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Analysing Multiple Causes of Death: Which Methods For Which Data? An

Application to the Cancer-Related Mortality in France and Italy
Article in European Journal of Population · November 2012

DOI: 10.1007/s10680-012-9272-3
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Eur J Population
DOI 10.1007/s10680-012-9272-3
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
Aline F. Désesquelles • Michele Antonio Salvatore •

Marilena Pappagallo • Luisa Frova • Monica Pace •
France Meslé • Viviana Egidi
Received: 2 January 2012 / Accepted: 31 July 2012

Ó Springer Science+Business Media B.V. 2012
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.
A. F. Désesquelles (&) F. Meslé

Institut National d’Etudes Démographiques (INED), 133 Bd Davout, 75980 Paris cedex 20, France
e-mail: alined@ined.fr
M. A. Salvatore M. Pappagallo L. Frova M. Pace

Istituto Nazionale di Statistica (Istat), Viale Liegi, 13, 00198 Rome, Italy
V. Egidi
Dipartimento di Scienze Statistiche, Sapienza Università di Roma (SUR),
Viale Regina Elena, 295, 00161 Rome, Italy
123
A. F. Désesquelles et al.
Keywords Multiple causes of death Mortality Cancer France Italy
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 as-
sociée 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»).
Mots-clés Causes multiples de décès Mortalité Cancer France Italie
In an article published in the 60s, Dorn and Moriyama (1964) lent support to the
widely accepted idea that ‘a single cause, no matter how selected, no longer
adequately describes the morbid conditions responsible for a large proportion of
deaths’. About 25 years earlier, Theodore Janssen (1940) had been one of the first to
highlight the importance of tabulating and analysing multiple1 causes of death. His
recommendation was followed by Lillian Guralnick (1966) who proposed a number
of methods for tabulating the exhaustive information reported on death certificates.
Almost 50 years after these pioneering studies, mortality is still analysed primarily
in terms of the underlying cause of death (UCD). Yet, multiple cause of death
(MCOD) data are increasingly produced and disseminated by statistical offices, and
they have been used in several ways that can be broadly classified into three lines of
research.
First, demographers and statisticians have used these data to build multiple-cause
life tables (David 1974; Lee and Thompson 1974; Manton et al. 1976; Manton and
Poss 1979; Wong 1977). Here, the aim is to compute the probability of death when
1
Multiple causes include both underlying and contributing causes.
123
Analysing Multiple Causes of Death
one or more causes of death are eliminated. Standard methods that rely on the UCD
and on competing risks theory require assumptions about independence/dependence
among causes. These assumptions may or may not be appropriate, depending on the
morbid processes under study. MCOD statistics offer interesting options for
addressing this problem: morbid states may indeed be redefined in order to represent
patterns of diseases which are more nearly independent (Manton and Poss 1979).
The second line of research aims at recalculating mortality levels attributed to a
given condition. To put it differently, the aim is to calculate mortality indicators that
take into account all the conditions reported on death certificates. This approach has
been developed mainly to reassess the contribution to mortality of certain conditions
that are frequently reported as a contributing cause of death. Among others, diabetes
(Jougla et al. 1992; Goldacre et al. 2004c; Romon et al. 2008; Tsung-Hsueh et al.
2010), asthma (McCoy et al. 2005; Fuhrman et al. 2009), hypertension (Wing and
Manton 1981), alcohol and tobacco use (Speizer et al. 1977; Nizard and Munoz-
Pérez 1993; Nam et al. 1994; Goldacre et al. 2004d), hepatitis (Wise and Sorvillo
2005), and musculoskeletal disorders (Coste and Jougla 1994; Ziadé et al. 2010)
have received particular attention. But cancers (Wrigley and Nam 1987; Mannino
et al. 1998; Goldacre et al. 2004a), heart failure, and stroke (Goldacre et al. 2005;
Goldacre et al. 2008) as well as other respiratory diseases (Goldacre et al. 2004b;
Fuhrman et al. 2006) have been studied too. Some authors have used the MCOD
approach on a larger or even unrestricted list of conditions (Manton and Stallard
1982; Crews 1988; White et al. 1989; Steenland et al. 1992; Tardon et al. 1995;
Mackenbach et al. 1995; Goldacre et al. 2003; Frova et al. 2009; Désesquelles et al.
2010). Most analyses we found in our review are country-specific and some have
focused on deaths at old or very old ages (Kohn 1982; Manton 1986; Manton and
Myers 1987; Stallard 2002; Désesquelles and Meslé 2004). With the rise in life
expectancy, a growing share of the population reaches ages where comorbidity is
very frequent. As a consequence, the number of reported conditions on the death
certificates is expected to increase.
Finally, the third line of research focuses on cause combinations. ‘Statistics
showing combinations of causes come nearer the truth than do those based on the
single cause principle because the majority of deaths actually result from a
combination of causes’ (Janssen 1940). When Janssen wrote these words, the
population ageing process was not as advanced as it is now, but degenerative and
man-made diseases that characterize the third stage of the epidemiological transition
(Omran 1971) had started to represent a growing share of total morbidity. Following
Nam (1986), Crews (1990) suggests that the underlying-cause approach oversim-
plifies the changes occurring in the epidemiological profile, and he believes that the
MCOD approach is more appropriate to examine the complexity of degenerative
disease processes.
In this article, we begin with a description of how MCOD data are collected, and
we investigate data quality. Then, we present the various indicators that have been
developed to revaluate mortality levels and examine combination of causes. Finally,
we provide a concrete illustration of the analytical potential of this approach based
on the comparison of cancer-related mortality in Italy and France. As we shall see,
the French and the Italian cause of death data are not fully comparable but the data
123
collection methods and the health and mortality profiles of the two countries are
similar enough to ensure that the comparison is not meaningless. This being said, we
believe in the heuristic virtues of cross-country comparison. As we cannot be certain
about data quality, both similarities and dissimilarities in the results obtained in the
two countries must be interpreted with caution, but they are a potentially fruitful
source of information. In particular, they can help to identify failures of the coding
and/or certification practices as well as other drawbacks of the data gathering tools.
Data for the two countries are for the year 2003. Among all causes of death,
cancer ranks first in France and second in Italy. In a previous study (Désesquelles
et al. 2010), we showed that, compared to less life-threatening diseases, cancers
are more often selected as the underlying cause of death. However, this result may
vary across anatomic sites because survival chances are not the same for all
cancers. Neoplasms with the best survival profiles can be considered as chronic
conditions, and long-term cancer survivors may develop other health problems
that they may eventually die from. All in all, given the increased incidence of
cancers among elderly people due to population ageing, and the development of
more effective treatments, cases of comorbidity involving cancers are expected to
become more frequent (Eakin et al. 2006). So, from a public health perspective,
the study of the interactions between cancers and other diseases will be
increasingly relevant.
1 MCOD Data: Collection and Quality
1.1 A Quite Recent Data source
Though the idea that death often results from the conjunction of several diseases,
conditions or risk factors, was already present in the mind of statisticians who
implemented the first International Classification of Diseases at the end of the 19th
century, their main efforts at that time focused on the production of tables
attributing one cause to one death. Strategies for deciding about the cause to be
chosen have changed over time. First, people in charge of data collection drew up
rules to help choose the underlying cause from among all the information reported
on the death certificate. At that time, they did not trust certifying physicians, who
often considered the immediate cause of death as the underlying one. To help coders
make a decision, the US Bureau of Census issued the first ‘Manual of Joint Causes
of death’ that provided practical cases for which a choice had to be made, and rules
to be followed (Moriyama 1956). This manual was revised several times during the
interwar years. It was only after the Second World War that greater trust was placed
in the certifying physicians. This trend was reinforced by the introduction of new
death certificates on which certifiers had to determine and describe the most likely
sequence of events that led to death, starting from the immediate cause and going
back into the past to identify the first medical problem that initiated the whole
process.
The elaboration of very precise rules to select the UCD improved cross-country
comparability. For a long time, the concern to ensure UCD comparability diverted
123
people in charge of cause of death statistics from taking into account all the
information reported on the death certificates. The ultimate aim was still to produce
consistent tables for the UCD. It is fair to say that before the computer age, it was
not a simple task to deal with tables linking several causes for one death. Until now,
not many countries have published data on multiple causes of death. The US, where
these tables have been produced in electronic format since 1968, remains an
exception. In France and Italy, the interest in multiple causes of death is much more
recent.
In France, the recording of multiple causes began in the early 50s with the
implementation of a new certificate on which the physician could report several
conditions that had contributed to the death (Aubenque 1975). This certificate was
based on the international model recommended by the World Heath Organization
(WHO). Physicians progressively became familiar with this new tool, and the
proportion of deaths with more than one coded condition grew from 25 % in 1955 to
45 % in 1967. After this period of regular increase, the proportion jumped suddenly
to 60 % in 1968. That year, the recording of causes of death was taken over by the
French National Institute for Health and Medical Research (Inserm), and the quality
of statistics immediately improved. Another jump occurred in 2000 with the
adoption of the ICD-10 and the implementation of an automatic coding system. In
the 2000s, the proportion of deaths with more than one coded condition reached
85 %. However, Inserm has only provided access to the complete information
reported on the death certificates since 2000.
In Italy, the collection, processing and dissemination of causes of death statistics
has been under the authority of the National Institute of Statistics (Istat) since 1926.
The Italian death certificate, also based on the WHO model, was introduced in 1951
with the adoption of the ICD-6. A first evaluation of co-morbidities over the period
1951–1954 was performed in 1958 (Istat 1958), but collection of MCOD data did
not begin until 1995, with the introduction of the automated coding system (Istat
2004). In 2008, 98 % of death certificates had more than one coded condition.
Codes for all reported conditions have been available in the databases since 1995,
but the first official release of MCOD data is for 2003, when the ICD-10 was
adopted.2 In Italy, data on contributing causes are not available for deaths attributed
to an external cause and for infant deaths. For the remainder of this study, all these
deaths have thus been excluded from the analysis.
1.2 Quality: ‘Could do Better!’
The production of cause of death statistics relies on two steps that are both crucial
for the quality of the MCOD data. First, the certifying physician reports the chain of
causes leading to death on the certificate. Second, this information is coded. A
growing number of countries now use an automatic coding system. To our mind,
this innovation represents a major advance towards improved quality of MCOD
data. Human intervention is limited to problematic cases that cannot be processed
automatically and, at least in theory, the WHO coding rules can be applied
2
Detailed tables are available since 2003 on the Istat website.
123
systematically and uniformly, irrespective of the coding agent or the country.

However, not every country uses the same coding system. As an example, France
uses STYX, a coding system that is derived from the American Automated
Classification of Medical Entities (ACME) (Pavillon et al. 2005). Italy uses
CODSAN II, an adaptation of both ACME and the American Mortality Medical
Indexing, Classification, and Retrieval (MICAR) system (Istat 2004). While STYX
directly produces ICD-10 codes, CODSAN II relies on the USA-Entity Reference
Number (ERN) system that translates each medical term into a six-digit number. A
transition table is then used to convert the ERN into an ICD-10 code. So the French
and the Italian systems may produce different outputs if detailed levels of the
classification are used.
Regarding certification problems, both over- and underreporting may occur. The
certifying physician may report conditions that the decedent was not suffering from,
or conditions that were present at death but played no role in the lethal process.
Incomplete reporting, for its part, is likely to be more frequent for conditions which
are difficult to diagnose (e.g. Alzheimer’s disease) as well as for causes of death that
are stigmatized (e.g. suicide). When interpreting combinations of causes, what
matters is whether such over/underreporting affects all the underlying causes in the
same way, a point which, in the words of Mackenbach et al. (1995), ‘can only be a
matter of speculation’. We suspect that overreporting is more frequent when the
UCD is not a very lethal disease. Conversely, the certifying physicians may not
report the full morbid process when the UCD is sufficient to explain the death.
Inadequate and/or insufficient training of the certifying physicians certainly plays a
major role in the quality of reporting,3 but even with proper training the certifying
physicians may not be fully informed about the morbid process that led to death. The
availability of detailed information also depends on trends in diagnostic behaviours,
on the part of both the physicians and the general population (Speizer et al. 1977).
More generally, it partly reflects the state-of-the-art of medical knowledge (Redelings
et al. 2007). For example, if the plausibility of a combination of causes is high—or is
already well established—then the physicians will be more likely to report these
causes on the certificate. In addition, given that the death certificate is designed to
select the underlying cause, the certifying physician is required to make a decision
about the single etiological sequence ending in death. This too may prevent him/her
from describing the clinical course of death completely (Guralnick 1966).
Another matter of concern for the quality of the MCOD data, and more specifically
for its comparability across countries, is related to the format of the death certificate.
Many countries use adaptations of the WHO recommended death certificate. Even
slight deviations from the WHO certificate may have a considerable impact on the
data. For example, one important difference between the French and the Italian death
certificates4 is the number of lines available to describe the morbid process: there are
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.
123
3,5
Average number of causes

2,5
Part I - France
2 Part I -Italy
Part II - France
Part II -Italy
1,5 Part I&II - France
Part I&II -Italy
1
0,5
0
1-9 10- 20- 30- 40- 50- 60- 70- 80- 90+
19 29 39 49 59 69 79 89
Fig. 1 Average number of causes reported on death certificates, all entries and entries on parts I and II—
deaths over the age of one, excluding deaths from external causes, France and Italy, 2003. Mechanisms of
death and ill-defined contributing causes are excluded. Data France: Inserm CépiDc mortality database/
Italy: Istat mortality database
13 lines in Italy (8 in part I, 5 in part II5) versus 6 in France (4 in part I, 2 in part II). This
is may explain why, on average, more causes are listed in Italy (4.0) than in France
(3.1). Some of the reported contributing conditions are ill-defined causes or
mechanisms of death that do not shed light on the mortality process. In a previous
study (Désesquelles et al. 2010), we found that these causes are more frequently
reported as contributing causes in Italy.6 For the remainder of this article, all ill-defined
causes or mechanisms of death as contributing cause entered on death certificates have
been excluded from the computation.7
Figure 1 displays the average number of causes entered on death certificates in
France and Italy by age, for all entries as well as for entries on parts I and II
separately. The average number of entries on part II is very similar in the two
countries. So the difference between the two countries is explained by the fact that
the Italian certifying physicians report more causes on the first part of the death
certificate. Figure 1 also shows that the average number of reported causes varies by
age. Both real differences in the morbid process and variations in certification
practices by age at death may explain this finding. The increase up to age 80
(Mackenbach et al. 1995; Désesquelles and Meslé 2004; Désesquelles et al. 2010) is
consistent with the increased frequency of comorbidity with age, but the subsequent
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.
123
decline is more puzzling. We cannot rule out a selection effect, people with fewer
diseases are likely to live longer. But we suspect that it is an artefact resulting from a
less thorough description of the morbid process when death occurs at very old ages.
At this point it is worth noting that when comparing the two countries for some
specific underlying causes of death, the situation may be very different from the one
described above. Figures 2a–c display the average number of death certificate entries
by age in France and Italy for three underlying causes that exemplify the main patterns
emerging from the comparison of the two countries. In the first pattern (corresponding
to the leading causes of death: neoplasms, diseases of the circulatory system and
diseases of the respiratory system), more causes are mentioned in Italy than France at
all ages, and the gap increases with age. The second pattern (infectious and parasitic
diseases as well as diseases of the endocrine, nutritional and metabolic system,
diseases of the digestive system and diseases of the skin and the subcutaneous tissue)
differs from the first one insofar as the gap between the two countries remains stable
with age. For all other underlying causes of death, the average number of entries is very
similar in the two countries, and there is no decline with age of the average number of
entries on the death certificates. So for these underlying causes of death, the
differences in death certificate format have no impact.
Apart from the effect of age and UCD, several other characteristics of the
decedent may affect the number of causes reported on the death certificate. For
example, the information available to the certifying physician is likely to be more
precise when death occurs in a medical structure. Marital status may also play a
role: the spouse, if present, may provide information on the decedent’s medical
history. We use a Poisson model to examine simultaneously the effect of the
following decedent characteristics on the number of listed causes: age at death,
UCD, sex, marital status (married, never married, widowed and divorced) and place
of death (hospital, residence for elderly people, private residence, other place). The
results for the two countries (Table 1) are very similar. As models are performed on
large numbers (507,547 deaths in France and 550,835 in Italy), almost all effects
reach statistical significance. After controlling for all characteristics, the shape of
the number of reported causes by age (increase followed by a decline in the oldest
age groups) is confirmed. We find fewer reported causes for females and for never-
married decedents but corresponding relative risks are only slightly under one. The
effect of the place of death is clearer: more causes are reported when death occurred
in hospital and, for Italy, in a residence for elderly people. The lowest relative risk is
for deaths occurring in a private residence. All these results are very similar to those
obtained by Wall (2005) with US data, except for marital status. In her study, death
certificates of married people less frequently listed more than one reported
condition. Regarding the UCD, some causes (diseases of the musculoskeletal
system/connective tissue, diseases of the digestive system, endocrine, nutritional
and metabolic diseases, as well as infectious and parasitic diseases) are associated
with a higher number of reported conditions, and some others (diseases of the
nervous system, mental and behavioural disorders, diseases of the respiratory
system and, not surprisingly, ill-defined causes/mechanisms of death) with a lower
number. The two main causes of death (neoplasms and diseases of the circulatory
system) occupy an intermediate position.
123
(a)

4,00
3,50
3,00
France
2,50
Italy
2,00
1,50
1,00
1-9 10- 20- 30- 40- 50- 60- 70- 80- 90+
19 29 39 49 59 69 79 89
(b)
4,00
3,50
3,00
France
2,50
Italy
2,00
1,50
1,00
1-9 10- 20- 30- 40- 50- 60- 70- 80- 90+
19 29 39 49 59 69 79 89
(c)
4,00
3,50
3,00
France
2,50
Italy
2,00
1,50
1,00
1-9 10- 20- 30- 40- 50- 60- 70- 80- 90+
19 29 39 49 59 69 79 89
Fig. 2 Average number of causes reported on death certificates by age for three underlying causes of
death. Deaths over the age of one, France and Italy, 2003. a Neoplasms as UCD. b Infectious and parasitic
diseases as UCD. c Diseases of the nervous system as UCD. Mechanisms of death and ill-defined
contributing causes are excluded. Data France: Inserm CépiDc mortality database/Italy: Istat mortality
database
2 Indicators
A variety of indicators have been developed to describe the frequency of multiple-

cause death certificate entries and to investigate relations between contributing and
underlying causes of death. We have already mentioned the average number of
123
Table 1 Impact of various decedent characteristics on the number of causes reported on the death
certificate: relative risks resulting from a Poisson model
France Italy
Age at death
1–39 0.92 0.85
40–49 0.95 0.91
50–59 0.97 0.93
60–69 0.99 0.96
70–79 Ref Ref
80–89 0.98 1.00 ns
90? 0.93 0.94
Sex
Males 1.03 1.02
Females Ref Ref
UCD
Infectious and parasitic diseases 1.07 1.13
Neoplasms 1.00 1.02
Diseases of the blood and blood-forming organs 1.11 1.00 ns
Endocrine, nutritional and metabolic diseases 1.18 1.15
Mental and behavioural disorders 0.96 0.81
Diseases of the nervous system 0.93 0.87
Diseases of the circulatory system Ref Ref
Diseases of the respiratory system 0.96 0.93
Diseases of the digestive system 1.12 1.06
Diseases of the skin and subcutaneous tissue 1.01 ns 0.93
Diseases of the musculoskeletal system/connective tissue 1.25 1.10
Diseases of the genitourinary system 1.12 0.98
Other diseases 1.20 1.09
Symptoms, signs, abnormal findings, ill-defined causes 0.44 0.36
and Mechanisms of death
Marital status
Divorced 1.00 ns 1.00 ns
Widowed 1.00 ns 1.00 ns
Never married 0.99 0.98
Married Ref Ref
Place of death
Private residence 0.87 0.90
Hospital Ref Ref
Residence for elderly people 0.96 1.04
Other 0.89 0.96
Mechanisms of death and ill-defined contributing causes are excluded. Deaths over the age of one,
excluding deaths from external causes, France and Italy, 2003. Data: France: Inserm CépiDc mortality
database/Italy: Istat mortality database
ns not significant
123
multiple causes, which is a summary indicator of the distribution of causes reported

on death certificates (Israel et al. 1986; Mackenbach et al. 1995). Basic descriptive
indicators also include MCOD rates that are based on counts of deaths for which a
given condition is mentioned as UCD or contributing cause. The ratio of multiple
(or, in some studies, contributing) cause to underlying cause is used to measure the
extent to which the role played by a given disease or condition is underestimated in
overall mortality when the analysis is performed using the underlying cause only
(Goodman et al. 1982; Australian Bureau of Statistics 2003; Goldacre et al. 2003). It
can be computed on the basis of absolute counts of deaths or of rates. The inverse of
this ratio, representing the relative number of times a cause of death is selected as
the underlying cause, is sometimes interpreted as an indirect indicator of the
severity of the disease under study (Stallard 2002). When comparisons are
performed, standardized indicators must be used (Stallard 2002; Désesquelles et al.
2010). In this study, we compute standardized ratios of multiple to underlying cause
(SRMU). For a given cause of death, the SRMU is defined as the ratio between the
multiple-cause mortality rate and the underlying-cause mortality rate, both
standardized by age and sex.
Regarding cause combinations, the simplest indicator, frequently referred to as
‘prevalence at death’ (Markush and Seigel 1968), is the share of the certificates
mentioning a particular condition among all deaths attributable to a given UCD
(Coste and Jougla 1994; Mannino et al. 1998). Its structure is that of a proportionate
mortality ratio, initially developed in the field of occupational epidemiology and
later adapted to MCOD analysis (Frenzen 2003). The age-standardized prevalence
at death, conditional to the underlying cause u, is given by the following formula:
P u dc;x
x u dx d x
SPc=u ¼ P
x dx
u dc;xis the number of deaths observed at age x with underlying cause u and con-
tributing cause c; u dx is the number of deaths observed at age x with cause u as
underlying cause; dx is the standard number of deaths at age x
Following a more investigative approach, several indicators have been elaborated
to determine the strength of any association of causes of death. Considering that the
reporting of a cause on the death certificate is a dichotomous event, the strength of a
given association can be estimated with odds ratios. The odds ratio for causes A and
B is defined as the ratio between the odds of cause B being reported on the
certificate, when cause A is also mentioned, divided by the odds of cause B being
reported, when cause A is not mentioned (Chamblee and Evans 1982; Smith and
Kliewer 1995; Wilkins et al. 1997; Redelings et al. 2007; Frova et al. 2009). The
ratio of observed to expected joint frequencies is another commonly used indicator.
In its general form, it is computed as the ratio between the actual number of deaths
involving a given combination of causes, and the expected number of deaths with
that combination, assuming that the combined causes are independent (Israel et al.
1986; Stallard 2002). A ratio over one suggests that causal relations between the
combined causes may exist (Australian Bureau of Statistics 2003). Mackenbach
et al. (1995) have proposed a more refined indicator. The ‘standardized prevalence
123
ratio’ is the result of an indirect standardization procedure: the age- and sex-specific
prevalence rates of a contributing cause among all deaths are applied to the age and
sex distribution of the deaths attributed to a given UCD to compute an expected
number of deaths. Having the structure of a standardized mortality ratio, this
indicator depends on the age and sex distribution of the UCD under study. As a
consequence, direct comparisons between underlying causes are not allowed. To
overcome this problem, we developed the cause of death association indicator
(CDAI) that can be used to compare various UCDs within a country, as well as
across various countries for a given UCD (Désesquelles et al. 2010). In the formula
of the CDAIs, both the observed and expected prevalence rates are age standardized.
The CDAI between a contributing cause c and an underlying cause u compares how
frequently (1) the cause c is contributing to deaths assigned to the underlying cause
u and (2) the cause c is contributing to all deaths of the country. It is thus the ratio
between an observed and an expected proportion of deaths with cause c as
contributing cause. It is worth noting that the CDAI may also be seen as the ratio
between the standardized prevalence at death of the combination u, c conditional to
the specific underlying cause u (SPc/u), and the unconditional standardized
prevalence of the same contributing cause (SPc)8:
P u dc;x P
P u dc;x
SPc=u x u dx d x x dx x dx
CDAIu;c ¼ ¼ P P 100 ¼ P du dc;xx 100
SPc dc;x
d x d x x d x
x dx x d x
u dc;xis the number of deaths observed at age x with underlying cause u and con-
tributing cause c; u dx is the number of deaths observed at age x with cause u as
underlying cause; dc;x is the total number of deaths observed at age x with cause c as
contributing cause (regardless of the underlying cause) dx is the total number of
deaths observed at age x (regardless of the underlying cause); dx is the standard
number of deaths at age x.
Note that the leading causes of death contribute more to the value of the
denominator of this indicator than other causes of death. As a consequence,
associations involving causes that frequently contribute to deaths due to a cancer or
a disease of the circulatory system are less likely to emerge as strong associations.
d
One possible alternative consists in replacing the dc;xx terms in the denominator by the
d
average value, for the various UCDs, of the uu dc;xx terms. In fact, both formulas lead to
very similar results.9
Finally, a choice needs to be made about how to count causes reported on a given
death certificate that belong to the same group under the classification used for the
8
As the indicator is based on the ratio of averages, age distributions of its components (udc,x/udx and dc,x/
dx) 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.
123
analysis. In this study, for the computation of the SRMUs, these causes are counted
only once. For CDAIs, whatever the underlying cause of death,10 only one mention
of a given group as contributing cause is considered in the computation of the
indicator. Distinct ICD-10 codes that are considered ‘redundant’ with an aggregated
classification, could of course be considered as different if a more detailed
categorization was chosen. This implies that values of the CDAIs computed at
different levels of the classification cannot be compared.
3 Results
3.1 Mortality Levels
Table 2 displays the basic descriptive indicators computed for all deaths involving a
neoplasm. When only the underlying cause of death is accounted for, the
standardized11 mortality rate for neoplasms is only slightly higher in France
(1,957 per million) than in Italy (1,918 per million). As the cancer-specific SRMU is
1.1 in both countries, the situation is unchanged when all mentions of a neoplasm
are accounted for (2,125 per million in France vs. 2,110 per million in Italy). Most
site-specific values of the SRMU are very close to one. If we exclude the secondary
malignant neoplasms that, not surprisingly, are mainly mentioned as a contributing
cause, the highest values are for the ‘malignant neoplasms of ill-defined/unspecified
and independent primary multiple sites’ (9.0 in Italy and 3.2 in France), for ‘benign
neoplasms/neoplasms of uncertain or unknown behaviour’ (1.7 in Italy and 1.6 in
France), and for ‘malignant neoplasms of the skin and the subcutaneous tissue’ (1.5
in both countries) and ‘malignant neoplasms of the prostate’ (1.4 in both countries).
The ranking of the mortality rates by anatomic site produces results that are
almost unchanged when all causes are taken into account. In both countries,
‘malignant neoplasms of larynx, trachea, bronchus and lung’ come first, followed by
‘malignant neoplasms of small intestine, colon, rectum, anus and other/ill-defined
digestive organs’ and ‘malignant neoplasm of lymphoid, haematopoietic and related
tissue’. In Italy, the ranking of the three following sites (‘liver, intrahepatic bile
ducts, gallbladder and other unspecified parts of biliary tract’, ‘breast’ and
‘stomach’) is unchanged. In France, ‘malignant neoplasms of breast’ and ‘malignant
neoplasms of prostate’ exchange their rankings. In both the single and the MCOD
approach, ‘malignant neoplasms of liver, the intrahepatic bile ducts, gallbladder and
other unspecified parts of biliary tract’ and ‘malignant neoplasms of stomach’ rank
lower in France than in Italy. In contrast, rates for malignant neoplasms of prostate,
of oesophagus, and for ‘malignant neoplasms of lip, oral cavity, pharynx’ are higher
in France.
In all, the impact of the MCOD approach in terms of cancer-related mortality
levels is modest. The most notable exception is for neoplasms of the prostate. In a
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.
123
Table 2 Standardized mortality rates (per million) for each cause reported as underlying cause or
multiple cause and standardized ratio of multiple to underlying cause (SRMU)—Neoplasms, France and
Italy, 2003
Underlying Multiple causea SRMU
cause
Italy France Italy France Italy France
Malignant neoplasm of lip, oral cavity, pharynx 36 65 42 78 1.2 1.2

Malignant neoplasm of oesophagus 23 58 25 68 1.1 1.2
Malignant neoplasm of stomach 122 60 134 66 1.1 1.1
Malignant neoplasm of small intestine, colon, 225 213 257 242 1.1 1.1
rectum, anus and other/ill-defined digestive organs
Malignant neoplasm of liver, the intrahepatic bile 147 110 161 124 1.1 1.1
ducts, gallbladder and other unspecified parts
of biliary tract
Malignant neoplasm of pancreas 96 91 101 95 1.0 1.0
Malignant neoplasm of larynx and trachea/ 425 403 458 442 1.1 1.1
bronchus/lung
Malignant melanoma of skin 19 19 21 21 1.1 1.1
Malignant neoplasm of skin 5 6 7 8 1.5 1.5
Malignant neoplasm of breast 125 131 145 152 1.2 1.2
Malignant neoplasm of cervix uteri and other 27 33 32 38 1.2 1.2
parts of uterus
Malignant neoplasm of ovary 33 37 36 40 1.1 1.1
Malignant neoplasm of prostate 94 122 129 166 1.4 1.4
Malignant neoplasm of kidney 35 40 41 47 1.2 1.2
Malignant neoplasm of bladder 58 56 75 70 1.3 1.2
Malignant neoplasm of lymph./haematopoietic tissue 153 150 185 179 1.2 1.2
Malignant neoplasm of eye, brain and other parts 43 46 46 48 1.1 1.1
of central nervous
Secondary malignant neoplasm 14 0 733 651 53.6 –
Malignant neoplasm of ill-defined/unspecified 87 183 785 586 9.0 3.2
and independent (primary) multiple sites
Other malignant neoplasms 65 64 75 73 1.2 1.2
Benign neoplasms/Neoplasms of uncertain 87 71 152 113 1.7 1.6
or unknown behaviour
All neoplasms 1918 1957 2110 2125 1.1 1.1
All deathsb 5620 5514 10725 9383 1.9 1.7
In France, there are very few deaths with a secondary malignant neoplasm as underlying cause, and the
corresponding SRMU has not been computed. Data: France: Inserm CépiDc mortality database/Italy: Istat
mortality database
a
Mechanisms of death and ill-defined contributing causes are excluded
b
Excluding deaths due to external causes and infant deaths
recent article based on US mortality data, Fink et al. (2011) also find that neoplasms
of the prostate are frequently reported as contributing cause of death. They suggest
that this might indicate better survival chances for this cancer. But it may also
123
reflect the fact that diagnosis often occurs at advanced ages when people may have
already developed other diseases.
3.2 Combinations of Causes
In both countries, the average number of causes reported on death certificates with a
neoplasm as UCD is higher than for all causes of death taken together (3.1 vs. 2.9 in
Italy, 2.5 vs. 2.4 in France), and the share of those certificates with no contributing
cause is lower (10 vs. 16 % in Italy, 23 vs. 33 % in France). When looking at the
standardized prevalence rates of the various combinations of causes (see Tables 3
and 4 in the appendix), we find that for all anatomic sites, the most frequent
associations are with neoplasms, diseases of the circulatory system, diseases of the
respiratory system, as well as—but to a lesser extent—diseases of the digestive
system and endocrine, nutritional and metabolic diseases. As these groups of causes
are the main killers in the two countries (Désesquelles et al. 2010), we suspect that
some of these associations are not specific to cancer-related mortality. And indeed,
the examination of the CDAIs provides a quite different picture. Figure 3a
(respectively Fig. 3b) display the contributing (respectively, underlying) causes of
death for which a neoplasm is mentioned as underlying (respectively contributing)
cause of death more frequently than expected. The next graphs (Fig. 4 for France
and Fig. 5 for Italy) display the CDAIs computed at a more detailed level of
classification12 for all deaths with a malignant neoplasm as UCD.13 The cells of the
table that result from the cross-matching of every site-specific malignant neoplasm
as UCD and every contributing cause of death are coloured according to the value of
the corresponding CDAI. After computing the standard deviation (r) of the
CDAIs,14 we created five classes: [0;100[, [100;100 ? r/4[, [100 ? r/4;100 ? r/
2[, [100 ? r/2;100 ? 3r/4[and [100 ? 3r/4;?[.The first class is white while all
other classes are progressively darker shades of grey.
In Fig. 3a, b, the similarity of the results for the two countries is very striking.
The frequent association we noted earlier between neoplasms and diseases of the
circulatory/respiratory system when commenting the standardized prevalence rates
is no longer visible (CDAIs are under 100). In contrast, this analysis confirms that
the simultaneous reporting of a neoplasm as underlying and contributing cause of
death is a feature of cancer-related mortality. When a neoplasm is mentioned as
contributing cause (Fig. 3b), no other associations have a CDAI over 100. Figures 4
and 5 show that for almost all anatomic sites as UCD, a secondary malignant
neoplasm or a ‘malignant neoplasm of ill-defined/unspecified and independent
primary multiple sites’ is very frequently reported as contributing cause of death.
For some of the emerging associations, the UCD and the contributing cause belong
to the same group (e.g. Intest/Intes, Haem/Haem), or involve proximate anatomic
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.
123
Ext OIlldef
Other Mecha
OGen Senil
Hyppro Other
OKidn OGen
Renal Hyppro
OMusc OKidn
Arthr Renal
Skin OMusc
ODiges Arthr
Chroliv Skin
Ulcer ODiges
Chroliv
OResp
Ulcer
Lung
OResp
Chrolow
Lung
Asthm Chrolow
Aculow Asthm
Pneu Aculow
Influ Pneu
OCirc Influ
Hypten OCirc
Cereb Hypten
OHeart Cereb
Ischae OHeart
ONerv Ischae
Parki ONerv
Alzh Parki
CONTRIBUTING CAUSE
Alzh
UNDERLYING CAUSE
Epi
OMent Epi
Demen OMent
Drug Demen
Alco Drug
OEndo Alco
OEndo
Thyro
Thyro
Obes
Obes
Malnu Malnu
Diab Diab
Blood Blood
Neoplasm-France
Neoplasm-France
Beni Beni
Neoplasm-Italy
Neoplasm-Italy
ONeo ONeo
UnsNeo UnsNeo
SecNeo SecNeo
Brain Brain
Haem Haem
Blad Blad
Kidn Kidn
Prost Prost
Ova Ova
Uter Uter
Brea Brea
Skin Skin
Mela Mela
Lung Lung
Panc Panc
Liv
Liv
Intes
Intes
Stom
Stom Oeso
Oeso UpAero
UpAero OInfec
OInfec Infint
Infint Sept
Sept Hepa
Hepa AIDS
(b)
(a)
AIDS Tub
Tub
Fig. 3 CDAIs—France and Italy, 2003. a Neoplasms (all anatomic sites) as UCD. b Neoplasms (all
anatomic sites) as contributing cause of death. The area of a circle is the value of the CDAI. Values of the
indicator under 100 and/or corresponding to fewer than 50 cases are not shown. See abbreviations in the
Table 5 in appendix. Data France: Inserm CépiDc mortality database/Italy: Istat mortality database
sites, such as sites of the digestive system (e.g. Intes/Stom, Intes/Intes15) or the
upper aerodigestive tract (UpAero/UpAero), reflecting the fact that cancers of any
tissue are likely to spread to neighbouring tissue. Concomitant use of alcohol and
15
See abbreviations in the Table 5 in appendix.
123
Fig. 4 CDAIs—associations (vertical axis) with neoplasms as UCD (horizontal axis)—France, 2003.
Values of the indicator under 100 and/or corresponding to fewer than 50 cases are not shown. See
abbreviations in the Table 5 in appendix. Data Inserm CépiDc mortality database
123
Fig. 5 CDAIs—associations (vertical axis) with neoplasms as UCD (horizontal axis)—Italy, 2003.
Values of the indicator under 100 and/or corresponding to fewer than 50 cases are not shown. See
abbreviations in the Table 5 in appendix. Data Istat mortality database
123
tobacco probably explains why, specifically to France, ‘neoplasms of larynx,

trachea, bronchus and lung’ are frequently reported as contributing cause of
neoplasms of oesophagus (Oeso/Lung) and ‘neoplasms of lip, oral cavity and
pharynx’ (UpAero/Lung). Tobacco use is also likely to be involved in the strong
association observed between ‘neoplasm of bladder’ and ‘neoplasm of larynx,
trachea, bronchus and lung’ (Blad/Lung in France, Lung/Blad in Italy). The link
between cigarette smoking and bladder cancer is indeed well established (Sasco
et al. 2004). The association between ‘neoplasm of larynx, trachea, bronchus and
lung’ and ‘neoplasm of prostate’ (Lung/Pros, Pros/Lung) may have a common
origin in tobacco use, perhaps through its effect on sex hormone metabolism; but
this link is a matter of debate (Matzkin and Soloway 1993; Van der Gulden et al.
1994).
When the underlying cause of death is a neoplasm (Fig. 3a), several associations
with other groups of causes have high CDAIs. Based on our knowledge of the
medical state-of-the-art, they can be categorized according to the following lines of
interpretation:
1. Cancer results from the degeneration of the contributing cause. As this
contributing cause preceded cancer, one might expect it to be selected as the
UCD. But in some cases, the WHO rules preclude this option. As an example,
only the MCOD approach is able to highlight the strong contribution of viral
hepatitis and chronic liver diseases to ‘neoplasms of liver, intrahepatic bile
ducts, gallbladder and other unspecified parts of biliary tract’ (Liv/Hepa and
Liv/Chroliv on Figs. 4, 5).
2. The contributing cause is a risk factor for cancer. Alcohol and tobacco use that,
specifically to France, emerge as a frequent contributing cause of several
neoplasms (UpAero/Alco, Oeso/Alco, Liv/Alco, UpAero/OMent,16 Oeso/OMent,
Lung/OMent) are emblematic of that situation.
3. The contributing cause and the cancer have a common cause. The role played
by tobacco use in the associations noted before between neoplasm of bladder
and lung cancer illustrates this point. Tobacco use might also explain the
frequent association observed in Italy between hyperplasia of prostate and lung
cancer (Lung/Hyppro) (Matzkin and Soloway 1993). Similarly, we suspect that
the combination between ‘malignant neoplasm of larynx and trachea/bronchus/
lung’ and tuberculosis (Lung/Tub) that is found in both countries, and that is
well documented too, reflects precarious social situations that are associated
with higher risks for both conditions (e.g. tobacco use, exposure to silicosis).
However, other explanations are possible. Recent results support the hypothesis
of an increased lung cancer risk in patients with tuberculosis (Vento and
Lanzafame 2011). It is also suggested that immunodeficiency due to the
neoplastic disease itself or its therapy could cause a reactivation of pre-existing
‘latent’ tuberculosis (Kaplan et al. 1974). Specifically to Italy, we find a
frequent association between viral hepatitis (mainly: chronic viral hepatitis C)
and ‘malignant neoplasm of lymphoid, haematopoietic and related tissue’
16
‘Mental and behavioural disorders due to use of tobacco’ (ICD-10 F179 code) is classified in the
‘Other Mental and behavioural disorders’ group.
123
(mainly: Non-Hodgkin’s lymphoma (Haem/Hepa)).The possibility that the

HCV virus plays a role on the onset of both diseases has been documented with
conflicting results in the literature (Mele et al. 2003). Finally, the association we
find between neoplasm of breast and Alzheimer’s disease (Brea/Alzh) in France,
and arthrosis (Brea/Arthr) in Italy also echoes recent medical research on
potential shared mechanisms between breast cancer tumorigenesis on the one
hand, and neurodegenerative processes, oxidative stress and inflammation on
the other (Staropoli 2008; Pavlides et al. 2010; Hedskog et al. 2011).
4. The contributing cause is a consequence or a complication of cancer. Figures 3,
4 and 5 provide numerous examples of this case. The combination between
neoplasms and ‘malnutrition and other nutritional deficiencies’ is one of them.
In Fig. 3a, it is visible in France only, but in Figs. 4 and 5, strong associations
between malnutrition and several anatomic sites of the upper aerodigestive
tract/digestive system (UpAero/Malnu, Oeso/Malnu, Stom/Malnu, Intes/Malnu
in France, Stom/Malnu, Intes/Malnu in Italy) are found in both countries. One
possible consequence of those cancers is an inability to eat normally. Similarly,
we suspect that bone metastases are involved in the association between ‘other
diseases of the musculoskeletal system/connective tissue’ (mainly: pathological
fractures) and several anatomic sites (Brea/OMusc, Pros/OMusc, Haem/
OMusc). Other examples are renal failure as contributing cause of several
neoplasms (Uter/Renal, Blad/Renal, Pros/Renal, Kidn/Renal, Haem/Renal), as
well as septicaemia, other infectious diseases, pneumonia and ‘other endocrine,
nutritional and metabolic diseases’ (mainly: disorders of calcium metabolism,
amyloidosis, volume depletion and other disorders of fluid, electrolyte and
acid–base balance) as contributing cause of ‘malignant neoplasm of lymphoid,
haematopoietic and related tissue’ (Haem/Sept, Haem/Oinfec, Haem/Pneu,
Haem/OEndo). Though it is probably difficult to distinguish between the two, it
should be noted that the contributing cause may be a consequence of the
neoplasm or of its therapy. The strong association between ‘diseases of the
blood (-forming organs), immunological disorders’ (mainly: anaemia, throm-
bocytopenia and immunodeficiency) and several anatomic sites (UpAero, Oeso,
Stom, Intes, Uter, Ova, Pros, Kidn, Blad, Haem) potentially illustrates the latter
case.
In all these examples, the similarity of the findings for the two countries is very
striking. However, a few associations in this category are country-specific. For Italy,
the observed association between external causes (mainly: surgical operation and
other surgical procedures, medical procedures as the cause of abnormal patient
reaction) and several neoplasms (UpAero/Ext, Stom/Ext, Kidn/Ext, Brea/Ext) is one
of them. For France, we find a frequent association between cancers and infectious
intestinal disease (mainly: diarrhoea and gastroenteritis of presumed infectious
origin), between external causes (mainly: foreign body in respiratory tract) and
malignant neoplasm of oesophagus (Oeso/Ext), as well as between ‘other endocrine,
nutritional and metabolic diseases’ (mainly: disorders of calcium metabolism,
volume depletion, and other disorders of fluid, electrolyte and acid–base balance)
and neoplasms of kidney (Kidn/OEndo) and bladder (Blad/OEndo). These
123
associations do not really challenge medical knowledge, and as they do not emerge
in both countries, we suspect that they reflect differences in French and Italian
certifying practices. The coincidence of thyroid disorders (mainly: hypothyroidism)
and breast cancer (Brea/Thyro), also specific to France, is more challenging, and a
topic of debate in the scientific literature. Hypothyroidism may be a consequence of
radioactive therapies (Daoud et al. 2005) but it is also suggested that thyroid
abnormalities could play a causal role in the development and progression of breast
cancers (Smyth 1997).
5. Among the various consequences/complications of cancers, symptoms may also
be distinguished—though the distinction is probably tenuous. As an example, in
both countries, brain cancer is frequently combined with epilepsy and other
diseases of the nervous system (mainly: benign intracranial hypertension,
compression of brain, cerebral oedema).
This categorization is necessarily a bit oversimplified, and in many cases it is
difficult to say whether an association belongs to one or another category. Frequent
associations involving ‘other diseases of the digestive system’ (Oeso/ODiges, Stom/
ODiges, Intes/ODiges, Liv/ODiges, Panc/ODiges), ‘other diseases of kidney and
ureter’ (Intes/OKidn, Uter/OKidn, Pros/OKidn, Blad/OKidn, Haem/OKidn), ‘other
diseases of the genitourinary system’ (Intes/OGen, Brea/OGen, Uter/OGen, Pros/
OGen, Kidn/OGen, Blad/OGen) or respiratory diseases (Chrolow, Lungdis, Oresp)
as contributing cause of death may well belong to any of these categories.
In the end, very few strong associations remain difficult to interpret. For instance,
it is unclear why, specifically to France, ‘other diseases of the circulatory system’
(mainly: pulmonary embolism, phlebitis and thrombophlebitis) emerge as a
contributing cause for neoplasm of uterus (Uter/OCircu). Similarly, we could not
find any explanation for the observed contribution of Alzheimer’s disease to
neoplasm of bladder (Blad/Alzh), and of ‘other diseases of the nervous system’
(mainly: benign intracranial hypertension, compression of brain, cerebral oedema),
to melanoma (Mela/ONerv) and neoplasm of kidney (Kidn/ONerv). Further research
on these associations is certainly indicated.
4 Conclusions
Our study leads to several firm conclusions. Concerning the quality of the MCOD
data, it is sometimes argued that a higher average number of causes per certificate
signals better diagnosis and more complete recording and, as a consequence, better
quality (White et al. 1989). The fact that the number of reported causes is higher
when death occurs at hospital supports this argument. As the average number of
mentions is higher in Italy, this tends to indicate better quality of the MCOD data in
this country. In any event, the similarity of the results of our study of cancer-related
mortality in France and Italy is very striking. It is tempting to interpret this
similarity as a positive signal for data quality, but caution is required. First, though
we do not consider it very likely, we cannot rule out that similar biases lead to
similar results. Second, we obviously cannot presume that this similarity holds true
123
for other causes of death. Note that while it is sometimes difficult to determine
primary and secondary anatomic sites, the reporting of the morbid process involving
a cancer may be less problematic than for other causes of death. People with cancer
usually receive regular medical follow-up, and the circumstances surrounding their
death are likely to be well described.
The fact that most of our results are in line with medical knowledge or with
ongoing debate in the medical literature speaks in favour of good data quality.
Hence, the MCOD approach can help to identify associations which, though not
currently validated by medical knowledge, should be taken seriously and
investigated further. Regarding the causes that frequently contribute to cancer
mortality, we were able to classify our results into five patterns of associations. It
will be interesting to examine how far these patterns apply to diseases other than
neoplasms.
As neoplasms are very often mentioned as the underlying cause of death, the
impact of the MCOD approach in terms of mortality levels is modest. Yet, the case
of cancer of the prostate, for which the impact is greater than for other sites,
suggests that with improved survival and increased incidence of cancers at old ages,
neoplasms may be mentioned more frequently as contributing causes of death. So,
we recommend that the MCOD approach can be used to monitor cancer-related
mortality.
Appendix
See Figs. 6 and 7; Tables 3, 4 and 5.
Fig. 6 French death certificate
123
Fig. 7 Italian death certificate
123
Table 3 Standardized prevalence at death (per 1,000)—Neoplasms as UCD—France, 2003
Infectious Neoplasms Diseases of the Endocrine, Mental and Diseases of Diseases of Diseases of Diseases of Diseases of the Diseases of the Diseases of the Other External
and blood (-forming nutritional and behavioural the nervous the the the digestive skin and musculoskeletal genitourinary diseases causes
parasitic organs), metabolic disorders system circulatory respiratory system subcutaneous system / system
diseases immunol.disorders diseases system system tissue connective tissue
123
Malignant neoplasm of lip, oral cavity &
40 303 81 75 146 140
pharynx
Malignant neoplasm of oesophagus 43 350 75 46 136 160 114 44
Malignant neoplasm of stomach 504 82 167 67 148
Malignant neoplasm of small intestine,
51 617 70 176 65 187 42
colon, rectum & anus
Malignant neoplasm of liver, intrahepatic
bile ducts, gallbladder&other parts of 108 258 89 43 156 49 346
biliary tract
Malignant neoplasm of pancreas 436 80 137 155
Malignant neoplasm of larynx, trachea,
417 57 65 188 160
bronchus & lung
Malignant melanoma of skin 834 51 81 122 69 51
Malignant neoplasm of skin 523 103 209 102
Malignant neoplasm of breast 735 77 45 188 89 62
Malignant neoplasm of cervix uteri & other
50 600 79 179 49 99 98
parts of uterus
Malignant neoplasm of ovary 702 48 131 60 166 42
Malignant neoplasm of prostate 45 633 43 72 40 211 106 53 110
Malignant neoplasm of kidney 696 97 213 89 53 120
Malignant neoplasm of bladder 54 512 76 190 83 72 162
Malignant neoplasm of lymphoid
141 153 155 82 224 158 52 87
/haematopoietic tissue
Malignant neoplasm of eye, brain & other
181 69 192 170 100
parts of central nervous system
Secondary malignant neoplasm
Malignant neoplasm of illdef./unspec./
44 677 72 42 180 97 85 44
independent primary multiple sites
Other Malignant neoplasms 469 71 173 103 54 60
Benign neoplasms and in situ neoplasms or
83 70 81 90 53 108 274 138 114 78 50
uncertain or unknown behaviour
Values of the indicator under 40 per 1,000 and/or corresponding to fewer than 50 cases are not shown
Data Inserm CépiDc mortality database
Table 4 Standardized prevalence at death (per 1,000)—Neoplasms as UCD—Italy, 2003
Infectious Neoplasms Diseases of the Endocrine, Mental and Diseases Diseases of Diseases of Diseases of Diseases of the Diseases of the Diseases of the Other External
and blood (-forming nutritional behavioural of the the the the skin and musculoskeletal genitourinary diseases causes
parasitic organs), and disorders nervous circulatory respiratory digestive subcutaneous system / system
diseases immunol.disorders metabolic system system system system tissue connective tissue
diseases
Malignant neoplasm of lip, oral cavity &
677 65 263 151 74
pharynx
Malignant neoplasm of oesophagus 684 57 78 249 182 156
Malignant neoplasm of stomach 700 86 61 245 101 199 61
Malignant neoplasm of small intestine,
725 54 68 265 103 219 87
colon, rectum & anus
Malignant neoplasm of liver,
intrahepatic bile ducts, 103 463 95 248 84 504 79
gallbladder&other parts of biliary tract
Malignant neoplasm of pancreas 682 126 230 78 260 67
Malignant neoplasm of larynx, trachea,
580 64 307 252 44 50
bronchus & lung

Malignant melanoma of skin 856 65 50 254 83 49 58
Malignant neoplasm of skin 734 332 140
Malignant neoplasm of breast 796 78 290 139 82 67
Malignant neoplasm of cervix uteri &
763 69 73 263 85 94 175
other parts of uterus
Malignant neoplasm of ovary 834 40 78 261 93 157 90
Malignant neoplasm of prostate 748 72 69 305 153 65 145
Malignant neoplasm of kidney 834 51 62 301 139 66 174
Malignant neoplasm of bladder 733 66 77 271 133 82 219
Malignant neoplasm of lymphoid
103 298 182 93 346 243 89 152
/haematopoietic tissue
Malignant neoplasm of eye, brain &
528 86 170 266 128 53
other parts of central nervous system
Secondary malignant neoplasm 49 137 97 47 305 153 284 134
Malignant neoplasm of illdef./unspec./
720 52 83 292 143 144 99
independent primary multiple sites
Other Malignant neoplasms 665 46 72 316 175 63 87
Benign neoplasms and in situ neoplasms
68 84 124 106 115 421 223 109 178
or uncertain or unknown behaviour
Values of the indicator under 40 per 1,000 and/or corresponding to fewer than 50 cases are not shown
Data Istat mortality database
123
Table 5 Groups of causes of death and abbreviations

Group # Abb. Groups and subgroups ICD-10 code
1 INF Infectious and parasitic diseases

Tub Tuberculosis A15–A19, B90
AIDS AIDS (HIV-disease) B20–B24
Hepa Viral hepatitis B15–B19, B94.2
Sept Septicaemia A40–A41
Intinf Intestinal infectious diseases A00–A09
OInfec Other infectious and parasitic diseases (A00–B99)–Supra codes
2 NEO Neoplasms
UpAero Malignant neoplasm of lip, oral cavity, C00–C14
pharynx
Oeso Malignant neoplasm of oesophagus C15
Stom Malignant neoplasm of stomach C16
Intes Malignant neoplasm of small intestine, C17, C18–C21, C26
colon, rectum and anus, and other/ill-
defined digestive organs
Liv Malignant neoplasm of liver, the C22–C24
intrahepatic bile ducts, gallbladder
and other unspecified parts of biliary
tract
Panc Malignant neoplasm of pancreas C25
Lung Malignant neoplasm of larynx and C32–C34
trachea/bronchus/lung
Mela Malignant melanoma of skin C43
Skin Malignant neoplasm of skin C44
Brea Malignant neoplasm of breast C50
Uter Malignant neoplasm of cervix uteri and C53, C54, C55
other parts of uterus
Ova Malignant neoplasm of ovary C56
Prost Malignant neoplasm of prostate C61
Kidn Malignant neoplasm of kidney C64
Blad Malignant neoplasm of bladder C67
Haem Malignant neoplasm of lymphoid, C81–C96
haematopoietic and related tissue
Brain Malignant neoplasm of eye, brain and C69–C72
other parts of central nervous system
SecNeo Secondary malignant neoplasm C77–C79
UnsNeo Malignant neoplasm of ill-defined/ C76, C80, C97
unspecified/independent (primary)
multiple sites
ONeo Other malignant neoplasms (C00–C99)—Supra codes
Beni Benign neoplasms, in situ neoplasms D00–D09, D10–D36, D37–D48
and neoplasms of uncertain or
unknown behaviour
3 BLOOD Diseases of the blood (-forming D50–D89
organs), immunol disorders
123
Table 5 continued
4 ENDOC Endocrine, nutritional and metabolic

diseases
Diab Diabetes mellitus E10–E14
Malnu Malnutrition and other nutritional E40–E64
deficiencies
Obes Obesity E65–E68
Thyro Disorders of thyroid gland E00–E07
OEndo Other endocrine, nutritional and (E00–E90)—Supra codes
metabolic diseases
5 MENT Mental and behavioural disorders
Alco Alcoholic psychosis/chronic alcohol F10.1–F10-9, G31.2
abuse
Drug Drug dependence, toxicomania F11–F16
except F11.0, F12.0, F13.0, F14.0,
F15.0, F16.0
F18, F19 except F18.0, F19.0
Demen Dementias (excluding Alzheimer’s) F01, F03, G31.0, G31.8, G31.1, G31.9
OMent Other mental and behavioural disorders (F00–F99) except F10.0, F11.0, F12.0,
F13.0, F14.0, F15.0, F16.0, F17.0,
F18.0, F19.0—Supra ‘F’ codes
6 NERV Diseases of the nervous system
Epi Epilepsy G40, G41
Alzh Alzheimer’s disease G30
Parki Parkinson’s disease G20, G21
ONerv Other diseases of the nervous system (G00–G98)—(G31.0–G31.2, G31.8,
G31.9)—Supra ‘G’ codes
7 CIRC Diseases of the circulatory system
Ischae Ischaemic heart diseases I20–I25
OHeart Other heart diseases I30–I33, I39–I45, I47, I48, I49.1–I52,
I00–I09
Cereb Cerebrovascular diseases I60–I69
Hypten Hypertensive diseases I10–I15
OCirc Other Diseases of the circulatory (I00–I99)—(I46, I49.0, I95.9, I99)—
system Supra codes
8 RESP Diseases of the respiratory system
Influ Influenza J10, J11
Pneu Pneumonia J12–J18
Aculow Other acute lower respiratory diseases J00–J09, J19–J22
Asthm Asthma J45, J46
Chrolow Other chronic lower respiratory J40–J44
diseases
Lungdis Lung diseases due to external agents J60–J70
OResp Other diseases of the respiratory (J00–J99)—(J96.0, J96.9)—Supra ‘J’
system codes
123
Table 5 continued
9 DIGES Diseases of the digestive system

Ulcer Ulcer of stomach, duodenum and K25–K28
jejunum
Chroliv Chronic liver disease K70, K73, K74
ODiges Other diseases of the digestive system (K00–K93)—Supra codes
10 SKIN Diseases of the skin and L00–L99
subcutaneous tissue
11 MUS Diseases of the musculoskeletal
system/connective tissue
Arthr Rheumatoid arthritis and osteoarthrosis M05, M06, M15–M19
OMusc Other diseases of the musculoskeletal (M00–M99)—Supra codes
system/connective tissue
12 GEN Diseases of the genitourinary system
Renal Renal failure N17–N19
OKidn Other diseases of kidney and ureter N00–N16
Hyppro Hyperplasia of prostate N40
OGen Other diseases of the genitourinary (N00–N99)—Supra codes
system
13 OTHER Other diseases
Pregn Complications of pregnancy, childbirth O00–O99
and puerperium
Perinat Certain conditions originating in the (P00–P96)—P28.5
perinatal period
Malfor Congenital malformations and Q00–Q99
chromosomal abnormalities
Eye Diseases of the eye and adnexia H00–H59
Ear Diseases of the ear and mastoid process H60–H95
SIDS SIDS R95
14 ILLDEF Symptoms, signs, abnormal findings
and ill-defined causes
Senil Senility R54
a
Mecha Mechanisms of the death I46, I49.0, R09.2, R40.2, R57
OIlldef Other symptoms, signs, abnormal (R00–R94), (R96–R99), I95.9, I99,
findings and ill-defined causesb J96.0, J96.9, P28.5, U00—Supra R
codes
15 EXT External causes S, T, V, W, X, Y codes and F10.0,
F11.0, F12.0, F13.0, F14.0, F15.0,
F16.0, F17.0, F18.0, F19.0
a
Cardiac arrest (I46.0), Ventricular fibrillation (I49.0), Respiratory arrest (R09.2), Coma (R40.2), Shock
(R57)
b
Hypotension (I95.9), Other unspecified disorders of circulatory system (I99), Acute respiratory failure
(J96.0), Respiratory failure unspecified (J96.9), Respiratory failure of newborn (P28.5)
123
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Analysing Multiple Causes of Death: Which Methods For Which Data? An

Article in European Journal of Population · November 2012

Aline Desesquelles Marilena Pappagallo

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Causes of death Bridge coding analysis Icd9 - Icd10 View project

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Analysing Multiple Causes of Death: Which Methods

Aline F. Désesquelles • Michele Antonio Salvatore •

Received: 2 January 2012 / Accepted: 31 July 2012

A. F. Désesquelles (&) F. Meslé

M. A. Salvatore M. Pappagallo L. Frova M. Pace

Keywords Multiple causes of death Mortality Cancer France Italy

Résumé La prise en compte pour l’étude de la mortalité de l’ensemble des causes

Mots-clés Causes multiples de décès Mortalité Cancer France Italie

1 MCOD Data: Collection and Quality

1.1 A Quite Recent Data source

1.2 Quality: ‘Could do Better!’

systematically and uniformly, irrespective of the coding agent or the country.

Average number of causes

Average number of causes

A variety of indicators have been developed to describe the frequency of multiple-

multiple causes, which is a summary indicator of the distribution of causes reported

3.1 Mortality Levels

Italy France Italy France Italy France

Malignant neoplasm of lip, oral cavity, pharynx 36 65 42 78 1.2 1.2

3.2 Combinations of Causes

tobacco probably explains why, specifically to France, ‘neoplasms of larynx,

(mainly: Non-Hodgkin’s lymphoma (Haem/Hepa)).The possibility that the

See Figs. 6 and 7; Tables 3, 4 and 5.

Fig. 6 French death certificate

Fig. 7 Italian death certificate

bronchus & lung

Table 5 Groups of causes of death and abbreviations

1 INF Infectious and parasitic diseases

Group # Abb. Groups and subgroups ICD-10 code

4 ENDOC Endocrine, nutritional and metabolic

Group # Abb. Groups and subgroups ICD-10 code

9 DIGES Diseases of the digestive system

Nam, C. B. (1986). Mortality differentials from a multiple cause-of-death perspective. Committee on

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