Burden of cancer in Serbia.

Abstract

To provide a comprehensive assessment of burden of selected cancers in Serbia.
We calculated disability adjusted life years (DALY)-- the sum of the years of life lost (YLL) from premature mortality and the years lived with disability (YLD)--for cancers of stomach, colon and rectum, lung, breast, and cervical cancer for central Serbia and Vojvodina, Serbia and Montenegro. The obtained values were compared with the corresponding values for European region as estimated by the World Health Organization. The study was conducted between October 2002 and September 2003. The cancer burden was estimated for the year 2000.
Observed cancers were responsible for 133,689 DALYs (73,197 for men and 60,482 for women). There were significantly more losses because of premature death than disease disability (95.2% vs 4.8% in men P<0.001, and 93.2% vs 6.8% in females, P<0.001). The cancer burden was dominated by lung cancer in men and breast cancer in women. The cancer burden was very small before the age of 35.
DALYs per 1000 population were higher in Serbia than in the European region for all observed cancers except for stomach cancer. The participation of a burden caused by disability in the total burden of selected cancers was lower in Serbia than in other European countries, with the greatest differences in colorectal, breast, and cervical cancers.

Full text

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Burden of Cancer in Serbia
Aim To provide a comprehensive assessment of burden of
selected cancers in Serbia.
Method We calculated disability adjusted life years (DALY)
– the sum of the years of life lost (YLL) from premature
mortality and the years lived with disability (YLD) – for
cancers of stomach, colon and rectum, lung, breast, and
cervical cancer for central Serbia and Vojvodina, Serbia and
Montenegro. The obtained values were compared with the
corresponding values for European region as estimated by
the World Health Organization. The study was conducted
between October 2002 and September 2003. The cancer
burden was estimated for the year 2000.
Results Observed cancers were responsible for 133 689
DALYs (73 197 for men and 60 482 for women). There
were significantly more losses because of premature death
than disease disability (95.2% vs 4.8% in men P<0.001, and
93.2% vs 6.8% in females, P<0.001). The cancer burden was
dominated by lung cancer in men and breast cancer in wom-
en. The cancer burden was very small before the age of 35.
Conclusion DALYs per 1000 population were higher in
Serbia than in the European region for all observed cancers
except for stomach cancer. The participation of a burden
caused by disability in the total burden of selected cancers
was lower in Serbia than in other European countries, with
the greatest differences in colorectal, breast, and cervical
cancers.
Hristina Vlajinac
Institute of Epidemiology
School of Medicine, University of Belgrade
Višegradska 26
11000 Belgrade, Serbia and Montenegro
kristiv@eunet.yu
> Received: April 27, 2005
> Accepted: October 5, 2005
1Institute of Epidemiology, Belgrade University
School of Medicine, Belgrade, Serbia and
Montenegro
2Institute for Medical Statistics and
Informatics, Belgrade University School of
Medicine, Belgrade, Serbia and Montenegro
3Institute of Social Medicine, Belgrade
University School of Medicine, Belgrade,
Serbia and Montenegro
Public Health
> Croat Med J. 2006;47:134-41
Hristina Vlajinac1, Sandra Šipetić-Grujičić1, Slavenka Janković1, Jelena
Marinković2, Nikola Kocev2, Ljiljana Marković-Denić1, Vesna Bjegović3
> Correspondence to:
134
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Vlajinac et al: Cancer Burden in Serbia
There is growing literature on the use of sum-
mary measures of population health, which com-
bine the information on mortality and non-fatal
health outcomes (1,2). One of them, called disabil-
ity-adjusted life years (DALY) was introduced by
the World Bank (3) and subsequently used by the
World Health Organization and Harvard Uni-
versity for detailed assessment of global burden of
disease and injuries (4). Afterwards, many inves-
tigators have performed and published studies on
burden of diseases and injuries using DALY, which
reflect both the years of life lost because of prema-
ture death and years lived with disability (5-7).
Morbidity and mortality of cancers have a
great impact on population of Serbia. During
many decades, malignant neoplasms have occu-
pied the second place as a cause of death, with
mortality rates for some cancers showing a slow
but steady increase (8,9). In 2000, cancer account-
ed for 19% of all causes of deaths (21% in men,
and 17% in women) in the population of Serbia
without Kosovo and Metohia. In 2000, stomach
cancer (International Classification of Diseases,
version 10 [ICD10], code C16), colorectal cancer
(ICD10 codes C18 – C21), lung cancer (ICD10
codes C33 – C34), breast cancer (ICD10 code
C50), and cervical cancer (ICD10 code C53)
were responsible for 50% of all cancer incidence
cases (45% in men and 54% in women) and for
65% of deaths caused by all malignant neoplasms
(63% in men, and 66% in women) (10). Lung
cancer, colorectal cancer, and stomach cancer
were among ten leading causes of deaths in men,
whereas breast cancer, colorectal cancer, lung
cancer, stomach cancer, and cervical cancer were
among twelve leading causes of death in women
(11). We chose these cancers to provide a com-
prehensive assessment of premature mortality
and disability attributable to cancers in Serbia by
calculating disability adjusted life years (DALY).
Method
The Serbian Burden of Disease Study was
carried out by the European Agency for Recon-
struction Project Team, using methods largely
based on those developed for the Global Burden
of Disease study (4). The project commenced in
October 2002 and was completed in September
2003. The study was conducted in Central Ser-
bia and Vojvodina, Serbia and Montenegro.
The burden of selected cancers was estimat-
ed for the year 2000 by the use of DALY, which
combines a measurement of premature mortality
and disability (12-15). This indicator is the aggre-
gation of years of life lost (YLL) and years lived
with disability (YLD) at the population level and
thus reflects the “burden of disease” in a popula-
tion (DALY = YLL + YLD).
Population data
The population estimates for the calcula-
tion of values of needed indicators were based
on the census adjustments for 2000, not in-
cluding the migration component (16). The
total number of observed population was
7 551 000. Direct method, with the European
population as the standard, was used for stan-
dardization (17).
Mortality data
The Regional Offices of Statistics compile in-
formation on death certificates. The Serbian Of-
fice of Statistics receives these data from each
region and provides a unit record file of deaths
with diagnosis, death date, age, sex, and place of
residence. For the burden of disease estimates, we
considered all deaths of people with place of resi-
dence in Serbia that occurred anywhere in or out
of Serbia and were registered in 2000.
The completeness of Serbian Office of Sta-
tistics 2000 mortality database was 98%. In ad-
dition to missing data, two other problems with
the validity and reliability of cause of death data
were present: not assigning a specific code but us-
ing “senility” or some other ill-defined code, and
assigning the wrong code due to diagnostic fash-
ion or carelessness.

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Croat Med J 2006;47:134-141
136
According to the Global Burden of Disease
methodology, ill-defined causes of deaths were
reassigned. The 8.7% of deaths assigned to ill-de-
fined and senility codes (U161) were redistrib-
uted proportionally, by sex and age, across the
group of communicable, maternal, perinatal, and
nutritional conditions among those 0-5 years
old, and across the group of non-communicable
diseases among those >5 years old. Cancers of
unspecified sites (U077), which made 3.4% of all
deaths, were redistributed proportionally by age
and sex across all specified sites. Finally, 0.1% of
deaths with missing age data were redistributed
proportionally by sex and cause.
YLL was determined by the average life ex-
pectancy at the age of death while discounting
future years by 3%. The 3% discount rate, rec-
ommended by the International Panel on Cost
Effectiveness in Health and Medicine (18), was
chosen to allow for international comparisons.
YLL were calculated by multiplying age-specific
mortality rates by age-specific standard expected
for YLL and population numbers. Standard ex-
pected YLL were derived from the standard life
table West 26 (19) with a life expectancy at birth
of 82.5 years for women. Life table West 25 (20)
for women was used for men with life expectancy
at birth of 80 years.
The Global Burden of Disease Study weight-
ed a year of healthy life lived at young age and
older age lower than for other ages, because there
is a broad social preference to value a year lived by
a young adult more highly than a year lived by a
young child or at older ages (4). Although not all
investigators agree that young age and older age
should be given less weight, in Serbian Burden of
Disease Study 2000, we decided to use this ap-
proach to be able to compare our results with the
results of other studies.
Incidence data
YLD was calculated on the basis of inci-
dence data. The incidence data were obtained
from the Cancer Registry of central Serbia for
1999 (10) and from Cancer Registry of Vojvodi-
na for 1998 (21). From data for Central Serbia,
only those for Belgrade population were used be-
cause they were more reliable than the data for
the rest of the region. Global Burden of Disease
(22), Dutch study (23) models, and provisional
disability weights for cancer stages were used for
all cancers. Since Dutch weights do not exist for
cervical cancer, we applied weights used in Victo-
ria study (24).
It was accepted that, according to the Global
Burden of Disease estimate, 20% of cancers were
untreated in the region of the former socialist
economies of Europe (4).
For all cancers observed, including breast
cancer, we assumed patients who survived five
years to be in remission and we took the five-year
survival rate as the cure rate. Patients who were
cured were assumed to be without disability (22).
For patients who died, average time to death was
assumed to follow an exponential distribution,
so that the mean survival time was estimated by
fitting this distribution to available survival data
(after 1, 3, and 5 years) by Kaplan-Meier product
limit method (24,25). The duration of primary
diagnosis, therapy, remission, and preterminal
phase of each cancer were discussed with experts.
The experts’ opinion was also asked for the fre-
quency of small cell and non-small cell lung can-
cer, both operable and inoperable ones, and for
the incidence of breast cancer by size. Since there
are no data on survival of cancer patients in Ser-
bia, we used 5-year survival data for Slovenia in
the period 1985-1989 (26). Both Serbia and Slo-
venia had been part of former Yugoslavia before
1991.
Results
The incidence and mortality rates for selected
malignant neoplasms in central Serbia and Vo-
jvodina in 2000 (Table 1) were compared for re-
liability with the same data for Slovenia (27) in
1999 (Table 2). Cancer incidence rates in these

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Vlajinac et al: Cancer Burden in Serbia
two populations were similar, although the fre-
quency of lung cancer and cervical cancer was
higher in Serbia, and the frequency of stomach
and colorectal cancers was higher in male popu-
lation of Slovenia. The incidence was almost the
same for breast cancer. Mortality rates of stom-
ach and colorectal cancers were similar, but mor-
tality rates for lung, breast, and cervical cancers
were higher in Serbia.
Observed cancers were responsible for 73 197
DALYs in men and for 60 482 DALYs in wom-
en. There were significantly more YLL than YLD
losses for all cancers (95.2% vs 4.8% in men, and
93.2% vs 6.8% in women), showing that the bur-
den of cancer was dominated by mortality rather
than long-term disability (Table 3).
Lung cancer accounted for the largest part of
the cancer burden in men, followed by colorec-
tal and stomach cancers, whereas the burden of
breast cancer was negligible. For women, the bur-
den of breast cancer was the greatest, followed by
lung cancer, colorectal cancer, cervical cancer,
and stomach cancer (Table 3).
The cancer burden was very small before the
age of 35 (Figure 1). The DALY rates per 1000
male population were the highest in the 55-74
age group for lung cancer and in the 65-74 age
group for stomach and colorectal cancer. For
women, DALY rates were the highest in the 55-
74 age group for lung cancer, and in those aged
≥65 years for stomach and colorectal cancers.
The burden of breast and cervical cancers was
greater in younger age groups, ie, those aged 45-
64 years and 45-54 years, respectively.
We compared the incidence, YLD, and
DALY per 1000 population, as well as YLD/
DALY ratio (%) of selected cancers in Serbia and
European region divided in European subregions
A, B, and C (Table 4). The incidence of breast
Table 2. Incidence and mortality rates from selected cancers by
sex in Slovenia, 1999*
Crude rate (standardized†) per 1000 population
incidence‡
mortality
Cancer site
Stomach
Colorectal
Lung
Breast
Cervical
All cancers
menwomen menwomen
0.16 (0.11)
0.29 (0.20)
0.22 (0.16)
0.32 (0.35) 0.16 (0.12) 0.25 (0.28)
0.59 (0.63) 0.42 (0.32) 0.35 (0.38)
0.85 (0.86) 0.21 (0.17) 0.78 (0.80)
0.01 (0.01) 0.98 (0.83) 0.003 (0.003) 0.39 (0.31)
– 0.20 (0.18)
4.58 (4.77) 4.15 (3.34) 2.77 (2.95)
– 0.05 (0.04)
2.08 (1.56)
*Population of Slovenia: men – 960 456, women – 1 021 289.
†According to European population (17).
‡According to Cancer Register of Slovenia (27).
Table 1. Incidence and mortality rates from selected cancers by
sex in Serbia, 2000*
Crude rate (standardized†) per 1000 population
incidence‡
men women
0.28 (0.24)0.14 (0.10)
0.57 (0.49)0.42 (0.32)
mortality
Cancer site
Stomach
Colorectal
men women
0.30 (0.25) 0.16 (0.12)
0.45 (0.38) 0.31 (0.22)
Lung 1.26 (0.95)0.29 (0.23) 1.18 (0.99) 0.30 (0.22)
Breast
Cervical
All cancers
0.02 (0.02)
–
4.70 (4.11)
1.02 (0.83)
0.33 (0.29)
4.08 (3.24)
0.01 (0.01) 0.50 (0.40)
–
3.06 (2.63) 2.15 (1.62)
0.16 (0.12)
*Population of Serbia: men – 3 673 529, women – 3 877 326.
†According to European population (17).
‡According to data for Belgrade, 2000 (10), and Vojvodina, 1998 (21).
Table 3. Burden of selected cancers by site and sex in Serbia, 2000*
Measures of population health
YLL YLL per 1000Cancer site
Men:
stomach cancer
colorectal cancer
lung cancer
breast cancer
total
Women:
stomach cancer
colorectal cancer
lung cancer
breast cancer
cervical cancer
total
*Abbreviations: YLD – years lived with disability, estimated by use of Global Burden of Disease (GBD) weights (22); YLL – years of life lost; DALY – disability-adjusted
life years.
YLDYLD per 1000 DALY DALY per 1000
386
983
2136
56
3561
0.10
0.27
0.58
0.02
0.97
10 416
14 542
44 407
271
69 636
2.84
3.96
12.09
0.07
18.96
10 416
15 525
46 543
327
73 197
2.94
4.23
12.67
0.09
19.93
198
802
518
2078
529
4125
0.05
0.21
0.13
0.54
0.14
1.06
5487
9680
12 027
21 463
7701
56 358
1.42
2.49
3.10
5.54
1.99
14.54
5685
10 482
12 545
23 541
8230
60 483
1.47
2.70
3.24
6.07
2.12
15.60

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Croat Med J 2006;47:134-141
138
cancer in Serbia was almost the same as that in
the European region. The incidence of stom-
ach and colorectal cancers was lower and the in-
cidence of lung and cervical cancers was higher
in Serbia. The most pronounced difference was
found in the incidence of cervical cancer, which
was 2.5 times higher in Serbia than in the Euro-
pean region. DALY per 1000 population in Ser-
bia was higher than in the European region for all
observed cancers, except for stomach cancer. The
differences between Serbia and the European
region in participation of YLD and YLL in the
total burden (DALY) were presented through
YLD/DALY ratio. The proportion of YLD in
DALY for stomach and lung cancers in Serbia
was similar to that estimated for the European
region. For colorectal, breast, and cervical can-
cer, the proportion of YLD in DALY was small-
er even in comparison to European B and Euro-
pean C regions.
The burden of the same cancers was also esti-
mated by Dutch weights used for calculation of
Table 5. The burden of cancers by site in the population of Serbia and selected countries, 2000
YLD* per 1000
Cancer siteYLD crude standardized§DALY
Stomach 12460.170.14
Colorectal 29450.39 0.32
Lung 4192 0.550.52
Breast 50860.670.59
Cervical11210.15 0.14
*YLD – years lived with disability; Dutch weights used for estimation of YLD (23,24).
†DALY – disability-adjusted life years.
‡Victoria (24), New Zealand (28), the Netherlands (29,30).
§Standardized according to European population (17).
DALY† per 1000
crudestandardized§
2.27
3.60
8.03
3.55
1.17
YLD/DALY (%)‡
New Zealand
not available
18.0
7.0
26.0
not available
Serbia
7.0
11.0
7.0
19.0
13.0
Victoria
10.0
20.0
9.0
28.0
19.0
The Netherlands
not available
not available
6.5
27.0
not available
17 149
27 167
60 626
26 820
8822
1.92
2.97
7.89
3.10
1.06
Table 4. Incidence, years lived with disability (YLD)*, disability-adjusted life years (DALY) per 1000 population (all persons), and YLD/
DALY ratio from selected cancers in Serbia and European region
Region†
Cancer site
Stomach cancer:
incidence
YLD
DALY
YLD/DALY (%)
Colorectal cancer:
incidence
YLD
DALY
YLD/DALY (%)
Lung cancer:
incidence
YLD
DALY
YLD/DALY (%)
Breast cancer:
incidence
YLD
DALY
YLD/DALY (%)
Cervical cancer:
incidence
YLD
DALY
YLD/DALY (%)
*Years lived with disability, estimated by use of Global Burden of Disease (GBD) weights (22).
†European region (22): European region A (very low child, very low adult mortality) – Andorra, Austria, Croatia, Czech Republic, Denmark, Finland, France, Germany,
Greece, Iceland, Ireland, Israel, Italy, Luxemburg, Malta, Monaco, Netherlands, Norway, Portugal, San Marino, Slovenia, Spain, Sweden, Switzerland, United King-
dom; European region B (low child, low adult mortality): B1 – Albania, Bosnia and Herzegovina, Bulgaria, Georgia, Poland, Romania, Slovakia, The Former Yugoslav
Republic of Macedonia, Turkey, Serbia and Montenegro; B2 – Armenia, Azerbaijan, Kyrgyzstan, Tajikistan, Turkmenistan, Uzbekistan; European region C (low child,
high adult mortality) – Belarus, Estonia, Hungary, Kazakhstan, Latvia, Lithuania, Republic of Moldavia, Russian Federation, Ukraine.
‡Standardized according to European population (17).
SerbiaEuropeanEuropean A European BEuropean C
0.16‡
0.06‡
1.84‡
3.0
0.25
0.06
1.83
3.0
–
0.06
1.15
5.0
–
0.04
1.48
3.0
–
0.09
3.29
3.0
0.39‡
0.20‡
2.85‡
7.0
0.43
0.27
2.14
13.0
–
0.50
2.63
19.0
–
0.12
1.30
9.0
–
0.20
2.49
8.0
0.62‡
0.29‡
6.66‡
4.0
0.46
0.12
3.75
3.0
–
0.14
4.04
3.0
–
0.08
2.76
3.0
–
0.11
4.49
2.0
0.45‡
0.25‡
2.76‡
9.0
0.42
0.36
2.14
17.0
–
0.50
2.46
20.0
–
0.18
1.36
13.0
–
0.27
2.29
12.0
0.15‡
0.06‡
0.98‡
6.0
0.06
0.05
0.46
11.0
–
0.03
0.26
12.0
–
0.05
0.67
7.0
–
0.06
0.69
9.0

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Vlajinac et al: Cancer Burden in Serbia
YLD (Table 5). Since Dutch weights were much
higher, the values of YLD and DALY were also
higher than those obtained by Global Burden
of Disease study weights. The same was true for
YLD/DALY ratios. Participation of YLD in
DALY for lung cancer in Serbia was similar to
that found in Victoria study (24), but YLD/
DALY ratio for stomach, colorectal, breast, and
cervical cancers in Serbia was lower.
Discussion
The total burden of lung, stomach, colorec-
tal, breast, and cervical cancers in Serbia in 2000
amounted to 133 689 DALYs. There were sig-
nificantly more losses on account of premature
death than disease-related disability. The partici-
pation of a burden caused by disease-related dis-
ability in the total burden of selected cancers was
lower in Serbia than in other European coun-
tries, with the greatest differences being found
for colorectal, breast, and cervical cancers.
Although we considered our mortality data
reliable, percentage of deaths assigned to ill-de-
fined codes was not small. However, we could
expect that among ill-defined causes of deaths,
cardiovascular diseases were more frequent than
malignant diseases.
On the basis of comparison with cancer in-
cidence in Slovenia (27), we assumed that data
from the Cancer Register for Belgrade and for
Vojvodina were reliable enough to estimate can-
cer incidence in Serbia. Slovenia was chosen for
comparison for several reasons. Serbia and Slo-
venia had been part of former Yugoslavia before
1991, the health service in Slovenia was close-
ly related to that in Serbia, and Cancer Registry
in Slovenia was one of the oldest services of this
type in Europe (26). With some exceptions, in-
cidence rates of observed cancers were similar in
these two populations. Higher incidence rates of
lung and cervical cancers in Serbia were expect-
ed, because smoking rate is one of the highest in
Europe and screening for cervical cancer has not
been established yet.
Method used for estimation of DALY was
largely based on the one developed for the Glob-
al Burden of Disease study (4). After discussion
with experts for selected cancers, the Global Bur-
den of Disease model and provisional disabili-
ty weights for cancer stages were used (22). The
estimation of YLD by Dutch disease model and
disability weights (23) was also performed to al-
low for comparison with other population data
analyzed by the same method. As expected, how-
ever, we obtained similar information from these
two models, at least when the burden of cancer
is concerned. Only the participation of YLD in
DALY was higher when Dutch weights were ap-
plied. In Australian Burden of Disease study (5),
the two sets of weights were used concurrent-
ly because there was a high correlation between
them for 54 conditions, indicating that the two
sets of weights valued the same conditions simi-
larly. Although it is possible to create own disease
model and to estimate own disability weights, in
Figure 1. The burden of cancer by site, sex and age in Serbia,
2000. Triangles – stomach cancer; open circles – colorectal can-
cer; rhombs – cervical cancer; squares – breast cancer; closed
circles – lung cancer.

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Croat Med J 2006;47:134-141
140
our opinion, the same disease model and disabil-
ity weights should be used in all studies to make
comparison between populations possible. Since
we had no reliable data about treated and non-
treated cases, we accepted that, according to the
Global Burden of Disease estimate, 20% of the
cancer cases were untreated (4).
We used 5-year survival data for Slovenia
from 1985 to 1989 (26) because it was more ap-
propriate than to use data on some other neigh-
boring country or Europe as a whole. The reason
was that in Serbia we could not expect positive
changes in survival during the preceding 10 years,
ie, in the period 1991-2000. The civil strife in
1991, which led to the war and the break-up of
the former Yugoslavia, United Nation’s econom-
ic sanctions imposed on Serbia and Montenegro,
and the ensuing economic crisis had a highly ad-
verse effect on the population health and the
quality of health care (31).
We may conclude that DALYs, used as the
summary measure of population health in the
present study, can be considered a good esti-
mate of cancer burden in Serbia. The differenc-
es in cancer burden and especially the differences
in YLD/DALY ratio between Serbia and Euro-
pean region, and between Serbia and Victoria,
New Zealand, and the Netherlands, could be ex-
plained by higher incidence and/or higher fatal-
ity of almost all observed cancers in Serbia. Ear-
ly diagnosis and early and adequate therapy of
lung cancer and to a less extent of stomach can-
cer do not influence significantly their progno-
sis. That is why YLD/DALY ratio for these can-
cers is similar both in the developed and in the
developing countries. On the other hand, ear-
ly diagnosis and therapy of cervical, breast, and
colorectal cancers have considerable influence on
their outcome. Consequently, the participation
of YLD in DALY is lower in countries like Ser-
bia, in which regular screening for these cancers
has not been organized yet, than in countries in
which early detection was established years ago.
It should be also mentioned that YLD/DALY
ratio can be affected by age distribution of the
diseased – the participation of YLL in DALY is
greater when fatal disease occurs in younger age
groups.
The most important advantage from a policy
perspective of the approach taken in this study is
that estimates of burden of cancers are expressed
in terms of a summary health-outcome measure,
which combines mortality and morbidity. These
estimates should guide future health strategies
and interventions and would allow for monitor-
ing of the improvements in health and the per-
formance of the health care system. However,
there are views that burden of disease assessment
should be supplemented with positive measures
of health expectancy or health adjusted life ex-
pectancy (HALE). According to Tobias (28),
these two families of summary measures of popu-
lation health could be measured in such a way to
make them not only conceptually, but also quan-
titatively complementary. In any case, the esti-
mate of disability adjusted life years for selected
cancers should be repeated after several years in
order to assess the effects of preventive strategies,
which are in the process of implementation.
Acknowledgment
This work was supported by European Agency for
Reconstruction (EAR), 2002-2003, and by the Ministry
of Science and Ecology of Serbia, contract No. 101927,
2002-2005.
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