Cancer Incidence and Mortality in the Czech Republic
Authors:
L. Dušek 1; J. Mužík 1; E. Gelnarová 1; J. Fínek 2; R. Vyzula 3; J. Abrahámová 4
Authors‘ workplace:
Institute of Biostatistics and Analyses, Faculty of Medicine and Faculty of Science, Masaryk University, Brno, Czech Republic
1; Department of Oncology and Radiotherapy, University Hospital, Plzeň, Czech Republic
2; Department of Comprehensive Cancer Care, Masaryk Memorial Cancer Institute, Brno, Czech Republic
3; Department of Oncology, Thomayer University Hospital, Prague, Czech Republic
4
Published in:
Klin Onkol 2010; 23(5): 311-324
Category:
Original Articles
Overview
Backgrounds:
The Czech Republic is ranked among those countries with the highest cancer burden in Europe and worldwide. The purpose of this study is to summarize long-term trends in the cancer burden and to provide up-to-date estimates of incidence and mortality rates from 2007.
Material and Methods:
The Czech National Cancer Registry (CNCR) was instituted in 1977 and contains information over a 30-year period of standardized registration covering 100% of cancer diagnoses and the entire Czech population. The analysis of CNCR is supported by demographic data of the Czech Republic and by the Death Records Database as civil registration systems. The epidemiology of malignant tumours in the Czech population is available online at www.svod.cz.
Results:
All neoplasms, including non-melanoma skin cancer, reached a crude incidence rate of almost 736 cases per 100,000 men and 648 cases per 100,000 women in 2007. The annual mortality rate exceeded 263 deaths per 100,000 population; each year, more than 27,000 persons die of cancer. The overall incidence of malignancies has increased during the last decade with growth index + 26.4% (1997–2007) while the mortality rate has stabilized over this time span (growth index in 1977–2007: –2.5%). Consequently, the prevalence has significantly increased in the registration period and in 2007 it exceeded 400,000 cases. In addition to the demographic ageing of the Czech population, the cancer burden is increased by the growing incidence of multiple primary tumours (recently more than 11% of the total incidence). The most frequent diagnoses include colorectal cancer, lung cancer, breast cancer and prostate cancer. Although some neoplasms are increasingly diagnosed at an early stage (e.g. proportion of stage I + II in female breast cancer: 71.9%, skin melanoma: 81.3%), in general early diagnostics is insufficient in the Czech Republic. This is the case even for highly prevalent colorectal carcinoma (only 43.2% of incident cases recently diagnosed at stage I or II).
Conclusion:
The Czech Republic is well equipped with high-quality and functional facilities for collecting and analysing population-based data on malignant tumours. The data survey has enabled the priorities of cancer management in the Czech Republic to be defined. This will undoubtedly lead to a sustained reduction in late diagnosed cases and a reduction in the remarkable regional differences in diagnostic efficiency.
Key words:
cancer epidemiology – incidence – mortality – Czech Republic
Acknowledgements
Validation of the Czech National Cancer Registry and population based monitoring of cancer disparities are supported by grant “Addressing Cancer Disparities in Central and Eastern Europe” Bristol Myers Squibb Foundation, 2009– 2011 (Project: National Information System for the Assessment and Communication of Cancer Care Results and Quality in the Czech Republic). The authors also greatly acknowledge professional support of data managers of the Czech National Cancer Registry, as well as excellent collaboration with the Institute of Health Information and Statistics of the Czech Republic (IHIS).
Backgrounds
Cancer epidemiology is of an ever growing importance due to the high incidence rates of malignant tumors [1,2]. In recent years, several comprehensive worldwide and European summaries of cancer incidence and prevalence have been published [3– 5]. These reports are unambiguous data based evidence of a rapid increase of cancer incidence in most of European countries. According to Ferlay et al [5] there were 3,191,000 diagnosed cancer cases (excluding nonmelanoma skin cancer) and 1,703,000 deaths from cancer in Europe in 2006. The same authors concluded that the total number of new cases of cancer in Europe appears to have increased by 300,000 since 2004. Therefore, the cancer is an important public health problem in Europe with only partially effective measures how to diminish the continuous growth of burden. The Czech Republic represents no exception in this respect; quite the opposite, the Czech population ranks among the most burdened countries worldwide [6].
The current role of epidemiology is not purely descriptive. Knowledge on age specific or stage specific trends is necessary to evaluate effectiveness of diagnostic processes, to identify weak points in the management of cancer care or to analyze associations with therapeutic outcomes [7]. Among all health care end points of population based cancer registries, survival occupies dominant position. Recently, a series of excellent articles summarizing cancer related survival in European countries has been published [8– 11]. Although significant improvement in reached survival rates have been reported for most of the European countries, there are still apparent regional differences, mostly associated with late diagnosis of advanced disease stage and with more o less specific care disparities. Based on current epidemiological trends, it seems that promising modern research technologies and onset of personalized medicine have not yet been effectively translated into cancer control. Epidemiologic data can thus strategically contribute to the management of this field of medicine [12].
Relevant epidemiologic analyses supporting control and planning of cancer prevention, diagnostics and therapy require population data rich in available parameters. Particularly records identifying morphology and clinical stage of tumors are important. Such clinical registries enable monitoring of early detection of cancer which is currently major area of interest in Europe [13], closely related to survival of cancer patients. Cancer population registries form an indispensable component of functional information systems for monitoring of organized screening programmes [14].
However, not all national cancer registries can provide such complex information and therefore many epidemiologic summaries covering large geographic areas cannot address the health care topics adequately. International epidemiologic surveys also often suffer from partially inconsistent data from participating countries or from interruption in time as it was the case of the Europe Against Cancer Programme of the European Commission [15]. Therefore separate processing of national databases leading to extraction of clinically relevant knowledge is still of a great value. That is why we prepared this overview of recent cancer epidemiology in the Czech Republic. This article presents cancer incidence and mortality in the Czech population, utilizing more than 30 years experience with nationwide cancer data collection. Up to date estimates of incidence and mortality rates from period 2006– 2007 are presented in the context of long term trends. We take not only general descriptive approach, detailed stage specific trends and regional differences are discussed as well.
Data sources and methods
Demographic data
As a standard part of population monitoring, the Czech Statistical Office administrates data on the demographic structure of the Czech population and makes it available on its website [16,17]. This fully consolidated data source describes the main demographic characteristics of the Czech population, such as the total population, the age structure, life expectancy, as well as predictions up to 2050. Basic demographic characteristics of the Czech population are summarized in Tab. 1.
Czech National Cancer Registry (CNCR)
The CNCR has been maintained since 1977 when it was instituted as a national database covering 100% of cancer diagnoses and the entire Czech population. The most recent validated outcomes are from 2007 and the CNCR database contains more than 1.6 million records. The registration of malignant neoplasms is stipulated by the legislation and is obligatory. The CNCR is a part of the National Health Information System (NHIS) and is administered by the Institute of Health Information and Statistics of the Czech Republic [18]. The CNCR is accepted as a key database component of the Czech National Cancer Control Programme, designated to report regular and timely estimates of the cancer burden in the Czech population. For the purpose, automated analytic tools with outputs in the final form were developed. The CNCR is equipped with an information system which, among others, provides free accessible an analytical web portal (www.svod.cz) [19].
Incidence data and associated attributes
The CNCR contains personal data on patients, data describing malignant tumors and diagnostic details (including morphology classification and stage), data on patients‘ treatment, as well as data on post treatment follow ups. The registration of a new incident case begins with the cancer diagnosis, its morphological verification and an accurate staging. Subsequently, basic records on primary therapy (employed modalities), reasoning of therapeutic strategy, follow up data and/ or deaths are transferred into the registration forms. The forms are directly linked to the database on the basis of standardized data model and data processing rules [20]. Malignant neoplasms were recorded according to the International Classification of Diseases for Oncology (ICD O, tenth revision) [21]. Tumours are staged on the basis of TNM classification system [22]. For the purposes of this article, all cases recorded in the CNCR, including DCO records, were included among incident cases. Identification of multiple cancers in the same person was accurately controlled in the CNCR database, based on strict recognition of individual code of a patient, date of the diagnosis and diagnostic typology of multiple cancers.
Mortality data
The Czech legislation requires all deaths in the Czech Republic to be registered in the Death Records Database, a civil registration system [17]. For this purpose, standardized Death Certificates (internationally recommended by WHO, [23]) are designed to collect precise data on the cause of death in each individual, typically performed and proved by general practitioner. The causes of death are classified according to the International Classification of Diseases (ICD 10), which provides standardized nomenclature in this field [21]. This system ensures comparability of official Czech mortality data [17] with common international reporting. The coding of underlying cause of death can be controlled against independently and timely filled National Cancer Registry. The CNCR serves as another source of mortality data in the Czech Republic. Here, the individual records on the cause of death according to the Death Certificate are directly linked to diagnostic data on decedents, which can be used to code cause specific mortality with respect to different cancer diagnoses. Death of a given person from malignant tumour is accurately indexed with respect to the main cancer diagnosis in accord with the immediate or the primary cause of death. So the Czech system allows the data managers to code distinct cancer entities and the records on causes of death are finally kept separately in two information systems. The system makes it possible to check the correctness of CNCR data retrospectively, and to verify the validity of mortality data on cancer patients according to internationally accepted rules [24,25], as discussed in [5].
Data analysis
Basic epidemiologic measures as crude incidence and mortality rates, age standardized rates and lifetime cumulative cancer rates were calculated according to widely accepted international guidelines [26,27]. Cumulative risk is expressed as the probability that an individual will develop the given cancer type during age span 0– 74 years, in the absence of other competing causes of death. Annual incidence and mortality rates per 100,000 population (crude incidence) were calculated by gender and related to the Czech population structure in 2007 [16]. Age standardized rates adjusted for the World and European population were calculated using age standards according to Waterhouse et al [28].
Results
Czech Republic belongs to the group of countries with the highest cancer burden, mortality from cancer contributes to the overall population mortality by 26.5% (Tab. 1). The highest relative proportion of mortality from cancer in relation to the other competing causes of death is registered in age group 50– 64 years (Tab. 2). Male population is ranked worldwide in the 7th position in cancer incidence and in the 18th position in cancer mortality, women population occupies 15th place in worldwide statistics of incidence and 36th position in mortality ranking (Tab. 3). In 2007, there were 71 757 (691.2 per 100 000 people) new incident cases of all cancers including skin neoplasms (C00– C97). In total, 27 359 cancer deaths were registered in 2007 (263.5 per 100 000 population) (Tab. 3). Crude incidence rate continuously increases with the growth index in the last decade 26.4 % (1997– 2007) while the crude mortality rate was stabilized in late 1990s and recently it has become to decrease with growth index –5.4% over time range 1997– 2007 (Fig. 1, Tab. 3– 4). Growing incidence and stabilized mortality necessarily increase prevalence which exceeded 400,000 of cases in 2007 (Tab. 3).
The age standardized incidence andmortality rates (World and European age standard) as well as crude incidence and mortality rates are presented in Tab. 5– 6 by sex and for all main cancer diagnostic groups. Following types of cancer are most frequent in men population (absolute number in 2007): prostate cancer (5,094), followed by nearly equally incident colorectal cancer (4,638) and lung cancer (4,630). In women, the breast cancer is significantly most frequently diagnosed (6,500 incident cases in 2007), followed by colorectal cancer (3,188), uterus cancer (1,771) and lung cancer (1,762). The highest value of lifetime cumulative risk (0– 74 years) was observed in breast cancer (women: 7.75), prostate cancer (men: 7.31), lung cancer (men: 6.82) and colorectal cancer (men: 6.44).
In addition to demographic ageing of the Czech population, the cancer burden is increased by growing incidence of multiple primary tumors. Data in Tab. 7 documents significantly growing contribution of multiple incident cases (both synchronous and metachronous) to the overall incidence. In most prevalent cancers, the rate of multiple diagnoses in the same patients forms more than 11% of the overall incidence (1998– 2007).
The database of CNCR offers accurate stratification of newly diagnosed cases according to clinical stage (Fig. 2, Tab. 8). It is evident that early detection of the disease is a weak point of the Czech cancer management, particularly in the following diagnoses: cancer of oesophagus, liver, gallbladder and pancreas. Relatively low proportion of early detected cases can also be observed in highly prevalent cancers like colorectal cancer (stage I + II: 43.2%) and lung cancer (stage I + II: 14.6 %). Furthermore, in all mentioned diagnoses there is no signal of improving situation over a wide time span 1998– 2007 (Fig. 2). On the other hand, our survey revealed also prevalent cancers with continuous increase of early diagnosed cases. It is the case of female breast cancer, male testicular and prostate cancer and bladder cancer in both sexes; all these diagnoses have recently exceeded 70 % of incident cases in stage I or II (Tab. 8, Fig. 2).
Problems with accessibility of early diagnostics in cancer management are indicated also in regional survey presented in Tab. 9. Significant regional heterogeneity in early detection rate was found in nearly all listed diagnoses, including most prevalent colorectal cancer (inter regional range in proportion of early diagnosed cases: 37.4%– 53.0%), prostate cancer (41.4%– 74.3%) or bladder cancer (62.1%– 89.6%). It should be emphasized here, that even generally calculated cancer burden significantly differs among regions of the Czech Republic. Crude incidence estimated in 2007 regionally ranges from 444.5 to 604.9 and crude mortality ranges from 236.7 to 301.4 (Tab. 9). Such heterogeneity cannot be explained only by different population structure of the regions. In selected types of cancer the regional distribution of age standardized incidence rather indicates potential influence of some external, environmental factors (Fig. 3).
Discussion
The cancer burden of the Czech population ranks among the highest worldwide and has been growing continuously [4,6]. During 1990s and 2000s, the incidence of all major cancers was constantly increasing in the Czech population [19] and the growth dynamic was consistent with recently published international data [2– 5]. Also relative profile of most prevalent cancer types (breast cancer in women, prostate cancer in men, colorectal and lung cancer in both sexes) corresponds to the outcomes of most recent European epidemiology summaries [5]. In agreement with international reports, lung cancer is the most frequent cause of death from cancer. In the Czech male and female population it means 4,032 and 1,444 deaths.
The growing trend in cancer burden can be generally attributed to widely known risk factors, like apparent demographic ageing of the Czech population, life style factors or more specifically, to changes in reproductive behavior (female breast cancer) [29].
Further growth in cancer incidence can be expected also in future, due to the demographic structure and ageing of the Czech population. In 1995, the average age was 35.6 years for men and 38.9 years for women. Within twelve years, these values shifted to 38.8 years for men and 41.8 years for women (data from 2007). During the period 1995– 2007, the proportion of inhabitants aged over 50 years increased by 6.6%.
The increasing trend in incidence is remarkable also in preventable cancers, particularly in breast and colorectal carcinoma. Latest IARC database [2] even shows the Czech Republic to have the highest male colorectal cancer incidence worldwide. The growing incidence of colorectal cancer (growth index 1997– 2007: 6.8%) is accompanied with relatively weak early detection of the disease (only 43.2% of incident cases in stage I or II). Furthermore, the relative rate of early detected cases greatly varied among regions (37.4– 53.0%) which indicates some disparities in the cancer control. These facts are challengeable for the Czech programme of colorectal screening which has well documented history [30,31].
International trials promise decrease in CRC mortality by more than 30% due to organized screening based on annual guaiac faecal occult blood test (gFOBT) [32,33]. However, recent Czech data indicates only 16% coverage of target adult population by gFOBT screening which is insufficient to initiate population changes.
The recent situation in epidemiology of breast cancer in the Czech women population is better than in colorectal cancer. Although the incidence of breast carcinoma is significantly increasing (growth index 1997– 2007: 41.4%), it is accompanied with continuous increase of early diagnosed cases (recently 72% of incident cases diagnosed in stage I or II). These positive changes are due to increasing power of the Czech national screening for breast cancer which already reached more than 50% coverage of target women population (> 45 years). Similarly, as a consequence of widely used PSA test, we can observe growing incidence of early detected prostate cancer (Tab. 8, Fig. 2) although no organized screening for this type of cancer exists in the Czech Republic.
The cancer burden in the Czech Republic has also been increasing due to growing incidence rate of multiple primary malignancies, diagnosed in the same patient. Although the registration of multiple tumors was discussed in literature as rather complicated topic [34], it is not the case of the Czech cancer registry. The CNCR database makes it possible to identify a specific patient; therefore, recurring malignancy in the same person can be accurately identified, whether it is in the same location or another. The chronological order of recurring malignancies can also be measured. Tab. 7 sums up the overall data, showing that multiple malignancies are relatively common, although they differ markedly among diagnoses. If non melanoma skin cancers (C44) and malignant neoplasms of uncertain behavior (D37– D48) are not taken into account, the relative frequency of recurring malignancies ranges from 12 to 14%, the overwhelming majority (96%) of recurring malignancies belonging to other diagnostic group than the primary tumor. Recurring malignancy of the same diagnostic group is more common in breast cancer (C50), bladder cancer (C67) and partly in testicular cancer (C62). This field is very compelling because of it offers a new dimension for cancer burden causation. Additionally, it represents an opportunity for prevention and for better targeting of already diagnosed and treated cancer patients [35,36].
In addition to insufficient early detection of many cancers and related disparity in cancer diagnostics, the Czech cancer care is faced with high regional variability in epidemiologic measures. Although we cannot exclude the influence of under registration in some regions, its real impact is highly probably limited, particularly in recent period since 2000. This assumption is based on the regional profiles of mortality rates which fully correspond to that observed for the incidence profiles. Mortality estimates are double controlled in the Czech Republic using two independent sources of information on death events, i.e. cancer registry and Death Records Database [17,18]. Furthermore, the CNCR management closely respects the administrative division of the country into 14 regions and is collected with the same operation in each of them. Moreover, observed regional differences in cancer burden are different for various cancers and do not reveal any consistent pattern (Fig. 3).
Therefore, in view of regional differences (Tab. 9, Fig. 3), we cannot neglect influence of environmental factors, although their contribution to aetiology of human cancer is disputably discussed in literature [37,38]. Czech adults who come to risk age categories 50– 60 years or older were probably at least partially exposed with environmental pollutants including DDT, PCBs, PAHs and pesticides in 1960s– 1970s [6]. This hypothesis however cannot be exactly quantified due to the lack of environmental data from the period of communist government before 1989. Although we cannot address the role of environment in cancer causation, some birth cohort effects should be studied as indirect population indicator of some unspecified harmful effect in past. This information should be translated into well designed future studies focused on space variability of cancer epidemiology in the Czech Republic.
This work is based on 30 year experience of a nationwide, fully representative cancer registry. It supports the idea that cancer registries can be accepted as one of the main strategies for improving our understanding of cancer and its causation. Representative registries may reveal factors underlying trends in cancer incidence; moreover, they can detect significant changes over time in the main diagnostic measures (such as morphology and staging). This information is necessary to promote prevention which might ultimately lead to better control of the disease. The Czech National Cancer Registry contains complete and comprehensive records on the clinical stage at the time of diagnosis, including detailed records on individual components of TNM classification. The overall CNCR assessment has revealed only 5.8% of records which unfoundedly miss information on both TNM classification and clinical stage (Fig. 2). The completeness of CNCR data increases in time and the most recent period provides high quality data. The CNCR is equipped by web based analytic tool which allows the user to perform comprehensive analyses in user friendly environment [19]. We regard the CNCR database and associated software as one of the most influential product of the Czech National Cancer Control Program. These products also support wider international collaboration which is preferred also by other, similarly equipped cancer control programs [39].
Conclusion
With the epidemiological data accessible, the cancer burden in the Czech Republic can be assessed throughout the population and for individual regions. The proportion of clinical stages as well as the success rate of early detection can be analyzed, and the time trends can then be drawn from all assembled data. The most impressive aspect of our study is the accessibility of information over a 30 year period of continuous and standardized registration covering 100% of cancer diagnoses and the entire Czech population; also available in an on line working, interactive tool [19]. The main challenge for the future is to achieve the unaccomplished objective of lowering cancer mortality, particularly by sustained reduction of late diagnosed cases and of remarkable regional differences in diagnostic efficiency.
The
authors declare they have no potential conflicts of interest
concerning drugs, pruducts, or services
used in the study.
Autoři
deklarují, že v souvislosti s předmětem studie nemají
žádné komerční zájmy.
The
Editorial Board declares that the manuscript met the ICMJE “uniform
requirements” for biomedical papers.
Redakční
rada potvrzuje, že rukopis práce splnil ICMJE kritéria pro
publikace zasílané do biomedicínských časopisů.
Assoc.
Prof. MUDr. Ladislav Dušek, Ph.D.
Institute
of Biostatistics and Analyses
Faculty
of Medicine and Faculty of
Science
Masaryk
University in Brno
Kamenice
126/3
625
00 Brno
Czech
Republic
e-mail:
dusek@iba.muni.cz
Sources
1. Ferlay J, Bray F, Pisani P et al. GLOBOCAN 2002: Cancer Incidence, Mortality and Prevalence Worldwide. IARC CancerBase No. 5. Version 2.0. Lyon: IARC 2004. [cited 2010 Sep 22]. Available from: http:/ / globocan.iarc.fr.
2. Ferlay J, Shin HR, Bray F et al. GLOBOCAN 2008: Cancer Incidence and Mortality Worldwide. IARC CancerBase No. 10. Lyon: IARC 2010. [cited 2010 Sep 22]. Available from: http:/ / globocan.iarc.fr.
3. Boyle P, Ferlay J. Cancer incidence and mortality in Europe, 2004. Ann Oncol 2005; 16(3): 481– 488.
4. Curado MP, Edwards B, Shin HR et al. Cancer Incidence in Five Continents. Vol. IX. IARC Scientific Publications No. 160. Lyon: IARC 2007. [cited 2010 Sep 22]. Available from: http:/ / ci5.iarc.fr.
5. Ferlay J, Autier P, Boniol M et al. Estimates of the cancer incidence and mortality in Europe in 2006. Ann Oncol 2007; 18(3): 581– 592.
6. Dušek L. Czech Cancer Care in Numbers, 2008– 2009. Praha: GRADA Publishing 2009.
7. Franco EL, Correa P, Santella RM et al. Role and limitations of epidemiology in establishing a causal association. Semin Cancer Biol 2004; 14(6): 413– 426.
8. Berrino F, De Angelis R, Sant M et al. Survival for eight major cancers and all cancers combined for European adults diagnosed in 1995– 1999: results of the EUROCARE‑ 4 study. Lancet Oncol 2007; 8(9): 773– 783.
9. Verdecchia A, Francisci S, Brenner H et al. Recent cancer survival in Europe: a 2000– 2002 period analysis of EUROCARE‑ 4 data. Lancet Oncol 2007; 8(9): 784– 796.
10. Brenner H, Gondos A, Arndt V. Recent major progress in long‑term cancer patient survival disclosed by modelled period analysis. J Clin Oncol 2007; 25(22): 3274– 3280.
11. Coleman MP, Quaresma, M, Berrino F et al. Cancer survival in five continents: a worldwide population‑based study (CONCORD). Lancet Oncol 2008; 9(8): 730– 756.
12. Ponz de Leon M, Rossi G, di Gregorio C et al. Epidemiology of colorectal cancer: the 21‑year experience of a specialised registry. Intern Emerg Med 2007; 2(4): 269– 279.
13. Council recommendation of 2 December 2003 on cancer screening (2003/ 878/ EC). Official J Eur Union 2003; L 327/ 34: 85– 89.
14. IARC Working Group on the Evaluation of Cancer‑ Preventive Strategies. Cervix Cancer Screening. Lyon: IARC 2005.
15. Bray F, Sankila R, Ferlay J et al. Estimates of cancer incidence and mortality in Europe in 1995. Eur J Cancer 2002; 38(1): 99– 166.
16. Czech Statistical Office. Demographic data of the Czech Republic and Death Records Database of the Czech Republic [cited 2010 Aug 18]. Available from: http:/ / www.czso.cz/ eng/ redakce.nsf/ i/ population.
17. Czech Statistical Office. Demographic Yearbook of the Czech Republic 2007 [cited 2010 Aug 18]. Available from: http:/ / www.czso.cz.
18. Institute of Health Information and Statistics of the Czech Republic (IHIS). National Health Information System (NHIS), Czech National Cancer Registry [cited 2007 Dec 20]. Available from: http:/ / www.uzis.cz/ info.php?article=368&mnu_id=7300.
19. Dušek L, Mužík J, Kubásek M et al. Epidemiology of malignant tumours in the Czech Republic [online]. Masaryk University 2005 [cited 2008 Dec 15]. Available from: http:/ / www.svod.cz.
20. Institute of Health Information and Statistics of the Czech Republic (IHIS). Binding instructions of the National Health Information System (NHIS): Czech National Cancer Registry – instruction for the contents of data structure, version 051– 20060101/ 2. Prague, IHIS 2006 [cited 2007 Jun 18]. Available from: http:/ / www.uzis.cz, section IHIS, part Binding instructions.
21. World Health Organization. International statistical classification of diseases and related health problems, 10th revision (ICD‑ 10). Geneve: World Health Organization 1992.
22. Sobin LH, Gospodarowicz MK, Wittekind CH. TNM Classification of Malignant Tumors, 7th ed. Oxford: Wiley‑ Blackwell 2009.
23. World Health Organization. WHO Statistical Information System. Geneva, Switzerland: WHO Databank [cited 2010 Sep 4]. Available from: http:/ / www.who.int/ whosis.
24. Comparability and Quality Improvement of European Causes of Death Statistics, EDC DGV/ F3 SOC 98 20108- INSERM SC8/ Ce’ piDc‑ Final Report. Jully 2001.
25. Percy C, Muir C. The international comparability of cancer mortality data. Results of an international death certificate study. Am J Epidemiol 1989; 129(5): 934– 946.
26. International Agency for Research on Cancer. Cancer Incidence in Five Continents. IARC Scientific Publication no. 42. Lyon: IARC 1982.
27. Adami HO, Hunter D, Trichopoulos D. Textbook of cancer epidemiology. New York: Oxford University Press 2002.
28. Waterhouse J, Muir C, Correa P et al. Cancer Incidence in Five Continents. Vol. III. IARC Scientific Publications No. 15. Lyon: IARC 1976.
29. Karim‑ Kos HE, de Vries E, Soerjomataram I et al. Recent trends of cancer in Europe: a combined approach of incidence, survival and mortality for 17 cancer sites since the 1990s. Eur J Cancer 2008; 44(10): 1345– 1389.
30. Frič P. The use of haemoccult test in the early diagnosis of colerectal cancer – experience from six pilot studies in Czechoslovakia. In: Hardcastle JV (ed). Haemoccult screening for the early detection of colorectal cancer. Stuttgart: Schattauer 1986: 73– 74.
31. Zavoral M, Suchánek S, Závada F et al. Colorectal cancer screening in Europe. World J Gastroenterol 2009; 15(47): 5907– 5915.
32. Mandel JS, Bond JH, Church TR et al. Reducing mortality from colorectal cancer by screening for fecal occult blood. Minnesota Colon Cancer Control Study. N Engl J Med 1993; 328(19): 1365– 1371.
33. Hardcastle JD, Chamberlain JO, Robinson MH et al. Randomised controlled trial of faecal‑ occult‑blood screening for colorectal cancer. Lancet 1996; 348(9040): 1472– 1477.
34. Flannery JT, Boice JD Jr, Devesa SS et al. Cancer registration in Connecticut and the study of multiple primary cancers, 1935– 1982. Natl Cancer Inst Monogr 1985; 68: 13– 24.
35. Anderson WF, Guyton KZ, Hiatt RA et al. Colorectal cancer screening for persons at average risk. J Natl Cancer Inst 2002; 94(15): 1126– 1133.
36. Winawer S, Fletcher R, Rex D et al. Colorectal cancer screening and surveillance: clinical guidelines and rationale‑ Update based on new evidence. Gastroenterology 2003; 124(2): 544– 560.
37. Boffetta P, McLaughlin JK, la Vecchia C et al. ‘Environment’ in cancer causation and etiological fraction: limitations and ambiguities. Carcinogenesis 2007; 28(5): 913– 915.
38. Wild CP. Environmental exposure measurement in cancer epidemiology. Mutagenesis 2009; 24(2): 117– 125.
39. Engholm G, Ferlay J, Christensen N et al. NORDCAN: Cancer Incidence, Mortality, Prevalence and Prediction in the Nordic Countries, Version 3.5. Association of the Nordic Cancer Registries. Danish Cancer Society 2009 [cited 2010 Sep 24]. Available from: http:/ / www.ancr.nu.
Labels
Paediatric clinical oncology Surgery Clinical oncologyArticle was published in
Clinical Oncology
2010 Issue 5
Most read in this issue
- Diagnostic Pitfalls of HIV‑ Associated Kaposi Sarcoma
- Hand‑ Foot Syndrome after Administration of Tyrosinkinase Inhibitors
- Mucoepidermoid Carcinoma of a Nasal Cavity – a Rare Tumour
- Detection of DNA Hypermethylation as a Potential Biomarker for Prostate Cancer