Lung cancer mortality: Comparing Sweden with other countries in the European Union

Abstract

To describe how snus use has reduced smoking among men in Sweden, and to estimate how smoking-attributable lung cancer mortality would decline in other European Union countries if they had the smoking prevalence of Sweden.
Lung cancer mortality rates (LCMRs) and numbers of deaths among men and women age 45+ years in 25 EU countries in 2002 were obtained from the World Health Organization mortality database, and the number of lung cancer deaths expected in each country at the LCMR of Sweden was calculated. LCMRs for EU countries were obtained during the period 1950-2004, and per capita consumption of nicotine from cigarettes and snus was estimated for men in Sweden from 1931 to 2004.
There were 172,000 lung cancer deaths among men in the EU in 2002. If all EU countries had the LCMR of men in Sweden, there would have been 92,000 (54%) fewer deaths. In contrast, the LCMR among Swedish women was the sixth highest in the EU; at the Swedish rate, deaths among EU women would have increased by 14,500 (26%). These LCMR patterns were in place for most of the last 50 years, and LCMRs among Swedish men can be correlated with snus and cigarette consumption.
This study shows that snus use has had a profound effect on smoking prevalence and LCMRs among Swedish men. While it cannot be proven that snus would have the same effect in other EU countries, the potential reduction in smoking-attributable deaths is considerable.

Full text

Scandinavian Journal of Public Health, 2009; 37: 481–486
ORIGINAL ARTICLE
Lung cancer mortality: Comparing Sweden with other countries
in the European Union
BRAD RODU
1
& PHILIP COLE
2
1
School of Medicine, University of Louisville, Louisville, KY, USA and
2
School of Public Health, University of Alabama at Birmingham, Birmingham, AL, USA
Abstract
Aims: To describe how snus use has reduced smoking among men in Sweden, and to estimate how smoking-attributable lung
cancer mortality would decline in other European Union countries if they had the smoking prevalence of Sweden. Methods:
Lung cancer mortality rates (LCMRs) and numbers of deaths among men and women age 45þyears in 25 EU countries in
2002 were obtained from the World Health Organization mortality database, and the number of lung cancer deaths expected
in each country at the LCMR of Sweden was calculated. LCMRs for EU countries were obtained during the period 1950–
2004, and per capita consumption of nicotine from cigarettes and snus was estimated for men in Sweden from 1931 to 2004.
Results: There were 172,000 lung cancer deaths among men in the EU in 2002. If all EU countries had the LCMR of men in
Sweden, there would have been 92,000 (54%) fewer deaths. In contrast, the LCMR among Swedish women was the sixth
highest in the EU; at the Swedish rate, deaths among EU women would have increased by 14,500 (26%). These LCMR
patterns were in place for most of the last 50 years, and LCMRs among Swedish men can be correlated with snus and
cigarette consumption. Conclusions: This study shows that snus use has had a profound effect on smoking
prevalence and LCMRs among Swedish men. While it cannot be proven that snus would have the same effect in
other EU countries, the potential reduction in smoking-attributable deaths is considerable.
Key Words: Cigarette smoking, European Union, lung cancer mortality, snus, Sweden
Background and Aims
For more than two centuries men in Sweden and
other Scandinavian countries have used snus, which
consists of ground tobacco, salt, water and flavouring
agents that undergoes heat treatment to prevent
formation of unwanted contaminants [1]. Snus,
available in loose form and more recently in small
pouches, is placed inside the upper lip.
Several studies have shown that the use of snus has
played a substantial role in the low smoking rate
among Swedish men [2–5]. However, that explana-
tion has been judged as not compelling by some
authorities, such as the European Commission’s
Scientific Committee on Emerging and Newly
Identified Health Risks (SCENIHR). Recently, a
SCENIHR report acknowledged that ‘‘particularly in
Swedish men, there is a clear trend over recent
decades for smoking prevalence to decrease and for
use of oral tobacco (snus) to increase,’’ but it
concluded that ‘‘these trends could also be due to
successful smoking reduction programs or other
socio-cultural factors, and it is therefore not clear
whether or by how much the availability of snus has
influenced smoking prevalence.’’ [1] The report also
stated that ‘‘it is not possible to extrapolate the trends
in prevalence of smoking and use of oral tobacco if it
were made available in a European Union (EU)
country where it is now unavailable.’’
The purpose of this study is to clarify how much
the availability of snus has influenced smoking among
men in Sweden, in the context of all other EU
countries. Studying smoking prevalence per se in the
EU is difficult because standardized and comparable
data are not available for all 27 countries. But there is
Correspondence: Brad Rodu, 529 South Jackson Street, School of Medicine, University of Louisville, Louisville, KY 40202, USA. Tel: þ01-502-561-7273.
Fax: þ01-502-561-7280. E-mail: brad.rodu@louisville.edu
(Accepted 26 March 2009)
ß2009 the Nordic Societies of Public Health
DOI: 10.1177/1403494809105797
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a measure that reflects differences in smoking among
EU countries: lung cancer mortality. Lung cancer is
the sentinel disease of smoking [6], and a country’s
lung cancer mortality rate (LCMR) in any single year
provides a reasonable indication of the amount
of smoking in that country about 20 years earlier.
While it is not possible to predict to what extent the
availability of snus would reduce smoking prevalence
in EU countries other than Sweden, it is possible to
estimate how smoking-attributable mortality would
decline if these countries had the smoking prevalence
of Sweden.
Methods
LCMRs and numbers of deaths were obtained sep-
arately for men and women age 45þyears in 25 EU
countries in 2002 (Denmark, 2001) from the World
Health Organization (WHO) mortality database [7].
No data are available for Cyprus and the latest data
for Belgium are from 1997. LCMRs were age-
adjusted by the WHO to the World Standard
Population and were expressed as deaths per
100,000 person-years. We calculated rate ratios for
each country, expressed as that country’s LCMR
divided by the Swedish LCMR. A rate ratio greater
than one indicates that the country’s LCMR is higher
than that of Sweden; a ratio less than one indicates
that the Swedish rate is higher. For both genders we
calculated the number of lung cancer deaths
expected if each country had the LCMR of Sweden.
LCMRs for EU countries except Cyprus were
obtained for all available years during the period
1950–2004. Based on data availability and general
LCMR trends, the countries were divided into two
groups: the 15 countries comprising the EU in 1995
(EU-1995 countries) and the 11 countries that joined
the EU in either 2004 or 2007 (EU-expansion
countries). Countries with similar LCMRs were
combined, and data are illustrated as three-year
moving averages.
We estimated the annual per capita consumption
of nicotine from cigarettes and snus by men in
Sweden from 1931 to 2004. Annual population
estimates (men and women aged 15þyears) and
annual Swedish tobacco consumption (number of
cigarettes and the amount of snus in grams) were
obtained from Research and Consulting Bureau
VECA (Ha¨sselby, Sweden). It was assumed that all
snus consumption was by men. Cigarette consump-
tion by men in each year was estimated by adjusting
total consumption using gender-specific LCMRs 20
years later. LCMR trends were projected to 2024
to estimate gender-specific cigarette consumption
through 2004. We estimated per capita nicotine
consumption using conversions developed by
Fagerstro¨m [8], 1.4 mg of nicotine per cigarette
and 2.0 mg per g of snus. The snus conversion applies
to traditional snus, which provides more nicotine
than portion-pack forms that became popular
recently [8].
Results
LCMRs among men in the EU
In 2002 the LCMR among men in the 25 EU
countries was 166 (Table I). The LCMR among
men in Sweden was 77, the lowest of all countries.
The LCMR among Portuguese men (105), the
second lowest in the EU, was 36% higher than that
of Sweden, and 17 EU countries had LCMRs
that were over twice as large as that of Sweden. The
number of lung cancer deaths among all men in the
EU was 172,000. If all countries had the LCMR of
Swedish men, 80,000 deaths would have occurred,
representing 92,000 fewer lives lost to lung cancer,
a 54% reduction.
Figure 1a shows the LCMRs among men in
Sweden and among men in other EU-1995 countries
from 1950 to 2004. The LCMR among men in
Sweden was 32 in 1951 and peaked in 1978 at 96,
followed by a gradual decline to 77 in 2002. These
LCMRs were much lower for all years than those for
all but one EU-1995 country. The exception is
Portugal, which had an LCMR of 26 in 1955 and
has experienced a gradual increase ever since, passing
Sweden in 1986. Spain, Italy, France, Ireland,
Denmark and Greece also had low LCMRs initially
(31–64 in 1952), with subsequent peaks between 180
and 220. Data are available for Germany starting in
1973, and the LCMR pattern is consistent with the
overall pattern for this group. Belgium and the
Netherlands had LCMRs of about 100 in the mid-
1950s, with subsequent peaks near 300 in the early to
mid-1980s. Finland and the United Kingdom (UK)
had LCMRs above 150 in 1952, with subsequent
peaks in the early 1970s at 261 and 281 respectively.
No data are available prior to 1973 for Luxembourg,
which had a peak LCMR of 273 in 1982. Austria had
an LCMR similar to Finland in 1955, but its peak at
196 occurred in 1968. Despite the different LCMR
patterns among these countries, there was a conver-
gence of the rates over the last 20 years. By 2002 the
range of LCMRs was from 120 (Finland) to 188 (the
Netherlands) in all countries except Sweden and
Portugal.
Figure 1b shows LCMRs among men in Sweden
compared with those in EU-expansion countries.
482 B. Rodu & P. Cole
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Data from these countries is more limited, but some
trends are apparent. Swedish LCMRs are much
lower than those for all other countries for all years.
Among countries with data from at least 1960,
Romania had an LCMR of 68 in 1959, with a
pattern similar to that in Spain. LCMRs in Poland
and Hungary in 1960 were 62 and 109, with subse-
quent peaks at 269 (1994) and 306 (1996) respec-
tively. By 2002 LCMRs were declining in all of these
countries except Romania and Bulgaria. However, in
2002 only Romania, Bulgaria and Malta had LCMRs
that were lower than 188, the highest LCMR among
EU-1995 countries in that year.
LCMRs among women in the EU
In 2002 the LCMR among women in the 25 EU
countries was 41. The LCMR among women in
Sweden was relatively high at 52; only Denmark,
Hungary, Ireland, the Netherlands and the UK had
higher rates. In 2002, the number of lung cancer
deaths among women in the EU was 55,800.
If women of all countries had the LCMR of
Swedish women, 70,300 lung cancer deaths would
have occurred, a 26% increase.
LCMRs among women in EU-1995 countries
during the period from 1950 to 2004 are shown in
Figure 2a. In the mid-1950s LCMRs ranged from
7 in Portugal to 23 in the UK. Denmark showed the
sharpest increase to a peak of 104 in 1995, with
little decline afterward. Ireland and the UK peaked
at 75–79 in 1988–89, followed by modest declines
to about 70. A peak has not occurred in any
other country, although there are five separate
slopes. The Netherlands’ LCMR was at the level
of that in Ireland and the UK in 2002, while
Sweden had an LCMR of 52, which is fifth highest
in this group. In 2004 Austria, Germany and
Luxembourg had LCMRs around 40; France,
Finland, Greece and Italy had LCMRs of 30;
Portugal and Spain were the lowest among
EU-1995 countries at 20.
Table I. Lung cancer mortality rates.
a
Number of deaths observed and number expected at Swedish rates among men and women in
25 European countries, 2002.
Men Women
Country Rate
a
Observed
deaths
Rate
ratio
b
Expected
deaths
c
Rate
a
Observed
deaths
Rate
ratio
b
Expected
deaths
c
Austria 138 2,354 1.79 1,313 44 1,002 0.84 1,194
Bulgaria 144 2,388 1.86 1,282 23 500 0.43 1,152
Czech Rep 217 4,242 2.80 1,511 46 1,258 0.87 1,440
Denmark 160 1,938 2.07 934 106 1,467 2.02 727
Estonia 227 551 2.95 187 28 122 0.54 227
Finland 120 1,376 1.55 887 30 462 0.58 803
France 163 20,315 2.12 9,586 29 4,646 0.55 8,437
Germany 148 28,320 1.91 14,793 41 10,077 0.78 12,981
Greece 175 4,715 2.26 2,082 26 858 0.50 1,706
Hungary 287 5,506 3.72 1,482 78 2,169 1.50 1,447
Ireland 135 920 1.75 525 63 533 1.21 442
Italy 170 25,492 2.20 11,582 32 6,344 0.61 10,336
Latvia 214 878 2.78 316 23 176 0.44 398
Lithuania 206 1,198 2.68 448 17 179 0.32 561
Luxembourg 164 145 2.13 68 31 33 0.59 56
Malta 158 122 2.04 60 18 13 0.35 38
Netherlands 188 6,321 2.43 2,599 66 2,425 1.25 1,933
Poland 260 16,426 3.37 4,880 50 4,393 0.96 4,586
Portugal 105 2,370 1.36 1,742 19 552 0.36 1,552
Romania 173 6,814 2.25 3,032 28 1,442 0.53 2,723
Slovakia 199 1,661 2.57 645 26 318 0.50 630
Slovenia 183 701 2.38 295 44 226 0.83 272
Spain 168 15,605 2.18 7,153 17 1,964 0.33 5,937
Sweden 77 1,761 – 1,761 52 1,329 – 1,329
UK 143 20,124 1.86 10,842 74 13,279 1.42 9,347
All 166 172,243 2.15 80,005 41 55,767 0.79 70,254
a
Deaths per 100,000 person-years, age-adjusted to the World Standard Population.
b
Country rate/Swedish rate.
c
At the Swedish rate. UK ¼United Kingdom.
Lung cancer mortality: Sweden compared with other EU countries 483
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Figure 2b shows LCMRs among women in
Sweden compared with those in EU-expansion
countries. Throughout most of the period LCMRs
among Swedish women were lower than those only in
Hungary, which had a rate of 80 in 2003. LCMRs
in the Czech Republic and Poland approached 50
by 2004, and the LCMR in Slovenia was over 40.
LCMRs increased more slowly in Bulgaria, Romania,
Slovakia, Estonia and Latvia, generally staying in the
mid-20s. LCMRs in Malta and Lithuania were
essentially stable at 20.
Nicotine consumption by Swedish men, 1931–2004
Figure 3 shows estimated annual per capita con-
sumption of nicotine from cigarettes and snus by
Swedish men age 15þyears. Prior to 1952, snus was
the dominant nicotine source but was declining while
cigarette consumption was increasing. Cigarettes
were the preferred nicotine source from 1955 to
1985, but consumption peaked by 1975; the nadir
of snus consumption was in 1969. After 1985 snus
regained dominance, and the snus-cigarette gap has
widened ever since.
Nicotine consumption from snus and cigarettes are
strongly and inversely correlated (correlation coeffi-
cient ¼0.86), but annual per capita nicotine con-
sumption from both sources combined was fairly
stable. The mean for all years was 4,600 mg. Nicotine
consumption fell below 4,000 mg only during World
War II (1942–45). Consumption was above 5,000
from about 1972 to 1988; during this period snus use
increased while cigarette smoking had just started to
decline. These usage patterns accelerated afterwards
with total nicotine consumption remaining above
4,000 mg.
0
50
100
150
200
250
300
350
(a)
(b)
Deaths per 100,000 person-years
SWE
POR
DEN, FRA, GER,
GRE, IRE, ITA, SPA
AUS
BEL, FIN, LUX, NETH, UK
0
50
100
150
200
250
300
350
Deaths per 100,000 person-years
SWE
ROM
BUL, MAL
HUN, POL
CZE
EST, LAT, LIT,
SLOVA, SLOVE
1950
1960
1970
1980
1990
2000
2004
1950
1960
1970
1980
1990
2004
2000
Figure 1. LCMRs among men age 45þyears in Sweden, in
(a) EU-1995, and (b) EU-expansion countries, 1950–2004.
0
20
40
60
80
100
120(a)
(b)
Deaths per 100,000 person-years
DEN
IRE, UK
NETH
SWE
AUS, BEL, GER, LUX
FRA, FIN, GRE, ITA
POR, SPA
0
20
40
60
80
100
120
Deaths per 100,000 person-years
HUN
SWE
CZE, POL
SLOVEBUL, EST, LAT
ROM, SLOVA
LIT, MAL
1950
1960
1970
1980
1990
2000
2004
1950
1960
1970
1980
1990
2000
2004
Figure 2. LCMRs among women age 45þyears in Sweden,
in (a) EU-1995 and (b) EU-expansion countries, 1950–2004.
0
1000
2000
3000
4000
5000
6000
1930
1945
1960
1975
1990
Milligrams
Total
Cigarettes
Snus
Figure 3. Estimated annual per capita nicotine consumption
(mg) from cigarettes and snus by men in Sweden, 1931–2004.
484 B. Rodu & P. Cole
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Discussion
The major finding of this study is that snus use is
inversely correlated with cigarette consumption
among men in Sweden, resulting in the lowest
LCMRs in Europe for most of the past 50 years.
In 2002, there were 172,000 lung cancer deaths
among men in the EU. If all EU countries had the
LCMR of men in Sweden, there would have been
92,000 fewer lung cancer deaths. But the potential
impact of low Swedish smoking rates is not limited to
lung cancer. For men in the EU, 91% of all lung
cancer deaths are attributed to smoking, and lung
cancer accounts for only 31% of all smoking-
attributable deaths [9]. Thus, we estimate that
there were 511,000 smoking-attributable deaths
among men in EU countries in 2002, which is
consistent with other recent estimates [9]. If all EU
countries had the smoking rates of Swedish men,
there would have been only 237,000 deaths from all
smoking-related diseases. In other words, 274,000
smoking-attributable deaths would have been
avoided throughout the EU in 2002. In addition,
longitudinal LCMR trends indicate that the differ-
ence between Swedish men and that of other EU
countries was modest in 2002 compared with previ-
ous years.
The large differences in LCMRs between Sweden
and other EU countries occur only in men. For
most of the last 50 years, the LCMR among Swedish
women was the sixth highest in the EU. This context
is important, because it has been suggested that
vigorous anti-smoking campaigns since the 1970s are
the major determinant of the low Swedish smoking
rates [10]. It is implausible that these campaigns were
highly effective for Swedish men and almost com-
pletely ineffective for Swedish women. The striking
difference in the relative EU ranking of Swedish men
and women is firm evidence that snus use, not anti-
smoking campaigns, has played the primary role in
low LCMR rates among men in Sweden for over a
half century.
World War II created millions of male smokers,
resulting in very high LCMRs throughout Europe in
the 1960s and 1970s. Men in Portugal, Spain and
Italy, which had LCMRs similar to those in Sweden
in the early 1950s, later experienced peak LCMRs
that were four to six times higher, while the peak in
Sweden represented only a three-fold increase. Even
though snus consumption declined until 1969, its use
was high enough to suppress smoking by Swedish
men and to keep their LCMR among the lowest in
the EU. Increasing snus consumption in the last two
decades has been accompanied by further declines
in smoking. If current trends hold, the LCMR
for Swedish men may become lower than that for
Swedish women by 2011. However, there is evidence
that snus has started to become popular among
Swedish women, with a consequential impact on
smoking [3,11].
There are other risk factors for lung cancer besides
smoking, but the latter is certainly the dominant
cause throughout the EU. Furthermore, the propor-
tion of lung cancer cases due to other causes is
unlikely to differ significantly across countries, with
the possible exception of women in Lithuania, Spain
and Portugal, who have extremely low LCMRs [9].
Thus, while the number of lung cancer deaths
reported here are not entirely due to smoking, other
risk factors play a minor role in the trends seen in this
study.
Nicotine consumption from snus and cigarettes are
strongly and inversely correlated. But the LCMR
decline among Swedish men started just 10 years
after the upturn in snus consumption and only six
years after cigarette consumption peaked. The
expected lag is about 20 years. A possible explanation
relates to differences in the available data; we had
information on snus and cigarette consumption
only for all men (age 15þyears), but lung cancer is
mainly seen in persons age 45þyears. In the 1950s
and 1960s snus use was seen predominantly in
older Swedish men [12], which may have influenced
the timing of the LCMR peak and decline in this
study.
Currently, snus is banned in all EU countries
except Sweden. While it cannot be proven that the
availability of snus would reduce smoking prevalence
in other EU countries, this study shows that snus use
has had a profound effect on smoking among
Swedish men. It also reveals that 274,000 smoking-
attributable deaths would be avoided if all men in all
EU countries had the smoking prevalence of men in
Sweden. Britton and Edwards recently wrote that
‘‘the absence of effective harm reduction options for
smokers is perverse, unjust, and acts against the
rights and best interests of smokers and the public
health.’’ [13]. It is time for the European
Commission to revise the Tobacco Directive to
make snus available to all European smokers.
Acknowledgments
This study was supported by unrestricted grants from
smokeless tobacco manufacturers (US Smokeless
Tobacco Company and Swedish Match AB) to the
University of Louisville. The terms of the grants
assure that the sponsors are unaware of this study,
and thus had no scientific input or other influence
Lung cancer mortality: Sweden compared with other EU countries 485
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with respect to its design, analysis, interpretation or
preparation of the manuscript. Neither author has
any financial or other personal relationship with
regard to the sponsors.
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