Skip to main content

Advertisement

SpringerLink
Log in

Analysing Multiple Causes of Death: Which Methods For Which Data? An Application to the Cancer-Related Mortality in France and Italy

Analyse des causes multiples de décès: quelles méthodes pour quelles données? L’exemple de la mortalité par cancer en France et en Italie

  • Published:
European Journal of Population / Revue européenne de Démographie Aims and scope Submit manuscript

Abstract

Multiple cause of death (MCOD) data have been used to recalculate mortality levels attributed to a given condition, and to determine the most frequent associations of causes involving this condition. In this article, we begin with a description of how the MCOD data is collected, and we discuss data quality. After presenting the main indicators specifically developed to analyse these data, we provide a concrete illustration of the method based on a comparison of cancer-related mortality in Italy and France. The results for the two countries are strikingly similar. The change in mortality levels is modest for most anatomic sites: cancer is often selected as the underlying cause of death (UCD). The most notable exception (cancer of the prostate) potentially exemplifies future trends, with more effective treatments and increased incidence of this disease among elderly people due to population ageing, cancers may more often play a contributing role in mortality. For all anatomic sites, the reporting of a neoplasm as both underlying and contributing cause of death is a feature of cancer-related mortality. We then categorize all other associations into five patterns (‘degeneration of the contributing cause’, ‘risk factor for the UCD’, ‘common cause’, ‘consequence/complication of the UCD’ and ‘symptom of the UCD’) that reflect current medical knowledge.

Résumé

La prise en compte pour l’étude de la mortalité de l’ensemble des causes mentionnées sur les certificats de décès (causes multiples) répond généralement à deux objectifs : réévaluer la contribution des différentes causes de décès dans la mortalité générale et repérer les combinaisons entre causes principales et causes associées particulièrement fréquentes. Dans cet article, après avoir rappelé les modalités de la collecte des causes multiples de décès, nous évaluons la qualité de ces données. Nous présentons ensuite les différents indicateurs qui ont été proposés pour en faire l’analyse. Enfin, nous illustrons cette approche dans le cas des cancers en comparant deux pays : la France et l’Italie. Les résultats obtenus dans les deux pays sont très proches. Pour la plupart des sites, les niveaux de mortalité sont peu modifiés par la prise en compte des causes associées : les cancers sont souvent sélectionnés en tant que cause principale du décès. Le cancer de la prostate constitue une exception notable qui, à terme, pourrait concerner un nombre croissant de cancers : à mesure que l’efficacité des traitements s’améliore et que l’allongement de l’espérance de vie conduit à poser le diagnostic d’un cancer chez des personnes déjà âgées, les cancers pourraient être plus fréquemment mentionnés en cause associée du décès. L’examen des associations entre causes montre que la mention sur un même certificat d’un cancer en cause principale et en cause associée est très courante. Nous proposons pour terminer une typologie des différentes associations mises au jour en cinq catégories («aggravation de la cause associée» , «facteur de risque» , «cause commune» , «conséquence/complication» et «symptôme»).

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Notes

  1. Multiple causes include both underlying and contributing causes.

  2. Detailed tables are available since 2003 on the Istat website.

  3. Note that both the selection of the underlying cause and the reporting of the contributing causes of death are potentially affected by inadequate/insufficient training.

  4. The two certificates are displayed in the Appendix.

  5. Part I is for the diseases or conditions that directly led to death. Part II is for any other significant condition that unfavourably influenced the course of the morbid process but is not related to the condition directly causing death. In many cases, it is difficult to decide whether a condition should be mentioned in part I or part II. If not explicitly specified, all indicators presented in this article are computed taking into account entries in parts I and II.

  6. When excluding these causes from the computation, the difference between the two countries narrows (2.4 in France vs. 3.0 in Italy).

  7. Note that we considered as redundant information and removed from the databases any recorded cause that, for a given death, is exactly identical (at the four-digit level of the ICD-10 classification) to another already registered cause.

  8. As the indicator is based on the ratio of averages, age distributions of its components (ud c,x /ud x and d c,x /d x ) may affect the value of the CDAI. Nevertheless, we find that for cancers as UCD, the correlation between CDAIs and the age structure of the components is close to zero.

  9. More precisely, the two series of indicators computed for a given contributing cause and various underlying causes are proportional (the denominator is the same for each UCD), so the conclusions are unchanged. The correlation between the two series of indicators computed for a given UCD and various contributing causes is generally very close to one.

  10. So, we do not exclude associations between an underlying cause and a contributing cause belonging to the same group.

  11. The standard population is the WHO 2003 European population by sex and five-year age groups.

  12. See the list of the groups in the Table 5 in appendix.

  13. Only malignant neoplasms with well-defined anatomic sites are presented.

  14. The standard deviation was calculated taking into account all the values of the CDAI in the two countries.

  15. See abbreviations in the Table 5 in appendix.

  16. ‘Mental and behavioural disorders due to use of tobacco’ (ICD-10 F179 code) is classified in the ‘Other Mental and behavioural disorders’ group.

References

  • Aubenque, M. (1975). Un aperçu historique des statistiques sanitaires de la France. Paris: INSEE.

  • Australian Bureau of Statistics. (2003). Multiple cause of death analysis, 1997–2001. http://www.abs.gov.au/ausstats/abs@.nsf/mf/3319.0.55.001.

  • Chamblee, R. F., & Evans, M. C. (1982). New dimensions in cause of death statistics. American Journal of Public Health, 72(11), 1265–1270.

    Article  Google Scholar 

  • Coste, J., & Jougla, E. (1994). Mortality from rheumatoid arthritis in France: 1970–1990. International Journal of Epidemiology, 23(3), 545–552.

    Article  Google Scholar 

  • Crews, D. E. (1988). Multiple causes of death and the epidemiological transition in American Samoa. Biodemography and Social Biology, 35(3–4), 198–213.

    Article  Google Scholar 

  • Crews, D. E. (1990). Multiple causes of death, chronic diseases and aging. Collegium antropologicum, 14(2), 197–204.

    Google Scholar 

  • Daoud, J., Siala, W., Guermazi, F., Besbes, M., Frikha, M., Ghorbel, M., et al. (2005). Hypothyroidism following cervical irradiation in the management of carcinoma of the nasopharynx and of the breast, a prospective study on eighty-four cases. Cancer Radiotherapy, 9, 140–147.

    Article  Google Scholar 

  • David, H. A. (1974). Parametric Approaches to the Theory of Competing Risks. In F. Proschan & R. J. Serfling (Eds.), Reliability and biometry (pp. 275–290). Philadelphia: Society for Industrial and Applied Mathematics.

    Google Scholar 

  • Désesquelles, A., & Meslé, F. (2004). Intérêt de l’analyse des causes multiples dans l’étude de la mortalité aux grands âges, l’exemple français. Cahiers québécois de démographie, 33(1), 83–116.

    Article  Google Scholar 

  • Désesquelles, A., Salvatore, M. A., Frova, L., Pace, M., Pappagallo, M., Meslé, M., et al. (2010). Revisiting the mortality of France and Italy with the multiple-cause-of-death approach. Demographic Research, 23(28), 71–806.

    Google Scholar 

  • Dorn, H. F., & Moriyama, I. M. (1964). Uses and significance of multiple cause tabulations for mortality statistics. American Journal of Public Health Nations Health, 54, 400–406.

    Article  Google Scholar 

  • Eakin, E. G., Youlden, D. R., Baade, P. D., Lawler, S. P., Reeves, M. M., Heyworth, J. S., et al. (2006). Health status of long-term cancer survivors: Results from an Australian population-based sample. Cancer Epidemiology Biomarkers Prevention, 15, 1969–1976.

    Article  Google Scholar 

  • Fink, A. K., German, R. R., Heron, M., Stewart, S. L., Johnson, C. J., Finch, J. L., et al. (2011). Impact of using multiple causes of death codes to compute site-specific, death certificate-based cancer mortality statistics in the United States. Cancer Epidemiology, 35(2), 126–131.

    Article  Google Scholar 

  • Frenzen, P. (2003). Mortality due to gastroenteritis of unknown etiology in the United States. The Journal of Infectious Diseases, 18, 441–452.

    Article  Google Scholar 

  • Frova, L., Salvatore, M. A., Pappagallo, & Egidi, V. (2009). The multiple cause of death approach to analyse mortality patterns. Genus, 65(1), 1–21.

    Google Scholar 

  • Fuhrman, C., Jougla, E., Nicolau, J., Eilstein, D., & Delmas, M. C. (2006). Deaths from chronic obstructive pulmonary disease in France, 1979–2002: A multiple cause analysis. Thorax, 61, 930–934.

    Article  Google Scholar 

  • Fuhrman, C., Jougla, E., Uhry, Z., & Delmas, M. (2009). Deaths with asthma in France, 2000–2005: A multiple-cause analysis. Journal of Asthma, 46(4), 402–406.

    Article  Google Scholar 

  • Goldacre, M. J., Duncan, M. E., Cook-Mozaffari, P., & Griffith, M. (2003). Trends in mortality rates comparing underlying-cause and multiple-cause coding in an English population 1979–1998. Journal of Public Health Medicine, 25, 249–253.

    Article  Google Scholar 

  • Goldacre, M. J., Duncan, M. E., Cook-Mozaffari, P., & Griffith, M. (2004a). Trends in mortality for cancers, comparing multiple- and underlying-cause rates, in an English population 1979–1999. British Journal of Cancer, 90, 1019–1021.

    Article  Google Scholar 

  • Goldacre, M. J., Duncan, M., Cook-Mozaffari, P., & Griffith, M. (2004b). Mortality rates for common respiratory diseases in an English population 1979–1998: Artefact and substantive trends. Journal of Public Health (Oxford), 26, 8–12.

    Article  Google Scholar 

  • Goldacre, M. J., Duncan, M. E., Cook-Mozaffari, P., & Neil, H. A. W. (2004c). Trends in mortality rates for death-certificate-coded diabetes mellitus in an English population 1979–99. Diabetic Medicine, 21, 936–939.

    Article  Google Scholar 

  • Goldacre, M. J., Duncan, M., Griffith, M., & Cook-Mozaffari, P. (2004d). Alcohol as a certified cause of death in a ‘middle England’ population 1979–1999: Database study. Journal of Public Health (Oxford), 26, 343–346.

    Article  Google Scholar 

  • Goldacre, M. J., Duncan, M., Griffith, M., & Rothwell, P. M. (2008). Mortality rates for stroke in England from 1979 to 2004: Trends, diagnostic precision, and artifacts. Stroke, 39, 2197–2203.

    Article  Google Scholar 

  • Goldacre, M. J., Mant, D., Duncan, M., & Griffith, M. (2005). Mortality from heart failure in an English population, 1979–2003: Study of death certification. Journal of Epidemiology and Community Health, 59, 782–784.

    Article  Google Scholar 

  • Goodman, R. A., Manton, K. G., Nolan, T. F., Bregmen, D. J., & Hinman, A. R. (1982). Mortality data analysis using a multiple-cause approach. Journal of the American Medical Association, 247(6), 793–796.

    Article  Google Scholar 

  • Guralnick, L. (1966). Some problems in the use of multiple causes of death. Journal of Chronic Diseases, 19(9), 979–990.

    Article  Google Scholar 

  • Hedskog, L., Zhang, S., & Ankarcrona, M. (2011). Strategic role for mitochondria in Alzheimer’s disease and cancer. Antioxidants & Redox Signaling, 15(10), 2150–2563.

    Google Scholar 

  • Israel, R. A., Rosenberg, H. M., & Curtin, L. R. (1986). Analytical potential for multiple cause-of-death data. American Journal of Epidemiology, 124, 161–179.

    Google Scholar 

  • ISTAT. (1958). Indagine statistica sulle concause di morte—1951–1954. Supplemento all’annuario di statistiche sanitarie del 1955.

  • ISTAT (2004). Applying ACS to Causes of death Statistics in Italy. Some clues on implementation, bridge coding and further steps. In Frova L, Marchetti S, Pace M (Eds.), Applying acs to causes of death statistics in Italy. Rome: ISTAT.

  • Janssen, T. A. (1940). Importance of tabulating multiple causes of death. American Journal of Public Health Nations Health, 30(8), 871–879.

    Article  Google Scholar 

  • Jougla, E., Papoz, L., Balkau, B., Maguin, P., & Hatton, F. (1992). Death certificate coding practices related to diabetes in European countries—The ‘EURODIAB subarea C’ study. International Journal of Epidemiology, 21(2), 343–351.

    Article  Google Scholar 

  • Kaplan, M. H., Armstrong, D., & Rosen, P. (1974). Tuberculosis complicating neoplastic disease. A review of 201 cases. Cancer, 33, 850–858.

    Article  Google Scholar 

  • Kohn, R. R. (1982). Cause of death in very old people. Journal of the American Medical Association, 247(20), 2793–2797.

    Article  Google Scholar 

  • Lee, L., & Thompson, W. A. (1974). Results on failure time and patterns for the series system. In Frank. Proschan & R. J. Serfling (Eds.), Reliability and biometry (pp. 291–302). Philadelphia: Society for Industrial and Applied Mathematics.

    Google Scholar 

  • Mackenbach, J. P., Kunst, A. E., Lautenbach, H., Bijlsma, F., & Oei, Y. B. (1995). Competing causes of death: an analysis using multiple-cause-of-death data from The Netherlands. American Journal of Epidemiology, 141(5), 466–475.

    Google Scholar 

  • Mannino, D. M., Ford, E., Giovino, G. A., & Thun, M. (1998). Lung cancer deaths in the United States from 1979 to 1992: An analysis using multiple-cause mortality data. International Journal of Epidemiology, 27(2), 159–166.

    Article  Google Scholar 

  • Manton, K. G. (1986). Cause specific mortality patterns among the oldest old: Multiple cause of death trends 1968 to 1980. Journal of Gerontology, 41(2), 282–289.

    Google Scholar 

  • Manton, K. G., & Myers, G. C. (1987). Recent trends in multiple-caused mortality 1968 to 1992: Age and cohort components. Population Research and Policy Review, 6, 161–176.

    Article  Google Scholar 

  • Manton, K. G., & Poss, S. S. (1979). Effects of dependency among causes of death for cause elimination life table strategies. Demography, 16, 313–327.

    Article  Google Scholar 

  • Manton, K. G., & Stallard, E. (1982). Temporal trends in U. S. multiple cause of death mortality data 1968 to 1977. Demography, 19(4), 527–547.

    Article  Google Scholar 

  • Manton, K. G., Tolley, D. H., & Poss, S. S. (1976). Life table techniques for multiple-cause mortality. Demography, 13, 541–564.

    Article  Google Scholar 

  • Markush, R. E., & Seigel, D. G. (1968). Prevalence at death. I. A new method for deriving death rates for specific diseases. American Journal of Public Health Nations Health, 58(3), 544–557.

    Article  Google Scholar 

  • Matzkin, H., & Soloway, M. S. (1993). Cigarette smoking: A review of possible associations with benign prostatic hyperplasia and prostate cancer. Prostate, 22, 277–290.

    Article  Google Scholar 

  • McCoy, L., Redelings, M., Sorvillo, F., & Simon, P. (2005). A multiple cause-of-death analysis of asthma mortality in the United States, 1990–2001. Journal of Asthma, 42(9), 757–763.

    Article  Google Scholar 

  • Mele, A., Pulsoni, A., Bianco, E., Musto, P., Szklo, A., Sanpaolo, M. G., et al. (2003). Hepatitis C virus and B-cell non-Hodgkin lymphomas: An Italian multicenter case–control study. Blood, 102, 996–999.

    Article  Google Scholar 

  • Moriyama, I. M. (1956). Development of the present concept of cause of death. American Journal of Public Health, 46, 436–451.

    Article  Google Scholar 

  • Nam, C. B. (1986). Mortality differentials from a multiple cause-of-death perspective. Committee on comparative mortality changes, In Seminar on comparative studies of mortality and morbidity: old and new approaches to measurement and analysis, July 7–12, IUSSP, Ciena, Italy.

  • Nam, C. B., Hummer, R. A., & Rogers, R. G. (1994). Underlying and multiple causes of death related to smoking. Population Research and Policy Review, 13(3), 305–325.

    Article  Google Scholar 

  • Nizard, A., & Munoz-Pérez, F. (1993). Alcool, tabac et mortalité en France depuis 1950—Essai d’évaluation des décès dus à la consommation d’alcool et de tabac en 1986. Population, 3, 571–607.

    Article  Google Scholar 

  • Omran, A. R. (1971). The epidemiologic transition. A theory of the epidemiology of population change. The Milbank Memorial Fund Quarterly, 49, 509–538.

    Article  Google Scholar 

  • Pavillon, G., Boileau, J., Tenaud, G., Lefèvre, H., & Jougla, E. (2005). Conséquences des changements de codage des causes médicales de décès sur les données nationales de mortalité en France, à partir de l’année 2000. Bulletin Epidémiologique Hebdomadaire, 4, 13–16.

    Google Scholar 

  • Pavlides, S., Tsirigos, A., Vera, I., Flomenberg, N., Frank, P. G., Casimiro, M. C., et al. (2010). Transcriptional evidence for the “Reverse Warburg Effect” in human breast cancer tumor stroma and metastasis: Similarities with oxidative stress, inflammation, Alzheimer’s disease, and “neuron-glia metabolic coupling”. Aging, 2, 185–199.

    Google Scholar 

  • Redelings, M. D., Wise, M., & Sorvillo, F. (2007). Using multiple cause-of-death data to investigate associations and causality between conditions listed on the death certificate. American Journal of Epidemiology, 166(1), 104–108.

    Article  Google Scholar 

  • Romon, I., Jougla, E., Balkau, B., & Fagot-Campagna, A. (2008). The burden of diabetes-related mortality in France in 2002: An analysis using both underlying and multiple causes of death. European Journal of Epidemiology, 23(5), 327–334.

    Article  Google Scholar 

  • Sasco, A. J., Secretan, M. B., & Straif, K. (2004). Tobacco smoking and cancer: A brief review of recent epidemiological evidence. Lung Cancer, 45(Suppl 2), S3–S9.

    Article  Google Scholar 

  • Smith, K. R., & Kliewer, E. V. (1995). Estimating standardized mortality odds ratios with national mortality folloback data. Epidemiology, 6(1), 55–60.

    Article  Google Scholar 

  • Smyth, P. P. (1997). The thyroid and breast cancer: A significant association? Annals of Medicine, 29, 189–191.

    Article  Google Scholar 

  • Speizer, F. E., Trey, C., & Parker, P. (1977). The uses of multiple causes of death data to clarify changing patterns of cirrhosis mortality in Massachusetts. American Journal of Public Health, 67(4), 333–336.

    Article  Google Scholar 

  • Stallard, E. (2002). Underlying and multiple cause mortality at advanced ages: United States 1980–1998. North American Actuarial Journal, 6(3), 64–87.

    Google Scholar 

  • Staropoli, J. F. (2008). Tumorigenesis and neurodegeneration: Two sides of the same coin? BioEssays, 30, 719–727.

    Article  Google Scholar 

  • Steenland, K., Nowlin, S., Ryan, B., & Adams, S. (1992). Use of multiple-cause mortality data in epidemiologic analyses: US rate and proportion files developed by the National Institute for Occupational Safety and Health and the National Cancer Institute. American Journal of Epidemiology, 136(7), 855–862.

    Article  Google Scholar 

  • Tardon, A. G., Zaplana, J., Hernandez, R., & Cueto, A. (1995). Usefulness of the codification of multiple causes of death in mortality statistics. International Journal of Epidemiology, 24, 1132–1137.

    Article  Google Scholar 

  • Tsung-Hsueh, L., Anderson, R. N., & Kawachi, I. (2010). Trends in frequency of reporting improper diabetes-related cause-of-death statements on death certificates, 1985–2005: An algorithm to identify incorrect causal sequences. American Journal of Epidemiology, 171, 1069–1078.

    Article  Google Scholar 

  • Van der Gulden, J. W., Verbeek, A. L., & Kolk, J. J. (1994). Smoking and drinking habits in relation to prostate cancer. British Journal of Urology, 73, 382–389.

    Article  Google Scholar 

  • Vento, S., & Lanzafame, M. (2011). Tuberculosis and cancer: A complex and dangerous liaison. Lancet Oncology, 12, 520–522.

    Article  Google Scholar 

  • Wall, M. M., Huang, J., Oswald, J., & McCullen, D. (2005). Factors associated with reporting multiple causes of death. BMC Medical Research Methodology, 5, 4.

    Article  Google Scholar 

  • White, M. C., Selvin, S., & Merrill, D. W. (1989). A study of multiple causes of death in California: 1955 and 1980. Journal of Clinical Epidemiology, 42(4), 355–365.

    Article  Google Scholar 

  • Wilkins, K., Wysocki, M., Morin, C., & Wood, P. (1997). Multiple causes of death. Statistics Canada Health Reports, 9(2), 19–29.

    Google Scholar 

  • Wing, S., & Manton, K. G. (1981). A multiple cause of death analysis of hypertension-related mortality in North Carolina, 1968–1977. American Journal of Public Health, 71(8), 823–830.

    Article  Google Scholar 

  • Wise, M. E., & Sorvillo, F. (2005). Hepatitis A-related mortality in California, 1989–2000: Analysis of multiple cause-coded death data. American Journal of Public Health, 95(5), 900–905.

    Article  Google Scholar 

  • Wong, O. (1977). A competing-risk model based on the life table procedure in epidemiological studies. International Journal of Epidemiology, 6, 153–159.

    Article  Google Scholar 

  • Wrigley, J. M., & Nam, C. B. (1987). Underlying versus multiple causes of death: Effects on interpreting cancer mortality differential by age, sex and race. Population Research and Policy Review, 16(2), 149–160.

    Article  Google Scholar 

  • Ziadé, N., Jougla, E., & Coste, J. (2010). Population-level impact of osteoporotic fractures on mortality and trends over time: a nationwide analysis of vital statistics for France, 1968–2004. American Journal of Epidemiology, 172, 942–951.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institut National d’Etudes Démographiques (INED), 133 Bd Davout, 75980, Paris cedex 20, France

    Aline F. Désesquelles & France Meslé

  2. Istituto Nazionale di Statistica (Istat), Viale Liegi, 13, 00198, Rome, Italy

    Michele Antonio Salvatore, Marilena Pappagallo, Luisa Frova & Monica Pace

  3. Dipartimento di Scienze Statistiche, Sapienza Università di Roma (SUR), Viale Regina Elena, 295, 00161, Rome, Italy

    Viviana Egidi

Authors
  1. Aline F. Désesquelles
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Michele Antonio Salvatore
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Marilena Pappagallo
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Luisa Frova
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Monica Pace
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. France Meslé
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Viviana Egidi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Aline F. Désesquelles.

Appendix

Appendix

See Figs. 6 and 7; Tables 3, 4 and 5.

Fig. 6
figure 6

French death certificate

Full size image
Fig. 7
figure 7

Italian death certificate

Full size image
Table 3 Standardized prevalence at death (per 1,000)—Neoplasms as UCD—France, 2003
Full size table
Table 4 Standardized prevalence at death (per 1,000)—Neoplasms as UCD—Italy, 2003
Full size table
Table 5 Groups of causes of death and abbreviations
Full size table

Rights and permissions

Reprints and permissions

About this article

Cite this article

Désesquelles, A.F., Salvatore, M.A., Pappagallo, M. et al. Analysing Multiple Causes of Death: Which Methods For Which Data? An Application to the Cancer-Related Mortality in France and Italy. Eur J Population 28, 467–498 (2012). https://doi.org/10.1007/s10680-012-9272-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10680-012-9272-3

Keywords

Mots-clés

Search

Navigation