Cancer incidence and mortality in France over the period 1980–2005

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Revue d’E´pide´miologie et de Sante´ Publique 56 (2008) 159–175

Original article

Cancer incidence and mortality in France over the period 1980–2005 Incidence et mortalite´ des cancers en France durant la pe´riode 1980–2005 A. Belot a,b,c,d,*, P. Grosclaude e, N. Bossard a,b,c, E. Jougla f, E. Benhamou g, P. Delafosse h, A.-V. Guizard i, F. Molinie´ j, A. Danzon k, S. Bara l, A.-M. Bouvier m, B. Tre´tarre n, F. Binder-Foucard o, M. Colonna h, L. Daubisse e, G. He´delin o, G. Launoy p,y, N. Le Stang q, M. Maynadie´ r, A. Monnereau s, X. Troussard t, J. Faivre m, A. Collignon t, I. Janoray r, P. Arveux u, A. Buemi v, N. Raverdy w, C. Schvartz x, M. Bovet f, L. Che´rie´-Challine d, J. Este`ve a,b,c, L. Remontet a,b,c, M. Velten o a

Service de biostatistique, hospices civils de Lyon, centre hospitalier Lyon-Sud, 69424 Lyon, France b Universite´ Lyon-I, 69622 Villeurbanne, France c UMR 5558, laboratoire biostatistique sante´, CNRS, baˆtiment 4D, 106, chemin du Grand Revoyet, 69495 Pierre-Be´nite cedex, France d De´partement des maladies chroniques et des traumatismes, institut de veille sanitaire, 12, rue du Val-d’Osne, 94415 Saint-Maurice, France e Registre des cancers du Tarn, France f Inserm, Ce´piDc, France g Institut de cance´rologie Gustave-Roussy, France h Registre des cancers de l’Ise`re, France i Registre des cancers du Calvados, France j Registre des cancers de Vende´e et de Loire-Atlantique, France k Registre des cancers du Doubs, France l Registre des cancers de la Manche, France m Registre Bourguignon des tumeurs digestives, France n Registre des cancers de l’He´rault, France o Registre des cancers du Bas-Rhin, France p Registre des cancers digestifs du Calvados, France q Registre multicentrique a` vocation nationale des me´sothe´liomes pleuraux, France r Registre des he´mopathies malignes de Coˆte d’Or, France s Registre des he´mopathies malignes de la Gironde, France t Registre re´gional des he´mopathies malignes de Basse Normandie, France u Registre des cancers du sein et cancers gyne´cologiques de Coˆte d’Or, France v Registre des cancers du Haut-Rhin, France w Registre des cancers de la Somme, France x Registre des cancers thyroı¨diens de Champagne-Ardennes, France y Re´seau FRANCIM des registres des cancers, France Received 29 January 2008; accepted 10 March 2008 Available online 10 June 2008

Abstract Background. – The objective of this study was to provide updated estimates of national trends in cancer incidence and mortality for France for 1980–2005. Methods. – Twenty-five cancer sites were analysed. Incidence data over the 1975–2003 period were collected from 17 registries working at the department level, covering 16% of the French population. Mortality data for 1975–2004 were provided by the Inserm. National incidence estimates were based on the use of mortality as a correlate of incidence, mortality being available at both department and national levels. Observed incidence

* Corresponding author. E-mail address: [email protected] (A. Belot). 0398-7620/$ – see front matter # 2008 Elsevier Masson SAS. All rights reserved. doi:10.1016/j.respe.2008.03.117

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and mortality data were modelled using an age-cohort approach, including an interaction term. Short-term predictions from that model gave estimates of new cancer cases and cancer deaths in 2005 for France. Results. – The number of new cancer cases in 2005 was approximately 320,000. This corresponds to an 89% increase since 1980. Demographic changes were responsible for almost half of that increase. The remainder was largely explained by increases in prostate cancer incidence in men and breast cancer incidence in women. The relative increase in the world age-standardised incidence rate was 39%. The number of deaths from cancer increased from 130,000 to 146,000. This 13% increase was much lower than anticipated on the basis of demographic changes (37%). The relative decrease in the age-standardised mortality rate was 22%. This decrease was steeper over the 2000–2005 period in both men and women. Alcohol-related cancer incidence and mortality continued to decrease in men. The increasing trend of lung cancer incidence and mortality among women continued; this cancer was the second cause of cancer death among women. Breast cancer incidence increased regularly, whereas mortality has decreased slowly since the end of the 1990s. Conclusion. – This study confirmed the divergence of cancer incidence and mortality trends in France over the 1980–2005 period. This divergence can be explained by the combined effects of a decrease in the incidence of the most aggressive cancers and an increase in the incidence of less aggressive cancers, partly due to changes in medical practices leading to earlier diagnoses. # 2008 Elsevier Masson SAS. All rights reserved. Re´sume´ Position du proble`me. – Notre e´tude avait pour objectif d’estimer les tendances de l’incidence et de la mortalite´ des cancers en France sur la pe´riode 1980–2005. Me´thodes. – Vingt-cinq localisations cance´reuses ont e´te´ analyse´es. Les donne´es d’incidence sur la pe´riode 1975–2003 ont e´te´ collecte´es par 17 registres de´partementaux, couvrant environ 16 % de la population. Les donne´es de mortalite´ sur la pe´riode 1975–2004 ont e´te´ fournies par l’Inserm. L’estimation de l’incidence nationale a e´te´ base´e sur l’utilisation de la mortalite´ comme corre´lat de l’incidence, la mortalite´ e´tant disponible au niveau de´partemental et national. Les donne´es d’incidence et de mortalite´ observe´es ont e´te´ mode´lise´es a` partir d’un mode`le aˆgecohorte incluant un terme d’interaction. Les nombres de nouveaux cas de cancer et de de´ce`s par cancer en 2005 ont e´te´ issus de pre´dictions a` court terme par mode´lisation statistique. Re´sultats. – En 2005, le nombre de nouveaux cas a e´te´ estime´ a` 320 000, traduisant une augmentation de 89 % depuis l’anne´e 1980. Cette augmentation e´tait due presque pour moitie´ aux changements de´mographiques. La part restante e´tait largement explique´e par l’augmentation de l’incidence du cancer de la prostate chez l’homme et du cancer du sein chez la femme. Le taux d’incidence standardise´ selon l’aˆge pour la population mondiale a augmente´ de 39 %. Le nombre de de´ce`s a e´te´ estime´ a` 146 000 en 2005, traduisant une augmentation de 13 % depuis 1980. Cette augmentation du nombre de de´ce`s est tre`s infe´rieure a` celle pre´vue par les changements de´mographiques (37 %). Le taux de mortalite´ standardise´ selon l’aˆge a diminue´ de 22 %. Cette de´croissance a e´te´ plus importante de 2000 a` 2005 pour les deux sexes. L’incidence et la mortalite´ des cancers lie´s a` l’alcool ont continue´ a` diminuer chez l’homme. L’incidence et la mortalite´ du cancer du poumon chez la femme ont continue´ a` augmenter: ce cancer e´tait la deuxie`me cause de de´ce`s par cancer chez la femme. L’incidence du cancer du sein a augmente´ re´gulie`rement alors que la mortalite´ a diminue´ depuis la fin des anne´es 1990. Conclusion. – Ces nouvelles estimations portant sur la pe´riode 1980–2005 confirment la divergence importante entre les tendances d’incidence et de mortalite´ par cancer en France. Cette divergence s’explique par l’effet combine´ de la diminution de l’incidence des cancers les plus agressifs et l’augmentation de l’incidence des cancers de meilleur pronostic, cette augmentation e´tant lie´e, en partie, a` des modifications des pratiques me´dicales, entrainant des diagnostics pre´coces. # 2008 Elsevier Masson SAS. All rights reserved. Keywords: Cancer; Incidence; Mortality; Trends; Registry Mots cle´s : Cancer ; Incidence ; Mortalite´ ; Tendance ; Registre

1. Introduction Cancer is a major public health problem in France as well as in other developed countries. Estimation and interpretation of incidence and mortality time trends for different cancer sites remain crucial epidemiological objectives that contribute to defining public health policy. These key epidemiological indicators are essential for establishing priorities in preventive strategies and in epidemiological and therapeutic research. They also contribute to assessing the overall performance of a healthcare system and to guiding resource allocation. Therefore, national estimates must be regularly updated. In 2007, there were 21 French population-based cancer registries operating at the level of a department, a French

subregional administrative entity. These registries (11 general and 10 cancer site-specific) provide cancer statistics on approximately 16% of the French population. In order to provide better access to this information, the Network of the French Cancer Registries (FRANCIM) created a common database. This network, together with the Department of Biostatistics of the Hospices Civils de Lyon, and the Institut de veille sanitaire (InVS) are responsible for the scientific and logistic tasks related to its administration. This database now totals nearly 650,000 patients and 690,000 tumours diagnosed between 1975 and 2003. Establishing a cancer registry in a given department was a local decision. The representativeness of the national population was not initially contemplated and it remains questionable. Thus, national incidence estimates are based on correlates of incidence available both at the

A. Belot et al. / Revue d’E´pide´miologie et de Sante´ Publique 56 (2008) 159–175

department level and at the national level. Such national estimates, obtained using mortality rates as correlates, were produced in the past for the period 1978–2000 [1] and they were based on an age-cohort model from incidence and mortality data collected between 1975 and 1997. We present here updated national incidence and mortality estimates as well as time trends over the 1980–2005 period. We used the most recent registry incidence data (available up to 2003) and updated statistical modelling made feasible by a larger amount of available information. 2. Materials and methods Information on cancer incidence was taken from 17 selected registries (11 general and six specialised) which had data for at least five years (Table 1). Twenty-five cancer sites were considered in the present analysis. Their selection was motivated by their frequency, their public health and epidemiological relevance, and the availability of reliable data on site identification. The latter argument led us to produce pleura cancer incidence estimates (all morphological types confounded) and to include only malignant central nervous system (CNS) tumours despite different international recommendations. Although cancers of the cervix and corpus uteri should be registered separately in mortality statistics, the number of ‘‘uterus not otherwise specified’’ is so large that it was necessary to re-estimate the death rates for each sub-site. We predicted cohort mortality from cohort incidence and survival of both sites and used the period-specific proportion thus estimated to distinguish deaths related to corpus uteri cancers from deaths related to cervix uteri cancers. In contrast to our previous study [1], we applied this procedure using data from six registries and survival estimates obtained from a population-based survival study

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[2]. The final classification of cancer sites used in the analysis is shown in Table 2. 2.1. Cases The case information recorded in the database was validated using the tools provided by WHO’s International Agency for Research on Cancer. Each possibly erroneous record was checked and if necessary amended by the source registry. The topography and morphology of the cancers were recorded according to the International Classification of Diseases for Oncology, Third edition (ICD-O-3). The following rules were applied as follows: (i) only invasive tumours contributed to the calculation of incidence rates, including CNS and bladder tumours; and (ii) for solid tumours, all morphology types were included except the haematological types. Given the unreliability of their registration, skin cancers other than melanomas are excluded from the incidence statistics. Therefore ‘‘All cancers’’ should be understood as ‘‘non-melanoma skin cancer excluded’’. The present study included 611,652 cases diagnosed between 1 January 1975 and 31 December 2003 (Table 1). 2.2. Deaths Mortality data were provided by the Institut national de la sante´ et de la recherche me´dicale, centre d’e´pide´miologie sur les causes me´dicales de de´ce`s (Inserm, Ce´piDc). All cancer deaths (4,194,296 anonymous records) that occurred in France between 1 January 1975 and 31 December 2004 were stored in the common database in Lyon by year of death, place of residence (department), sex, age at death, and ICD code (8th, 9th and 10th revision). Age at death was

Table 1 Incidence data used for national estimates Registry

Department

Years of operation

Type of registry

1

Ardennes Marne Calvados

1975–2003

Thyroid

1978–2002 1978–2003 1976–2003 1980–2003 1982–2003 1978–2003 1986–2003 1979–2003 1991–2003 1998–2003 1994–2003 1975–2003 1988–2002 1982–2003 1982–2003 1982–2003 1997–2003

General (nondigestive) Digestive tract Digestive tract Haematopoietic Breast General General General Breast, large bowel General General General General Digestive tract General General General

2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17

Coˆte d’Or

Doubs He´rault Ise`re Loire-Atlantique Manche Bas-Rhin Haut-Rhin Saoˆne&Loire Somme Tarn Vende´e Total

Population (2005) 286,014 563,923 663,585 514,011

513,471 982,220 1,159,324 1,203,338 488,318 1,069,854 735,169 547,207 557,774 362,203 584,528

Number of cases over the total period 463 1031 40,734 15,467 13,191 4,582 5945 43,700 63,677 90,578 16,979 23,305 22,081 111,441 44,639 15,336 46,673 34,119 17,711 611,652

A. Belot et al. / Revue d’E´pide´miologie et de Sante´ Publique 56 (2008) 159–175

162 Table 2 Subsite definition Site

Incidence CIMO3 a

Lip, oral cavity, pharynx (Lip-OC-P) Oesophagus Stomach Large bowel Liver Pancreas Larynx Lung Pleura Skin melanoma Breast Cervix uterib Corpus uterib Ovary

Prostate Testis Bladder Kidney Brain and central nervous system (CNS) Thyroid Non-Hodgkin lymphoma

Mortality a

Topography

Morphology

1975–1978 (CIM8)

1979–1999 (CIM9)

2000–2004 (CIM10)

C0*, C10*, C11*, C12*, C13*, C14* C15* C16* C18*, C19*, C20*, C21* C22* C25* C32* C33*, C34* C384 C44* C50* C53* C54* C56*, C570, C571, C572, C573, C574

All

14*

14*

All All All

150* 151* 153*, 154*

150* 151* 153*, 154*

C0*, C10*, C11*, C12*, C13*, C14* C15* C16* C18*, C19*, C20*, C21*

All All All All All 87203–87803 All All All All excluding {84423; 84513; 84613; 84623; 84723; 84733} All All All All

155*, 1978 157* 161* 162* 1630 172* 174* 180* to 182* 180* to 182* 183*

155* 157* 161* 162* 163* 172* 174* 179* to 182* 179* to 182* 183*

C22* C25* C32* C33*, C34* C384, C450, C459 C43* C50* C53*, C54*, C55* C53*, C54*, C55* C56*, C570, C571, C572 C573, C574

185* 186* 188* 189*

185* 186* 188* 189*

C61* C62* C67* C64*, C65*, C66*; C68*

 91103 or  91800

191*, 192*

191*, 192*

C70*, C71*, C72*

All 95903–95963 96703–97193 97273–97293 98323–98343 96503–96673 97313–97343 97603–97643

193* 200*, 202*

193* 200*, 202*

C73* C82*, C83*, C84*, C85*

201* 203*

201* 203*, 2386

C81* C90*, C88*

2040, 2050, 2060, 2070, 208*

2040, 2042, 2050, 2052, 2053, 2060, 2062, 2070, 2080, 2082

C910, C920, C924, C925, C930, C942, C943, C950

2041 140* to 208*

2041 140* to 208*

C911 C00* to C97*

C61* C62* C67* C64*, C65*, C66*; C68* C70*, C71*, C72* C73* All

Hodgkin’s disease Multiple myeloma and immunoproliferative diseases (ID) Acute leukaemia

All All

Chronic lymphocytic leukaemia All cancersc

All C00* to C80*

All

98013–98203 98263–98273 98353–98613 98663–98743 98913–99203 99483 98233 All

or or or

or

or or or or or

*All codes between 0 and 9. a Haematological codes are always excluded from solid tumour sites and included in the relevant haematological site. b Cervix uteri and corpus uteri deaths were re-estimated (see materials & methods). c Excluding skin.

the difference between the year of death and the year of birth.

number of survivors who reached a given age at 1 January by gender. For age above 99, the Insee provided the number of survivors who reached age 99 or more on 1 January.

2.3. Population data 2.4. Rates Population data were available from the institut de statistique et des e´tudes e´conomiques (Insee) for each department and from 1975 to 2006. These data provided the

One-year interval data for age, birth cohort, and period were used to estimate incidence and mortality rates. Age-specific

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rates were estimated from the models described in the next section. Since age at diagnosis (respectively, age at death) was calculated as the difference between year of diagnosis (respectively, year of death) and year of birth and because person-years were calculated as the mean between the population size of age a on 1 January of year p and the population size of age a + 1 on 1 January of year p + 1, the incidence rate of a five-year age group was estimated for a population six months younger than usual [3]. Thus, to correct for this minor difference, age-standardised rates were calculated using modified weights for each age group. Unless otherwise stated, rates were standardised on the world population age structure and were expressed for 100,000 person-years. 2.5. Statistical modelling Let lFac be the French national incidence rate for age a and cohort c. To obtain an estimate of lFac , the general principle is to use (i) an estimate of incidence rates lˆ ac and of mortality rates ˆ ac in the area covered by all registries and (ii) an estimate of m ˆ Fac French national mortality rates m

2.5.2. Mortality in the area covered by the registries Observed mortality data were fitted using the model: Dacz  Poissonðmacz macz Þ Logðmacz Þ ¼ az þ S1 ðaÞ þ S2 ðcÞ þ b1  p2 þ b2  ð1z  cÞ þ b3  ð1z  p2 Þ (3) where D being the number of deaths and z a covariate defining ‘‘the area covered by all cancer registries’’ (first modality) or ‘‘the rest of France’’ (second modality). The indicator term 1z take the value 1 for the first modality of z, 0 otherwise. This model involved some information from the rest of France to be used for the prediction of the number of deaths in the De´partements covered by the cancer registries. 2.5.3. Mortality in France French mortality data were fitted using the model: Dac  Poissonðmac mac Þ

F

ˆ m F lˆ ac ¼ lˆ ac  ac ˆ ac m

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Logðmac Þ ¼ s1 ðaÞ þ s2 ðcÞ þ b1  p2 (4)

(1)

Thus, the incidence estimate in the area covered by all registries provides the trend for French national incidence, while the level of that incidence is provided by the ratio of the French national mortality estimate over the mortality estimate in the area covered by all registries. To obtain incidence and mortality estimates, we decided to use an age-cohort model [4–6] with a linear-by-linear interaction between age and cohort, which is equivalent to an age-period-cohort model with a second order period term p2. Age and cohort effects were modelled using smoothing splines [7–9]. The second-order period term p2 was introduced in the model only when it was statistically significant (likelihood ratio test, a = 1%).

2.5.4. Incidence in France Combining values predicted from models (2), (3) and (4), we F obtained an estimate of the incident rate lˆ ac in France according F to formula (1) (the number of incident cases Kˆ ac ). Given that cohorts were not entirely observed, we applied a similar APC approach to the predicted number of cases to obtain all agespecific rates for each cohort. The cohort effect on the incidence rate was expressed using the net cumulative risk CR of developing a cancer between 0 and 74 years of age for a subject of this cohort. This risk represents the probability of developing a cancer, between 0 and 74 years of age, in the absence of mortality. It is defined as: CRc ¼ 1  expð

74 X

F lˆ ac Þ

(5)

a¼0

2.5.1. Incidence in the area covered by the registries Observed incidence data tabulated in one-year classes were fitted using an age-period-cohort model in which the department covariate was introduced as a factor in order to avoid confounding space and time effects. More precisely:

The same calculation was done for mortality. Confidence intervals for the number of cases predicted for the year 2005 were obtained using a jackknife approach [1]. 3. Results

K acd  Poissonðmacd lacd Þ Logðlacd Þ ¼ ad þ s1 ðaÞ þ s2 ðcÞ þ b  p2

(2)

where s1 and s2 are smoothing splines, K and m are the number of cases and person-years, respectively, in the relevant agecohort-department cell, d being the indicator for departments and p the period term defined with age a and cohort c by the relation p = a + c. The incidence in the whole area covered by all registries is obtained by: P ˆ ˆlac ¼ Pd Kacd d macd

Age-standardised rates are essential to understand risk changes, whereas the number of cases is required to evaluate cancer burden and for healthcare planning. Age-standardised incidence and mortality rates in 2005 in men and women are provided in Fig. 1. The number of new cancer cases and cancer deaths in 2005 in men and women is provided in Fig. 2. We shall discuss below the trend in the age-adjusted rates of each cancer site (Tables 3 and 4 in men and women, respectively) and the trend in the number of cases at each cancer site (Tables 5 and 6 in men and women, respectively). The confidence intervals for the number of cancer cases in 2005 are

164

A. Belot et al. / Revue d’E´pide´miologie et de Sante´ Publique 56 (2008) 159–175

Fig. 1. World age-standardised incidence and mortality rates in France: estimates for 2005.

presented in Table 7. The birth cohort effect is provided with the cumulative risk of cancer between 0 and 74 years (Tables 8 and 9 in men and women, respectively). All mortality results presented in this article are estimated from statistical modelling (see model (4) in section 2). The number of new cancer cases was approximately 320,000 in 2005. It was only roughly 170,000 in 1980. This 89% increase over 25 years results partly from the ageing of the

population: during the same period, the world age-standardised incidence rate increased by only 39%. The number of deaths from cancer increased from 130,000 to 146,000. This 13% increase is much lower than anticipated on the basis of the demographic changes, and the world age-standardised mortality rate decreased over this period by roughly 22%. The increase in the age-standardised incidence rate was slightly steeper over the more recent 2000–2005 period than over the

A. Belot et al. / Revue d’E´pide´miologie et de Sante´ Publique 56 (2008) 159–175

165

Fig. 2. Number of new cancer cases and cancer deaths in France: estimates for 2005.

entire 1980–2005 period in both men and women (Tables 3 and 4). A particularly interesting finding of the study is the large decrease in mortality since the end of the 1990s (Tables 3 and 4), especially in men. In the following sections, we emphasise, site by site, the main changes that have occurred since the last publication [1]. It should be noted that estimates for 1980–2000 may be somewhat different from those published in our previous paper because a longer period of observation was available and, to a

lesser extent, because the method used this larger amount of information to introduce interactions (see section 2). International comparisons are based on Cancer incidence on five continents, volume 9, published in 2007 [10]. 3.1. Lip, oral cavity and pharynx In 2005, with 12,270 new cases (78% of which occurred in males) and 4000 deaths, these cancer sites were still frequent in

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Table 3 Estimated annual age–standardised1 incidence and mortality rates per 100,000 person–years in France in men Rate of changeb Mortality rates

Incidence rates Type of cancer Lip, oral cavity, pharynx Oesophagus Stomach Large bowel Liver Pancreas Larynx Lung Pleura Skin melanoma Prostate Testis Bladder Kidney Brain and CNS Thyroid Non-Hodgkin lymphoma Hodgkin’s disease Multiple myeloma and ID Acute leukaemia Chronic lymphocytic leukaemia All cancersc

1980

1985

1990

1995

38.2 15.2 14.6 33.6 4.1 4.7 14.3 48.3 0.8 2.4 26 3.4 15.7 7.3 4.7 1 6.2 2.9 2.7 3.6 3.1

39.4 14.6 13.2 36.1 5.3 4.6 13.8 50.7 1.1 3.7 33 3.9 17.3 8.7 5.1 1.3 8.2 2.8 3 3.8 3.3

37.8 13.4 11.8 37.8 6.8 4.8 12.7 52 1.3 5 42.2 4.4 18.1 9.8 5.3 1.7 10 2.7 3.5 4 3.4

33.8 11.8 10.5 38.7 8.2 5.3 11 52.4 1.5 6.3 56.5 4.9 17.8 10.7 5.5 2.3 11.5 2.6 3.8 4.1 3.5

278

2000

2005

Overall Recent 1980

28.2 21.8 –2.2 9.9 7.9 –2.6 9.2 8.2 –2.3 38.7 37.7 +0.5 9.5 10.4 +3.8 6.2 7.7 +2.0 9.1 7.1 –2.7 51.9 50.5 +0.2 1.4 1.2 +1.7 7.3 7.6 +4.7 80.4 121.2 +6.3 5.6 6.4 +2.5 16.6 14.6 –0.3 11.3 11.4 +1.8 5.6 5.7 +0.7 3.1 4.2 +5.8 12.2 12.1 +2.7 2.4 2.3 –0.9 4.2 4.6 +2.2 4.3 4.5 +0.9 3.6 3.6 +0.6

–5.0 –4.5 –2.4 –0.5 +1.9 +4.4 –4.7 –0.5 –3.4 +0.8 +8.5 +2.7 –2.5 +0.3 +0.1 +6.4 –0.1 –0.8 +1.5 +0.9 +0.2

298.4 314.3 328.6 346.4 376.1 +1.2

+1.7

15.9 13.9 13.2 19.9 * * 11.4 43.2 * 0.9 16.9 0.7 6.9 4 3.2 0.4 2.9 1 1.8 3.2 1

Rate of changeb

1985

1990

1995

2000

2005

15.1 12.6 10.9 19.1 * * 9.7 46.5 * 1.1 17.8 0.5 7.1 4.4 3.6 0.4 3.7 0.8 1.9 3.1 1.1

13.7 11.2 9 18.1 * * 7.7 48.2 * 1.3 17.7 0.4 7.1 4.6 3.9 0.4 4.3 0.6 2.1 3 1.2

11.7 9.6 7.5 17.2 * * 5.7 48 * 1.5 16.7 0.3 6.8 4.7 4 0.3 4.6 0.5 2.2 2.9 1.2

9.5 8 6.3 16.2 * * 4 45.9 * 1.6 15.3 0.3 6.3 4.5 4 0.3 4.5 0.4 2.3 2.9 1.1

7.2 6.3 5.3 15.2 * * 2.6 42 * 1.6 13.5 0.2 5.6 4.3 3.9 0.3 4 0.3 2.3 2.8 0.9

214.4 215.8 210.4 198.9 182

Over–all Recent –3.1 –3.1 –3.6 –1.1 * * –5.8 –0.1 * +2.3 –0.9 –4.4 –0.8 +0.2 +0.8 –1.8 +1.3 –4.9 +1.0 –0.5 –0.3

–5.4 –4.6 –3.3 –1.2 * * –8.3 –1.7 * +0.3 –2.5 –4.5 –2.1 –1.2 –0.6 –2.7 –2.3 –5.3 +0.5 –0.2 –2.8

160.7 –1.1

–2.5

*The quality of the mortality data is too weak for this site to interpret them in terms of trends (section 4). 1 Based on the standard World population. b Annual rate of change in percent (%). Overall concerned the 1980–2005 period and Recent the 2000–2005 period. c Excluding skin.

France. Despite a substantial and steady decrease in incidence and mortality in men, the age-standardised rates were equal to 21.8 and 7.2, respectively. These values are still higher than those found in other countries. This decrease in incidence was more pronounced during the most recent 2000–2005 period (5% annual rate of change) than during the overall 1980–2005 period (2.2% annual rate of change). The cumulative risk of cancer reached its maximum for the 1930 birth cohort, then decreased continually afterwards. In 2005, the age-standardised incidence and mortality rates in women were 5.2 and 1.2, respectively. Time trends showed a constant increase in incidence during the entire period (+1.6% annual rate of change for 1980–2005), while mortality remained nearly constant. The decrease in risk in men reflects a decrease in alcohol consumption, which has been observed in France since the 1950s [11] and, to a lesser degree, to a decrease in tobacco consumption. However, the incidence rate trends for women probably result from the increasing similarity of men’s and women’s lifestyle. 3.2. Oesophagus The number of new cancer cases and cancer deaths was 4721 and 3850 in 2005, respectively, with 79.1% of new cases occurring in males. The age-standardised incidence rate was 7.9 in men and 1.5 in women. The corresponding values for age-standardised mortality rates were 6.3 and 1.0, respectively.

There was a major decrease in incidence in men during the last 25 years, while the incidence trend in women increased slowly but steadily. Mortality rates declined continually in men and levelled off in women. The pattern of the cumulative risk of cancer was the same as that of ‘‘lip, oral cavity and pharynx’’ cancers and the reasons for observing such time trends in men and women are similar [12,13]. Taking histology into consideration, the decrease seen in men is related to epidermoid cancers. The incidence of adenocarcinoma is increasing in both genders [13]. The reasons for this trend are still unknown. 3.3. Stomach In 2005, this cancer site contributed 4405 new cases in men and 2389 in women. As reported earlier [1], incidence and mortality rates in both sexes decreased from 1980 to 2005. In men, the annual rate of change was approximately 2.3% for incidence and 3.6% for mortality. In women, the annual rate of change was roughly 2.8% for incidence and 4% for mortality. It has been shown that the decrease in incidence was limited to distal cancers [12,14]. Changes in the methods for preserving foods and avoidance of salt and pickles are probably responsible for the long-term decrease in the incidence of stomach cancer. The decrease in the prevalence of Helicobacter infection may have played a major role in the recent trend. Incidence rates in France are lower than in most European countries [15].

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Table 4 Estimated annual age–standardised1 incidence and mortality rates per 100,000 person–years in France in women Type of cancer

Lip, oral cavity, pharynx Oesophagus Stomach Large bowel Liver Pancreas Larynx Lung Pleura Skin melanoma Breast Cervix uteri Corpus uteri Ovary Bladder Kidney Brain and CNS Thyroid Non-Hodgkin lymphoma Hodgkin’s disease Multiple myeloma and ID Acute leukaemia Chronic lymphocytic leukaemia All cancers c

Rate of changeb

Incidence rates 1980

1985

1990

1995

3.5 1 6.2 22.8 0.8 1.9 0.6 3.6 0.2 3.9 56.8 14.9 10.4 8.9 2.9 3 3.2 2.9 4 1.9 1.9 2.8 1.5

3.7 1.1 5.4 23.4 0.9 2.1 0.6 4.5 0.2 5.2 64.2 12.1 10.3 9 2.8 3.8 3.5 3.9 5.3 1.8 2.1 2.9 1.6

4 1.2 4.6 23.9 1.1 2.5 0.7 5.7 0.3 6.6 72.8 10.1 10.2 8.9 2.6 4.4 3.7 5.2 6.4 1.8 2.4 3.1 1.7

4.4 1.3 4 24.2 1.4 3.1 0.8 7.3 0.3 7.8 82 8.7 10.1 8.8 2.5 4.8 4 7 7.4 1.9 2.6 3.2 1.8

176.6 186.9 200

2000

2005

Rate of changeb

Mortality rates

Over–all Recent 1980

1985 1990 1995 2000 2005 Overall Recent

4.8 5.2 +1.6 1.4 1.5 +1.5 3.5 3.1 –2.8 24.4 24.5 +0.3 1.7 2 +4.0 3.7 4.7 +3.8 0.9 1 +2.1 9.5 12.6 +5.1 0.3 0.4 +3.1 8.6 8.8 +3.4 91.5 101.5 +2.4 7.8 7.1 –2.9 10 10 –0.2 8.5 8.1 –0.4 2.3 2.1 –1.3 4.8 4.5 +1.6 4.1 4.2 +1.1 9.5 12.7 +6.0 8 8.2 +2.9 2.1 2.5 +1.1 2.8 2.9 +1.8 3.3 3.5 +0.9 1.9 2 +1.2

+1.6 +1.4 –2.5 +0.1 +3.6 +4.5 +2.0 +5.8 +1.8 +0.5 +2.1 –1.8 –0.1 –1.0 –1.6 –1.4 +0.6 +6.1 +0.4 +3.3 +1.1 +0.9 +0.7

1.2 1.3 1.1 1.1 5.7 4.5 12.4 11.4 * * * * 0.4 0.4 3.9 4.5 * * 0.8 0.9 19.4 20 5.4 4.2 2.6 2.6 5.6 6 1.4 1.3 1.8 1.8 1.9 2.3 0.6 0.6 1.6 2.2 0.5 0.4 1.3 1.4 2.3 2.1 0.4 0.5

1.3 1 3.6 10.5 * * 0.3 5.3 * 1 20.1 3.3 2.5 6 1.3 1.8 2.5 0.5 2.6 0.3 1.4 2 0.5

1.3 1 2.9 9.8 * * 0.3 6.3 * 1.1 19.8 2.7 2.5 5.8 1.2 1.8 2.6 0.4 2.8 0.3 1.5 2 0.5

1.3 1 2.4 9.3 * * 0.3 7.6 * 1.1 18.9 2.2 2.4 5.3 1.1 1.7 2.6 0.4 2.7 0.2 1.5 1.9 0.5

1.2 1 2 8.9 * * 0.3 9.4 * 1.1 17.7 1.9 2.3 4.6 1.1 1.7 2.5 0.3 2.3 0.2 1.6 1.9 0.4

0 –0.2 –4.0 –1.3 * * –1.7 +3.5 * +1.3 –0.4 –4.0 –0.5 –0.7 –1.0 –0.3 +1.0 –3.1 +1.5 –4.4 +0.6 –0.7 0

–0.8 +0.2 –3.1 –0.8 * * –1.8 +4.2 * –0.8 –1.3 –3.2 –0.6 –2.8 –1.2 –0.8 –0.9 –3.9 –3.0 –4.5 +0.5 –0.2 –2.6

215.5 232.7 251.9 +1.4

+1.6

100.4 97.4

93.7

89.6

85

80

–0.9

–1.2

*The quality of the mortality data is too weak for this site to interpret them in terms of trends (section 4). 1 Based on the standard World population. b Annual rate of change in percent (%). Overall concerned the 1980–2005 period and Recent the 2000–2005 period. c Excluding skin.

Table 5 Estimated number of new cancer cases and cancer deaths in France in men, by year Type of cancer

Number of new cases 1980

1985

Number of deaths

1990

1995

2000

2005

1980

1985

1990

1995

2000

2005

Lip, oral cavity, pharynx Oesophagus Stomach Large bowel Liver Pancreas Larynx Lung Pleura Skin melanoma Prostate Testis Bladder Kidney Brain and CNS Thyroid Non-Hodgkin lymphoma Hodgkin’s disease Multiple myeloma and ID Acute leukaemia Chronic lymphocytic leukaemia

11,883 4987 5344 12,282 1406 1660 4547 16,317 263 764 10,756 977 5560 2448 1365 325 2014 858 949 1058 1090

12,846 5019 5121 13,869 1918 1680 4625 17,951 388 1210 14,190 1157 6512 3018 1540 421 2781 849 1142 1141 1208

13,032 4897 4894 15,478 2594 1860 4490 19,539 516 1775 18,979 1349 7323 3632 1722 571 3610 839 1385 1232 1345

12,506 4644 4714 17,118 3411 2220 4,188 21,148 624 2388 26,760 1544 7882 4280 1913 794 4435 818 1685 1348 1504

11,300 4241 4523 18,582 4257 2848 3760 22,615 674 2935 39,636 1745 8079 4876 2080 1119 5090 798 2038 1488 1670

9531 3733 4405 19,913 5104 3882 3242 23,937 642 3303 62,245 2002 7959 5368 2255 1599 5523 787 2445 1657 1856

5168 4758 5001 7590 * * 3793 15,160 * 298 7001 205 2653 1443 988 151 971 315 684 1047 387

5140 4524 4436 7758 * * 3379 17,151 * 388 8090 173 2925 1675 1174 153 1350 268 795 1071 475

4890 4238 3944 7965 * * 2846 18,849 * 490 8875 144 3145 1891 1352 152 1731 222 919 1115 542

4488 3908 3537 8215 * * 2286 20,153 * 594 9279 118 3297 2088 1500 151 2046 184 1053 1185 587

3933 3527 3207 8488 * * 1738 20,857 * 691 9295 100 3362 2238 1610 150 2226 152 1207 1290 599

3264 3095 2974 8901 * * 1251 20,950 * 772 9202 82 3384 2349 1688 147 2242 127 1393 1447 588

All cancers a

95,138

107,528

120,709

136,322

155,567

183,485

76,795

82,143

85,947

88,080

88,030

86,489

*The quality of the mortality data is too weak for this site to interpret them in terms of trends (section 4). a Excluding skin.

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Table 6 Estimated number of new cancer cases and cancer deaths in France in women, by year Type of cancer

Number of new cases

Number of deaths

1980

1985

1990

1995

2000

2005

Lip, oral cavity, pharynx Oesophagus Stomach Large bowel Liver Pancreas Larynx Lung Pleura Skin melanoma Breast Cervix uteri Corpus uteri Ovary Bladder Kidney Brain and CNS Thyroid Non-Hodgkin lymphoma Hodgkin’s disease Multiple myeloma and ID Acute leukaemia Chronic lymphocytic leukaemia

1397 507 3560 11,522 362 992 227 1595 80 1446 21,704 5136 4287 3403 1589 1241 995 1027 1713 564 916 927 720

1568 572 3299 12,601 463 1197 261 2031 105 1992 25,114 4431 4427 3613 1686 1635 1160 1352 2379 579 1095 1003 825

1780 645 3048 13,709 596 1491 304 2647 135 2611 29,649 3939 4640 3818 1732 2015 1335 1844 3074 592 1296 1,088 941

2043 737 2815 14,872 780 1909 354 3537 170 3240 35,392 3576 4912 4023 1749 2334 1516 2572 3744 613 1530 1186 1072

2360 850 2551 16,041 1019 2483 417 4825 213 3766 42,000 3295 5274 4218 1716 2544 1690 3607 4305 665 1789 1291 1213

2739 988 2389 17,500 1329 3336 493 6714 264 4098 49,814 3068 5774 4375 1720 2581 1865 5073 4701 757 2071 1425 1368

All cancersa

73,712

81,214

91,067

103,470

117,951

135,895

1980 579 620 3735 7563 * * 181 2011 * 324 8689 2258 1448 2461 910 936 710 345 771 195 779 922 283 52,479

1985

1990

1995

2000

2005

619 623 3202 7480 * * 171 2382 * 407 9445 1888 1508 2832 987 1022 886 339 1164 175 878 947 359

659 637 2739 7481 * * 165 2868 * 493 10,130 1605 1574 3104 1041 1108 1056 324 1571 151 987 993 425

697 660 2350 7563 * * 159 3528 * 572 10,697 1393 1652 3270 1080 1194 1203 302 1891 128 1106 1062 472

719 695 2010 7653 * * 158 4428 * 633 11,035 1215 1712 3281 1086 1262 1293 280 2023 107 1230 1154 483

736 755 1782 7964 * * 155 5674 * 668 11,201 1067 1800 3180 1098 1335 1331 256 1961 91 1396 1286 471

54,192

55,804

57,298

58,135

59,273

*The quality of the mortality data is too weak for this site to interpret them in terms of trends (section 4). a Excluding skin.

3.4. Colon and rectum Table 7 Jacknife confidence interval for number of new cancer cases in 2005 Site

Men

Women

Lip, oral cavity, pharynx Oesophagus Stomach Large bowel Liver Pancreas Larynx Lung Pleura Skin melanoma Breast Cervix uteri Corpus uteri Ovary Prostate Testis Bladder Kidney Brain and central nervous system Thyroid Non-Hodgkin lymphoma Hodgkin’s disease Multiple myeloma and immunoproliferative diseases Acute leukaemia Chronic lymphocytic leukaemia

[7,874; 11,189] [3,230; 4,239] [4,114; 4,696] [18,363; 21,466] [4,220; 5,987] [2,992; 4,777] [2,698; 3,789] [20,878; 27,001] [477; 807] [2,724; 3882]

[2,424; 3,052] [871; 1,107] [2,111; 2,665] [16,161; 18,836] [1,044; 1,618] [2,562; 4,110] [403; 586] [6,204; 7,223] [186; 381] [3,576; 4,625] [45,739; 53,887] [2,739; 3,399] [5,310; 6,237] [3,832; 4,914]

[53,614; 70,876] [1,565; 2,435] [7,016; 8,904] [4,790; 5,949] [1,961; 2,548]

[1,454; 1,990] [2,154; 3,011] [1,668; 2,061]

[958; 2,239] [4,920; 6,126] [680; 896] [2,113; 2,780]

[3,286; 6,859] [4,160; 5,238] [632; 885] [1,799; 2,344]

[1,264; 2,051] [1,283; 2,428]

[1,036; 1,811] [944; 1,789]

In France, in 2005, colon–rectum cancer contributed 37,413 new cases, 53% of which occurred in males, causing 16,865 deaths. Age-standardised incidence rates were 37.7 and 24.5 in men and women, respectively, and the most recent trends levelled off. Mortality rates have decreased since 1980 to reach 15.2 in men and 8.9 in women, while the number of cancer deaths increased to reach 8901 men and 7964 women. The increase in the number of cancer deaths was mostly due to the ageing of the population. The difference in the time trends between incidence and mortality was due to better survival, as observed in a population-based study of the FRANCIM network [2,16]. The cumulative risk of colorectal cancer was nearly constant in women born after 1930 (2.6%), while it seemed to reach a maximum of 4.4% in men born in 1930 and decreased slowly afterwards. The cumulative risk of cancer death has decreased slowly since the 1910 cohort, with a recent leveling off over the 1940–1950 period in both sexes (1.4% in men and 0.9% in women). The decrease in incidence observed in the USA has not been observed yet in Europe [17,18]. A high caloric intake and a high meat and processed meat intake are risk factors, while vegetables and dietary fibre consumption are protective. 3.5. Liver Mortality from liver cancer must be interpreted with caution because some secondary cancers are classified as primary

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169

Table 8 Cumulative risk (%) between 0 and 74 years according to birth cohort in men Incidence Type of cancer/birth cohort Lip, oral cavity, pharynx Oesophagus Stomach Large bowel Liver Pancreas Larynx Lung Pleura Skin melanoma Prostate Bladder Kidney Brain and CNS Thyroid Non-Hodgkin lymphoma Multiple myeloma and ID Acute leukaemia Chronic lymphocytic leukaemia All cancers a

1910 2.95 1.72 1.99 3.54 0.40 0.81 1.42 5.37 0.06 0.10 2.73 1.56 0.65 0.33 0.07 0.38 0.26 0.26 0.35 25.59 1930

Testis Hodgkin’s disease

0.22 0.26

Mortality 1920 3.84 1.72 1.54 4.03 0.71 0.62 1.66 5.89 0.13 0.25 4.23 2.00 0.97 0.47 0.09 0.68 0.36 0.29 0.40 28.55 1940 0.23 0.23

1930 4.28 1.66 1.17 4.39 1.08 0.69 1.51 6.28 0.17 0.46 7.99 2.05 1.19 0.58 0.14 0.95 0.45 0.31 0.42 33.25 1950 0.30 0.22

1940 2.99 1.07 0.93 4.13 1.32 1.03 1.00 5.83 0.15 0.60 18.63 1.60 1.27 0.63 0.26 1.13 0.54 0.34 0.44 34.97 1960 0.44 0.21

1950

3.88

5.90

0.62 1.00

35.15 1970 0.51 0.17

1910 1.64 1.73 1.75 2.18 * * 1.42 4.41 * 0.05 1.36 0.70 0.40 0.25 0.06 0.19 0.18 0.76 0.09 19.63 1930 0.09 0.12

1920 1.61 1.46 1.13 1.94 * * 1.21 4.95 * 0.09 1.27 0.71 0.49 0.35 0.05 0.35 0.21 0.57 0.10 19.94 1940 0.05 0.07

1930 1.60 1.31 0.78 1.78 * * 0.92 5.48 * 0.14 1.09 0.67 0.52 0.40 0.04 0.43 0.23 0.48 0.10 19.83 1950 0.04 0.04

1940 0.98 0.80 0.54 1.44 * * 0.41 4.63 * 0.16 0.85 0.51 0.43 0.39 0.03 0.39 0.24 0.40 0.08 15.46 1960 0.02 0.02

1950

1.41

4.10

0.38 0.27

12.74 1970 0.02 0.01

*The quality of the mortality data is too weak for this site to interpret them in terms of trends (section 4). a Excluding skin.

Table 9 Cumulative risk (%) between 0 and 74 years according to birth cohort in women Incidence Type of cancer/birth cohort Lip, oral cavity, pharynx Oesophagus Stomach Large bowel Liver Pancreas Larynx Lung Pleura Skin melanoma Breast Cervix uteri Corpus uteri Ovary Bladder Kidney Brain and CNS Thyroid Non-Hodgkin lymphoma Multiple myeloma and ID Acute leukaemia Chronic lymphocytic leukaemia All cancers a

1910 0.33 0.11 0.84 2.50 0.07 0.18 0.06 0.34 0.02 0.15 4.88 3.57 1.38 0.93 0.37 0.21 0.20 0.17 0.28 0.20 0.19 0.16 16.44 1930

Hodgkin’s disease

0.15

Mortality 1920 0.37 0.12 0.59 2.64 0.10 0.26 0.07 0.51 0.03 0.29 5.71 2.60 1.37 1.02 0.30 0.37 0.31 0.19 0.47 0.26 0.21 0.19 17.59 1940 0.15

1930 0.40 0.14 0.42 2.65 0.16 0.37 0.08 0.77 0.04 0.47 7.11 1.47 1.33 1.06 0.26 0.48 0.38 0.34 0.64 0.31 0.23 0.22 19.14 1950 0.14

1940 0.51 0.17 0.32 2.66 0.24 0.52 0.10 1.17 0.05 0.65 10.49 0.85 1.34 1.02 0.22 0.47 0.41 0.72 0.77 0.35 0.25 0.23 23.24 1960 0.14

1950

2.70

2.49

12.14 0.64 0.90

0.44 0.76

26.42 1970 0.13

1910 0.10 0.11 0.75 1.42 * * 0.05 0.37 * 0.04 1.83 1.25 0.31 0.53 0.14 0.20 0.13 0.09 0.11 0.15 0.69 0.04 10.05 1930 0.07

*The quality of the mortality data is too weak for this site to interpret them in terms of trends (section 4). a Excluding skin.

1920 0.12 0.10 0.42 1.16 * * 0.04 0.49 * 0.07 2.06 0.81 0.30 0.65 0.12 0.21 0.21 0.07 0.21 0.15 0.48 0.04 9.69 1940 0.04

1930 0.13 0.11 0.26 0.97 * * 0.04 0.68 * 0.09 2.12 0.40 0.28 0.68 0.10 0.20 0.26 0.05 0.25 0.16 0.38 0.04 9.02 1950 0.03

1940 0.12 0.11 0.19 0.85 * * 0.03 0.84 * 0.10 2.00 0.22 0.26 0.58 0.08 0.18 0.24 0.03 0.22 0.17 0.31 0.03 8.06 1960 0.02

1950

0.87

1.55

1.66 0.18 0.38

0.23 0.13

7.40 1970 0.01

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cancers, leading to over-reporting. The incidence rate has increased in men since 1980 but has slowed down slightly for the most recent period: the annual rate of change was +3.8% over the entire period and +1.9% over the 2000–2005 period. In women, a constant increase in incidence was shown, with an annual rate of change of approximately +4% over the 1980– 2005 period. The increase in incidence rates may be explained by better management of cirrhosis, particularly in alcoholics, which results in more time for the development of liver cancer. It is also possible that the increasing number of hepatitis C cirrhoses and the recent observation of metabolic syndromes through fatty degeneration of the liver may have played a role in the increase in liver cancer incidence [19]. 3.6. Pancreas It is well-known that deaths from pancreas cancer are overreported. In 2005, age-standardised incidence rates were equal to 7.7 and 4.7 in men and women, respectively. An increase in incidence rates has been observed in men and women since 1980. We speculate that this trend was the result of improved diagnostic procedures (advances in medical imaging). These considerations are not sufficient to explain the trends observed and an increase in the risk factors remains plausible. However, the causes of this cancer are currently poorly elucidated. 3.7. Larynx In 2005, larynx cancer contributed 3735 cases, 87% of which occurred among men. In men, the age-standardised incidence rates decreased from 14.3 in 1980 to 7.1 in 2005; resulting in a 2.7% annual rate of change. Age-standardised incidence rates regularly increased in women over the same period (annual rate of change, +2%), albeit remaining at far lower rates than in men, and reached approximately 1.0 in 2005. Age-standardised mortality rates decreased in both men and women over the 1980–2005 period, with a more pronounced decrease in men during the last five years (annual rate of change, 8.3%). It is well-accepted that the reduction in alcohol and tobacco consumption explains the majority of the decrease in incidence in men. Inversely, the observed trends in women are consequences of the rise in tobacco consumption, which occurred more recently than in men. Human papilloma virus is now considered as a possible risk factor for larynx cancer [20]. 3.8. Lung With 26,624 deaths in 2005, lung cancer is the greatest contributor to cancer deaths. Among 30,651 new cases, 78% occurred among men. In 2005, the age-standardised incidence rates in men and women were 50.5 and 12.6, respectively. In men, the incidence rates decreased by 0.5% and mortality rates decreased by 1.7% over the 2000–2005 period. In contrast, incidence and mortality increased in women. The agestandardised incidence rate was 3.6 in 1980 and 12.6 in 2005, with a +5.1% annual rate of change. The age-

standardised mortality rates increased from 3.9 in 1980 to 9.4 in 2005, with an annual rate of change of +3.5%. In men, the cumulative risk of lung cancer has been stable since the 1930 cohort, equal to 6%. In women, it was 0.3% for the 1910 cohort and 2.5% for the 1950 cohort, i.e. an increase by a factor of 8. Although the age-standardised incidence rates are still increasing in women in most European countries, a significant decrease – correlated with a decrease in tobacco smoking – is seen in the youngest cohorts in some of these countries [21,22]. 3.9. Pleura This cancer site was not described in the previous analysis [1]. In men, incidence rates reached their maximum between 1995 and 2000 and then began to drop, with a –3.4% annual rate of change in 2000–2005. In women, this phenomenon for incidence was not observed. These results should not be interpreted as a decrease in mesothelioma incidence. A collaborative study with the Programme national de surveillance du me´sothe´liome is currently attempting to obtain reliable estimates for mesothelioma. 3.10. Skin melanoma Skin melanoma cancer contributed 7401 new cases in France in 2005, 45% of which occurred in men. It was deemed to have caused 1440 deaths. The age-standardised incidence rates in men and women in 2005 were 7.6 and 8.8, respectively. The annual rates of change were 4.7% and 3.4% over the 1980–2005 period in men and women, respectively, whereas the corresponding results for the most recent period, 2000–2005, fell to 0.8 and 0.5%. Similarly, the increase in mortality was smaller during the most recent period in men, and a slight decrease was observed in women. These trends, which require confirmation in the future, might be explained by an increase in earlier detection of in-situ tumours resulting from a growing public awareness of the dangers of sun exposure. A stabilisation of incidence had already been reported in some countries of Western Europe [23–25]. Evidence of different temporal trends according to clinical characteristics at diagnosis has been published [26]. 3.11. Breast Breast cancer remains the most frequent cancer in women with an age-standardised incidence rate of 101.5, which contributed 49,814 cases in 2005. It was also the first cause of cancer death in 2005 with 11,201 deaths in women and with an age-standardised mortality rate of 17.7. Incidence trends showed a constant increase with an annual rate of change of +2.4% over the 1980–2005 period. For the cohort born between 1920 and 1940, the cumulative risk of cancer increased from 5.7 to 10.5%, but this increase seemed smaller for cohorts born after 1940. Mortality started to decrease in 1998. The annual rate of change was –1.3% over the 2000–2005 period. Changes in lifestyle risk factors and mass or individual screening contribute to the increase in incidence. Screening also

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contributes to a lesser but unknown extent, and in combination with improvements in therapeutic strategies, to the decrease in mortality. We did not observe a similar decline in incidence to that reported in the United States, which was largely interpreted to be a consequence of less hormone replacement therapy [27]. In comparison with other European countries, France has a relatively high incidence [15].

showed that men aged 50–70, the most targeted by the PSA test in recent years, contributed most to that increase. Although similar incidence trends are observed in most European countries [29,30], France is among the European countries with the highest incidence.

3.12. Cervix uteri/Corpus uteri

In 2005, testis cancer contributed 2002 new cases and 82 deaths. The age-standardised incidence rate increased from 3.4 in 1980 to 6.4 in 2005, representing a +2.5% annual rate of change. Mortality has decreased sharply since 1980, with a 4.4% annual rate of change over the 1980–2005 period. The testis cancer incidence rate has risen in most populations worldwide, although that increase was greater in Europe [31]. The substantial decline in mortality may be mainly explained by the introduction of platinum-based chemotherapy in the 1970s.

The new distribution of mortality from these two cancers gave a larger share to the cervix uteri; so the number of cancer deaths and mortality rates was slightly higher in comparison with our previous report [1]. Cancer of cervix uteri contributed 3068 cases in 2005 and 1067 deaths with, respectively, agestandardised rates of 7.1 and 1.9. From 1980 to 2005, the annual rate of change for incidence was equal to 2.9%. The annual rate of change for mortality reached 4%. It is well-accepted that the generalised practice of cervical cancer screening is largely responsible for that regular and major decrease of cervical cancer incidence. This favourable progression has not yet been observed in some Eastern Europe countries, as recently demonstrated by Arbyn et al. [28]. In 2005, cancer of the corpus uteri contributed 5774 new cases and 1800 deaths. The age-standardised incidence rate was equal to 10 and the mortality rate was 2.3. A slight decrease in both incidence and mortality between 1980 and 2005 is continuing.

3.15. Testis

3.16. Bladder

Analysis of time trends for ovarian cancer incidence was based on invasive tumours only, excluding borderline tumours. Ovarian cancer contributed 4375 new cases and 3180 deaths in 2005, with an age-standardised incidence rate of 8.1 and an agestandardised mortality rate of 4.6. Trends for incidence have shown a slight decrease since 1995, with a 1% annual rate of change over the recent 2000–2005 period. This decrease was greater for mortality, with a 2.8% annual rate of change over the same period. The protective effect of oral contraceptives might be the cause of a decrease in incidence in the younger cohorts. In comparison with other European countries, France has a relatively low incidence.

The international recommendations for bladder cancer registration varied over the study period [32]. As a result, the estimates presented here, considering only invasive tumours, should be interpreted with caution. In 2005, 7959 new cases were diagnosed in men and 1720 in women. The incidence rates were 14.6 and 2.1 in men and women, respectively. Regarding mortality, 3384 cancer deaths in men and 1098 in women were observed in 2005. In men, over the 2000–2005 period, the annual rates of change were equal to 2.5 and 2.1% for incidence and mortality, respectively. In women, over the 1980–2005 period, the annual rates of change were equal to 1.3 and 1% for incidence and mortality, respectively. This decrease in men may be related to changes in the prevalence of risk factors (tobacco use, occupational exposures). However, in women, a correlation between trends in tobacco smoking and bladder cancer incidence was not seen. This difference of trends between ‘‘lung’’, ‘‘lip, oral cavity and pharynx’’ cancers and ‘‘bladder’’ cancer, all tobacco-related cancers, was also observed in the USA [33]. For mortality, decreasing trends were observed in both genders, with a more pronounced decrease in men (annual rate of change equal to 2.1%) during the 2000–2005 period.

3.14. Prostate

3.17. Kidney

In 2005, prostate cancer was the most frequent and contributed 62,245 cases. With 9202 deaths, it ranked third in terms of the number of cancer deaths in men. The trend for incidence showed the greatest increase, with an annual rate of change equal to +8.5% over the recent 2000–2005 period. The cumulative risk of cancer increased until reaching 18.6% for the 1940 cohort. On the other hand, the trend for mortality showed a decrease over the 1980–2005 period, with an annual rate of change equal to 0.9%, reaching 2.5% for 2000–2005. The dramatic increase in incidence rates is clearly explained by the use of prostate-specific antigen. In comparison with our previous estimates, the age-specific incidence rates in 2005

In 2005, 7949 new cases occurred, 68% of which occurred among men, and 3684 cancer deaths (64% among men). The age-standardised incidence rates were 11.4 in men and 4.5 in women. The trends for incidence rates have stabilised for men and declined slightly over the last few years in women, with the annual rate of change over the recent period equal to +0.3% in men and 1.4% in women. Mortality rates showed a more pronounced decrease during the recent 2000–2005 period. For both genders, the effect of fortuitous diagnosis by medical imaging has probably reached its maximum. The recent improvement in survival of kidney cancer may have played a role in the decline in mortality [2].

3.13. Ovary

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3.18. Brain and central nervous system In contrast with our previous paper, only malignant tumours were counted as incident cases. Interpretation of brain and central nervous system cancer incidence trends over time is difficult for several reasons, including changes in coding practices. In 2005, the age-standardised incidence rates were equal to 5.7 and 4.2 and age-standardised mortality rates were equaled to 3.9 and 2.5 in men and women, respectively. An increasing trend was observed in both genders, but its amplitude was reduced during the most recent period. Mortality trends changed over the whole period in both genders, with a positive annual rate of change for 1980–2005 but a negative annual rate of change for the recent 2000–2005 period. 3.19. Thyroid With 6672 new cases estimated in 2005, 76% of which occurred among women, thyroid cancer ranked third among cancers in women. The age-standardised incidence rates in men and women were, respectively, 4.2 and 12.7, while the agestandardised mortality rates were equal to 0.3 in both genders. The trends for age-standardised incidence rates contrasted with the trends of age-standardised mortality rates. The annual rates of change in incidence rates were approximately equal to +6% in both genders over the entire period, while the annual rates of change for mortality decreased. The increase in incidence rates is explained by an increase in papillary carcinoma and partly by micro-carcinoma, which are both associated with a good prognosis [34], while the decrease of mortality rates is explained by a decrease in the incidence rates of anaplasia, which is associated with a poor prognosis [35]. Changes in thyroid cancer incidence correlate strongly with changes in medical practices: the effects of earlier diagnosis on the increase in incidence of thyroid cancer have already been shown [36]. 3.20. Haematological sites Non-Hodgkin lymphoma (NHL) was the most frequent haematological malignancy in France. Incidence trends showed an increase in both genders over the 1980–2005 period with the figures levelling off over the 2000–2005 period. This stabilisation has already been reported in the USA and in Europe [37,38]. Although known risk factors such as altered immune function and some infectious agents appear to play a role in the aetiology of NHL, these factors explain only a small proportion of cases, and trends for incidence cannot be interpreted using those factors alone [39]. The decrease in mortality since the mid-1990s may be the consequence of better patient management. Age-standardised incidence rates for Hodgkin disease in 2005 were 2.3 in men and 2.5 in women and age-standardised mortality rates were 0.3 and 0.2 in men and women, respectively. Incidence decreased in men but increased in women. However, the increase in incidence rates in women showed great variability between registries and should be

interpreted with caution. On the other hand, mortality decreased in both genders; this was most probably caused by improved therapeutic strategies. As for multiple myeloma, both incidence and mortality increased. However, the trends were less pronounced over the last period, with a reduced annual rate of change compared to the whole period. The incidence of acute leukaemia increased over the whole period, with an annual rate of change equal to +0.9% in both genders. Mortality decreased slowly in both genders and stabilised over the recent 2000–2005 period, with an annual rate of change of –0.2% in both genders. The incidence of chronic lymphocytic leukaemia increased slightly over the 25-year period. However, the age-standardised mortality rates decreased over the recent period, with an annual rate of change equal to 2.8 and 2.6% in men and women, respectively. The decrease in mortality may be explained by the introduction in the therapeutic strategy of purine analogues and monoclonal antibodies (anti-CD20, anti-CD52) adapted to new prognostic factors (Ig VH mutation status). 4. Discussion The previous study on incidence and mortality trends in France showed large quantitative and qualitative changes in the cancer burden between 1980 and 2000 [1]. The main message was the recent divergence of incidence and mortality trends. The present study confirmed this result. Moreover, while the main feature of the trend pattern has been reinforced by these extended results, other trends were revealed. The present study, based on 17 French cancer registries, updates our previous results [1] by adding new registries and a longer period of observation. Taken together, these French cancer registries record incidence rates in a population of more than 8.3 million persons (more than 9.3 million for digestive tract cancers) and some of these registries have been providing reliable observations for more than 25 years. Although the ability of this network to measure French cancer incidence has considerably improved, we anticipated a possible lack of representativeness using mortality as a geographical correlate of incidence, which has been a classical way to correct for a possible remaining bias and to provide national statistics. In addition, considering the size of the registered population, it can be seen that the precision of the incidence measure in recent years is similar to that obtained in the Nordic countries where the registered populations are slightly smaller. National mortality data were modelled in order to smooth out random fluctuations and to provide a more legible structure of the detailed time trends. When compared to the observed mortality data, however, the estimated and observed world agestandardised rates are very close. In comparison with our previous report, the statistical method for this updated study was significantly modified. According to Eq. (1), the incidence/mortality ratio was used in both studies to provide national incidence. It is important to mention that this approach did not assume identical incidence/ mortality ratios for each registry and for France. This requires

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the incidence/mortality ratio in the entire area covered by all the registries to be a good estimate of the incidence/mortality ratio of the entire country. For most cancer sites, when comparing the estimates to those obtained from a direct extrapolation of the rates relative to the cancer registry area, the correction was minimal (results not shown). The period of observation covered seven additional years compared to the previous study and it became possible to propose a more complex model than the robust age-cohort model. However, since the birth cohort effect played a prominent role [40], we remained in the age-cohort paradigm and modelled an interaction between age and cohort effects, which allowed different patterns of age-effect for different cohorts. Modelling this interaction was necessary to fit data such as those related to ‘‘lip, oral cavity, pharynx’’ for which a decrease in alcohol consumption leads to complex age and cohort effects. However, a better fit does not automatically provide a better projection; therefore, we had to consider the extrapolation of the interaction effect with caution. For example, the estimates of the cumulative risk of cancer between 0 and 75 years for the 1950 cohort correspond to a projection up to 2025. Reporting the cumulative risk up to the 1940 cohort, or exceptionally up to the 1950 cohort when this latter was reasonably well-observed, limits such uncertainties. Unlike our previous estimates, those reported here were not obtained using five-year age groups. We preferred to estimate the age, period, and cohort effects using smoothing splines from one-year data. This approach avoided information loss when estimating age-specific rates. Carstensen gave a comprehensive and pertinent review on the tabulation of data and on modelling the effects in the context of age-period-cohort models [41]. All cancers taken together, the number of cases increased over the last 25 years by 89% (93% in men, 84% in women), while the number of cancer deaths increased by only approximately 13% in both genders. Using a method described earlier [42], we were able to calculate that a 22% incidence increase in the number of cases stems from a population increase, 18% from the change in the age structure of the population and 49% from changes in cancer risks: 21, 24 and 48% in men and 22, 16 and 46% in women, respectively. For mortality, analysing the changes in the number of cancer deaths, these figures become 13%, 24%, 24% for both genders combined, 12, 30, 29% in men and 13, 22, 22% in women, respectively. Thus, the change in the number of cancer deaths was much lower than that predicted by the demographic changes. The present study reinforced the evidence of a large divergence between incidence and mortality trends. Given the longer period of observation, our analysis was able to demonstrate a clear decrease in mortality for many cancer sites, especially in men. The decrease over the recent 2000– 2005 period was steeper. Note that age-standardised mortality rates decreased by 22% between 1980 and 2005. The same calculation between 1980 and 2000 showed a 15% decrease. The latter estimate was –10% when considering only data until 1997 [1]. As explained in the previous study, the combined effects of the decrease in the incidence of cancers with poor survival and the increase in the incidence of cancers with a fair

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prognosis may partly explain the divergent trends in incidence and mortality. Among cancer sites with poor survival, all alcohol-related cancers except liver cancer showed the same decreasing trend in men, both in incidence and mortality. However, despite a very pronounced decrease in mortality rates over the 2000–2005 period, these rates were still elevated when compared to other European countries. In women, the situation was the opposite: the incidence of alcohol-related cancers increased, although the rates remained low. The improvement in survival of patients with cirrhosis is usually mentioned as an explanation for the increase in liver cancer, which now have enough time to develop. Lung cancer is the most frequent aggressive cancer. A recent and slight decrease in its incidence rates in men was observed. However, cumulative risks were stable in cohorts born after 1940, so this slight incidence decrease may be temporary. In contrast, incidence rates increased steadily in women as a consequence of the increase in tobacco smoking among women born after World War II. Lung cancer is now the second cause of death from cancer after breast cancer in women, colorectal cancer being the third (Fig. 1). As already mentioned, our results regarding pleura cancer incidence – showing a very recent decrease – should not be interpreted as a decrease in mesothelioma incidence; a dedicated study is currently being conducted in France. Since mortality was greater than incidence for that cancer site, trends in mortality were too difficult to interpret and were finally not shown. Among the cancer sites with rather poor survival, stomach cancer, which showed a continuing decrease in incidence, contributed substantially to the decrease in overall mortality. The risk factors responsible for these changes still need to be more precisely identified. The increase in the incidence of less aggressive cancers is related to the influence of medical practices, albeit the relation is still difficult to quantify. Prostate cancer remains the typical example: in 2005 the age-standardised rate was five times greater than in 1980. In 2005, prostate cancers contributed 34% of all cancer cases in men, up from only 11% in 1980. Thus, as already mentioned in our previous report, this cancer site is, to a large extent, responsible for the increase in cancer incidence in men. The increase in prostate cancer is the result of its early detection with PSA [43], a method which is now widely used in France, despite the absence of a demonstrated benefit [44,45]. Even if a slight decrease in mortality has been seen in recent years, it is not clear that it was associated with screening. However, it may not compensate widespread overdiagnosis in terms of the risk–benefit ratio [29,46,47]. In Denmark, where PSA testing is discouraged, the increase in prostate cancer incidence is considerably less than in other European countries. Two randomised trials evaluating the impact of a mass screening program on prostate cancer mortality are being conducted and should be published soon [48]. The example of breast cancer is more complicated. A massscreening program was initiated on an experimental basis in several French departments in 1990 and was generalised in 2003. In parallel, many women were screened on an individual basis at their own request or following the prescription of a gynaecologist. As a consequence, a large increase in in-situ

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cancers and in small cancers was observed among middle-aged women. At the same time, breast cancer incidence increased because important changes in risk factors occurred in successive birth cohorts, especially the postponement of the first child [49]. Although a slight inflexion in the incidence increase could be noted for the younger cohort, this incidence increase is still affecting older women of the previous generations. It is therefore difficult to quantify the increase in breast cancer due to screening. A decline in incidence has been reported in the United States [27], which has been interpreted as a consequence of the reduction in hormone replacement therapy. A similar decline has been very recently reported in France [50] on basis of data from the Assurance maladie (the national health insurance fund) covering the 2000– 2006 period. The FRANCIM incidence for the same period will be available in 2010; updated estimates could then be produced and compared. The decrease in breast cancer mortality began at the end of the 1990s and is now well-established. Part of the decrease may be attributed to the improvements in therapy that occurred in the middle of the 1980s and, to an unknown extent, to screening. Among other cancers amenable to early detection, melanoma and thyroid cancers are still increasing substantially. This increase is difficult to attribute to recent changes in risk factor prevalence. For those cancers that are better detected based on progress in imaging technologies, kidney and central nervous system cancers tend to show a stabilizing incidence. As for the increase in pancreatic and liver cancer incidence, there is considerable uncertainty as to its causes and its level. Imaging may have played a role in improving the diagnosis of pancreatic cancer, and improvement in survival rates for cirrhosis has certainly played a role in the increase in liver cancer incidence; however, data for these particular sites still lack sufficient quality and the quantification of the increase should be interpreted with caution. For these two cancers, the trends for mortality may be almost entirely artefactual. Because of problems encountered in reliably classifying cases and deaths in various haematological malignancy subtypes, it was not possible to obtain reliable national incidence estimates and temporal trends for each subtype of leukaemia. New studies will soon provide national incidence estimates according to the WHO classification published in 2001, which makes more sense than the one used here. The increase in non-Hodgkin lymphoma incidence is continuing, but, as observed in other countries, at a slower pace. This may indicate changes in environmental exposures. To analyse this trend, it will be necessary to obtain results by sub-categories with specific aetiological studies. The interpretation of observed time trends in cancer has always been a subject of debate. Many contradictions may arise from a limited examination of the data. Long-term and recent trends, period and birth cohort trends, and age-standardised and age-specific trends do not necessarily convey the same message. A fair interpretation should be based on a synthesis of these various points of view. It was seen above that changes in classification, changes in competing causes of death, and changes in detection methods have all played an important role

in the trend patterns observed in France, above and beyond the demographic changes, which, taken alone, explained almost half the increase in the number of cases. Considering together the cancer sites with an increasing risk, it may be calculated that half the number of cases attributable to the risk increase in women are breast cancer cases and about 70% of the cases attributable to the risk increase in men are prostate cancer cases. Reinforcing the main conclusion of the Inserm expert commission [51] following the last publication on cancer trends in France, we can confirm that changes in demography and in medical practices play the prominent role in the updated trend patterns. Some researchers, considering correctly that the changes in incidence are not entirely explained by these two factors, proposed that the environment stricto sensu is responsible for the yet unexplained increases [52–54]. This hypothesis is certainly worth considering and studying, but, at present, it is impossible to quantify the contributions of these environmental factors to the increase in the number of cancers. Our lack of knowledge in this field, which has precluded proving a causal relationship and quantifying the level of exposure, has been recently underlined by two publications [55,56]. 5. Nota More detailed results for each cancer site are available at: http://www.invs.sante.fr/surveillance/cancers/estimations_ cancers/default.htm. Acknowledgement The authors thank Dr J. Iwaz, PhD and scientific advisor for his assistance in editing the manuscript. References [1] Remontet L, Esteve J, Bouvier AM, Grosclaude P, Launoy G, Menegoz F, et al. Cancer incidence and mortality in France over the period 1978–2000. Rev Epidemiol Sante Publique 2003;51(1 Pt 1):3–30. [2] Bossard N, Velten M, Remontet L, Belot A, Maarouf N, Bouvier AM, et al. Survival of cancer patients in France: A population-based study from The Association of the French Cancer Registries (FRANCIM). Eur J Cancer 2007;43(1):149–60. [3] Hill C, Doyon F. Age in completed years versus age reached during the year. Rev Epidemiol Sante Publique 2005;53(2):205–8. [4] Clayton D, Schifflers E. Models for temporal variation in cancer rates. I: Age-Period and Age-Cohort models. Stat Med 1987;6:449–67. [5] Clayton D, Schifflers E. Models for temporal variation in cancer rates. II. Age-Period- Cohort models. Stat Med 1987;6:469–81. [6] Esteve J, Benhamou E, Raymond L. Statistical methods in cancer research. Descriptive epidemiology. IARC, Press, 1994. [7] Royston P. A strategy for modelling the effect of a continuous covariate in medicine and epidemiology. Stat Med 2000;19(14):1831–47. [8] Hastie T, Tibshirani R. Generalized additive models. London, New York: Chapman and Hall; 1995. [9] Green PJ, Silverman BW. Nonparametric regression and generalized linear models: a rougness penalty approach.. London: Chapman and Hall; 1994. [10] Curado.M.P., Edwards B, Shin.H.R., Storm.H., Ferlay.J., Heanue.M. et al. Cancer incidence in five continents, vol. 9 2007 ed. Lyon: IARC Scientific Publications No. 160, 2007.

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