith-Bindman R, Chu P, Miglioretti DL, et al. Physician predictors of mammographic accuracy. J Natl Cancer Inst (2005) 97:358–367.
44. Theberge I, Hebert-Croteau N, Langlois A, et al. Volume of screening mammography and performance in the Quebec population-based Breast Cancer Screening Program. CMAJ (2005) 172:195–199.
45. Clarke CA, Glaser SL, Uratsu CS, et al. Recent declines in hormone therapy utilization and breast cancer incidence: clinical and population-based evidence. J Clin Oncol (2006) 24:e49–e50.
46. Sainsbury R, Haward B, Rider L, et al. Influence of clinician workload and patterns of treatment on survival from breast cancer. Lancet (1995) 345:1265–1270.[CrossRef][Web of Science][Medline]
47. Gillis CR, Hole DJ. Survival outcome of care by specialist surgeons in breast cancer: a study of 3786 patients in the west of Scotland. Br Med J (1996) 312:145–148.
48. Selby P, Gillis C, Haward R. Benefits from specialised cancer care. Lancet (1996) 348:313–318.[CrossRef][Web of Science][Medline]
49. Gilligan MA, Neuner J, Zhang X, et al. Relationship between number of breast cancer operations performed and 5-year survival after treatment for early-stage breast cancer. Am J Public Health (2007) 97:539–544.
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  M. Pollan, R. Pastor-Barriuso, E. Ardanaz, M. Arguelles, C. Martos, J. Galceran, M.-J. Sanchez-Perez, M.-D. Chirlaque, N. Larranaga, R. Martinez-Cobo, et al. Recent Changes in Breast Cancer Incidence in Spain, 1980-2004 J Natl Cancer Inst, November 18, 2009; 101(22): 1584 - 1591. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 T. Deng, J. C. Liu, K. I. Pritchard, A. Eisen, and E. Zacksenhaus Preferential Killing of Breast Tumor Initiating Cells by N,N-Diethyl-2-[4-(Phenylmethyl)Phenoxy]Ethanamine/Tesmilifene Clin. Cancer Res., January 1, 2009; 15(1): 119 - 130. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||