Download - Cervical Cancer Burden and Prevention Activities in EuropeCervical Cancer Burden and Prevention Activities in Europe Vesna Kesic1, Mario Poljak2, and Svetlana Rogovskaya3 Abstract

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Cervical Cancer Burden and Prevention Activities in Europe

Vesna Kesic1, Mario Poljak2, and Svetlana Rogovskaya3

AbstractCervical cancer is an important public health care problem in Europe. The overall incidence rate of cervical

cancer in Europe is 10.6 per 100,000. However, within Europe, the incidence rates significantly differ, being

lower in Western Europe where prevention programs are better developed. Significantly higher are the

incidence and mortality rates in Central and Eastern Europe, being in close correlation to the intensity of

organized screening. Human papillomavirus (HPV) vaccines are being delivered to the low-incidence

populations that already have extensive screening programs, whereas the high-incidence countries have not

implemented the vaccination programs yet. The resolution of the problem of cervical cancer control in Europe

will be a matter of the implementation of public health care programs across the whole continent. Cancer

Epidemiol Biomarkers Prev; 21(9); 1423–33. �2012 AACR.

IntroductionCervical cancer is generally defined as a disease of

disparity. This is due to marked differences in the inci-dence and mortality of cervical cancer between the devel-oped and developingworld. As a continent, Europe is notan exception. Cervical cancer in Europe is a true exampleof inequality—an almost straight line can be drawn for theincidence and mortality between Western and EasternEurope.Usually,WesternEurope is considered as adevel-oped world. The countries of Eastern Europe (includingCentral European countries) as well as the former SovietUnion countries (including Central Asian countries) arereferred to as "countries in transition" (Table 1). However,most of them in the international reports are still regardedas "developing countries." This article describes cervicalcancer epidemiology and cancer control efforts includingscreening and vaccination in Europe. It compares andcontrasts prevention efforts in different parts of Europe.

Current cervical cancer incidence in EuropeA total of 54,517 new cases of cervical cancer cases and

24,874 deaths were reported in Europe in 2008 (1). Bothincidence and mortality rates, age-standardized to theworld standard million population are generally higherin Central and Eastern Europe and former Soviet Unioncountries than in Western Europe.

The overall incidence rate of cervical cancer in Europe is10.6 per 100,000. The analysis between different parts ofEurope shows more than doubled incidence rates inCentral/Eastern Europe (14.9/100,000) when comparedwith Western Europe (6.9/100,000). Average incidencerates in Northern and Southern Europe are similar (8.4/100,000 and 8.1/100,000, respectively).

The highest incidence rates are currently reported inRomania and FYR Macedonia (23.9/100,000 and 22.0/100,000, respectively; Fig. 1). The lowest rates are observedin Malta (2.1/100,000), Switzerland (4.0/100,000), Greece(4.1/100 000), and Finland (4.5/100,000). Cumulative riskfor getting the disease in Eastern Europe is 4 to 5 timeshigher than in Western and Nordic countries (Table 2).

In 1993, EuropeanUnion (EU)was formally establishedas an economic and political confederation of memberstates. Today, EU consists of 27 sovereignMembers Statesand includes most of Central and Eastern Europeancountries.

Within EU, the incidence rates of cervical cancer aregenerally lower than in the rest of Europe (2). However,the differences between old and new EU members aresubstantial. The burden of cervical cancer is particularlyhigh in the newmember states, which geographically andhistorically belong to eastern part of Europe (Fig. 2).

Inmost Eastern European countries, the incidence ratesare more than 20 per 100,000, in some regions and someage groups are reaching 40 per 100,000 (Romania, Serbia).Incidence rates above 13 per 100,000 are observed inRussia and countries of the former Soviet Union, withArmenia (17.3/100,000) and Moldova (17/100,000) rank-ing the first in the region (1, 3).

Trends in cervical cancer incidence over past fewdecades

Comparing the latest Globocan report (2008) with theprevious one (2002), the incidence of cervical cancerin Europe has not changed (11.05 to 10.6 per 100,000

Authors' Affiliations: 1Faculty ofMedicine,University ofBelgrade;Depart-ment of Obstetrics and Gynecology, Clinical Center of Serbia, Belgrade,Serbia; 2Institute of Microbiology and Immunology, Faculty of Medicine,University of Ljubljana, Ljubljana, Slovenia; and 3RussianMedical academyof post-graduate education; Ministry of Healthcare and Social Develop-ment of the Russian Federation, Moscow, Russia

Corresponding Author: Vesna Kesic, Faculty of Medicine, University ofBelgrade, Department of Obstetrics and Gynecology, Clinical Center ofSerbia, Visegradska 26,Beograd 11000, Serbia. Phone: 381-11-366-36-44or 381-63-89-88-335; Fax: 381-11-361-56-03; E-mail:[email protected]

doi: 10.1158/1055-9965.EPI-12-0181

�2012 American Association for Cancer Research.

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Cancer Research. by guest on October 25, 2020. Copyright 2012 American Association forhttps://bloodcancerdiscov.aacrjournals.orgDownloaded from

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women in 2002 and 2008, respectively), whereasmortalitydecreased for 10% (from 5.0 to 4.5 per 100,000 women;refs. 1, 4). Meanwhile, the age-adjusted incidence rate ofcervical cancer in United States decreased from 7.7 per100,000 women in 2002 to 5.7 per 100,000 women in 2008(4). According to SEER Cancer Statistics Review, since1975, the age-adjusted incidence rate of cervical cancer inUnited States has decreased from 14.8 per 100,000womento 6.6 in 2008 (5).

Cancer incidence statistics from early periods incertain registries are inflated by shortcomings in theregistration, which is why mortality trends may betterreflect changes in burden from cervical cancer, over thetime.

In EU, corrected age-standardized cervical cancer mor-tality rates have decreased significantly over the pastdecades in the old member states and continue todecrease, whereas in Eastern Europe and in the Balticstates, they are decreasing at a lower intensity (CzechRepublic, Poland), remaining constant at a high rate(Estonia, Slovakia) or even increasing (Bulgaria, Latvia,Lithuania, Romania; ref. 6).

Generally, in all Eastern European and former SovietUnion countries, the incidence has been increasing duringlast decade (7). In Russia, the number of patients with anewly diagnosed cancer increased by 4.6% from 2000 to2005 (8). In Belarus, cervical cancer incidence increasedfrom14.3 per 100,000 in 1997 to 17.2 per 100,000 in 2006 (9).

The trends in incidence of cervical cancer largely reflectcoverage and quality of screening, as well as the exposureto risk factors.

The prevalence of human papillomavirus (HPV) infec-tion differs within Europe, being in close correlation withthe incidence of cervical cancer. In most EU countries, theage-standardized prevalence of high-risk HPV types inwomen with normal cytology, aged 30 to 64 years, rangesbetween 2%and 10%, being the lowest in Spain (1.2%) andNetherlands (4.6%). In the other countries, such as Franceand Belgium, the prevalence is more than 12% showingsustained elevated levels in women aged >35 years withthe most prevalent HPV types being 16 and 18 (10). Arecent study conducted inMoscow, Russia, has shown theoverall HPV prevalence in screening population of 13.4%(<25 years, 42%; 25–30 years, 28.8%; >30 years, 11.1%). Themost frequent HPV types were HPV 16 (32.5%), HPV 31(17.0%), HPV 52 (13.1%), and HPV 56 (12.8%; ref. 11). In

Table 1. List of European countries

EU countries

Old member countries New member countries

* Austria (1) * Bulgaria (3)* Belgium (1) * Cyprus (3)* Denmark (1) * Czech Republic (2)* Finland (1) * Estonia (5)* France (1) * Hungary (2)* Germany (1) * Latvia (5)* Greece (1) * Lithuania (5)* Ireland (1) * Malta (1)* Italy (1) * Romania (3)* Luxembourg (1) * Poland (2)* Netherlands (1) * Slovakia (2)* Portugal (1) * Slovenia (2)* Spain (1)* Sweden (1)* United Kingdom (1)Non-EU countries* Albania (3)* Andorra (1)* Armenia (6)* Azerbaijan (6)* Belarus (4)* Bosnia & Herzegovina (3)* Croatia (3)* Georgia (6)* FYR Macedonia (3)* Iceland (1)* Liechtenstein (1)* Moldova (4)* Monaco (1)* Montenegro (3)* Norway (1)* Russia (4)* San Marino (1)* Switzerland (1)* Serbia (3)* Turkey (3)* Ukraine (4)* Vatican City-Holy See (1)

NOTE: 1, Western Europe; 2, Central Europe; 3, South-Eastern Europe; 4, former Soviet Union states; 5, Balticstates; and 6, Transcaucasia.

28

26

24

22

20

18

16

14

12

10

8

6

4

2

0

23.9

22 21.921 20.9

9.2

7.4

5.6 5.9 6.2

4.83.9

5.94.9

6

7.3

3.62.5

4.2

5.8

2.8

11.111.611.812.112.212.4

1313.213.314

15.815.816.116.617.1

8.3

1.8

8.9

6.5

IncidenceMortality

Rom

ania

FYR M

aced

onia

Bulga

ria

Den

mar

k

Cro

atia

Polan

d

Slove

nia

Portu

gal

Latvia

Mon

tene

gro

Belar

us

Rus

sian

Fed

erat

ion

Cze

ch R

epub

lic

Slova

kia

Eston

ia

Ukr

aine

Hun

gary

Rep

ublic

of M

oldo

va

Serbia

Lith

uania

AS

R (

W)

per

100,0

00

Figure 1. Cervix uteri, all ages. The list of first 20 countries in Europe.ASR (W), age-standardized rate by world population (1).

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general, prevalence rate reported in Eastern Europe(21.4%) is comparable with rates of sub-Saharan Africa(24%) and even higher than those in Latin America (16%)with the most common high-risk HPV types being notonly HPV16 and HPV 18 but also HPV 31, HPV 33, andHPV 39 (12).

Early onset of sexual life (in Russia, 13.5% girls startsexual relations before the age of 15 and by the age of 17,47.8%adolescents are sexually active; refs. 11, 13) andhighproportion of young female smokers (age, 13–15 years) inEastern Europe (ranging from 8.2% in FYR Macedonia to39.2% in Bulgaria; ref. 14) are important contributingfactors to the onset of the disease. However, differencesin sexual behavior and HPV infection cannot entirelyaccount for the geographic variation of the cervical cancerincidence. The most important factor is the availability ofscreening.

Status report of cervical cancer screening ratesOverviews on incidence and mortality trends for cer-

vical cancer have indicated close correlation to the inten-sity of organized screening. In the populations where thescreening quality and coverage have been high, theseefforts have markedly reduced the incidence of invasivecervical cancer (15).

Cervical cancer screeningpractices in countries ofEUThe EU currently recommends to start screening

between the age of 20 to 30 years and to extend it to 60

Table 2. Age-standardized incidence rates andcumulative risk for cervical cancer in Europe

Population ASR (W) Cumulative risk

Romania 23.9 2.28FYR Macedonia 22.0 2.28Bulgaria 21.9 2.06Lithuania 21.0 1.99Serbia 20.9 2.10Republic of Moldova 17.1 1.61Hungary 16.6 1.51Ukraine 16.1 1.52Slovakia 15.8 1.50Estonia 15.8 1.51Czech Republic 14.0 1.31Russian Federation 13.3 1.27Belarus 13.2 1.25Montenegro 13.0 1.31Latvia 12.4 1.20Portugal 12.2 1.18Denmark 12.1 1.00Croatia 11.8 1.11Poland 11.6 1.27Slovenia 11.1 0.99Ireland 10.9 1.00Norway 9.4 0.79Bosnia Herzegovena 9.1 0.91Iceland 8.4 0.66Belgium 8.4 0.76Sweden 7.8 0.66United Kingdom 7.2 0.61Albania 7.1 0.72France (metropolitan) 7.1 0.64Germany 6.9 0.66The Netherlands 6.8 0.60Italy 6.7 0.64Spain 6.3 0.57Luxembourg 6.3 0.66Austria 5.7 0.52Finland 4.5 0.37Cyprus 4.5 0.44Greece 4.1 0.42Switzerland 4.0 0.37Malta 2.1 0.24

NOTE: Data derived from the work of Ferlay andcolleagues (1).Abbreviation: ASR (W), age-standardized rate by worldpopulation.

Romania

Bulgaria

Lithuania

Hungary

Estonia

Slovakia

Czech Republic

Poland

Slovenia

Latvia

Portugal

Ireland

Denmark

Belgium

European Union (27)

Norway

Austria

Sweden

Germany

France

United Kingdom

Luxembourg

Italy

Spain

Iceland

The Netherlands

Cyprus

Switzerland

Greece

Finland

Malta

5 10 15 20 25 30

IncidenceMortality

Figure 2. Estimated incidence and mortality from cervix uteri cancer in2008; age-standardized rate (European) per 100,000 (1).


www.aacrjournals.org Cancer Epidemiol Biomarkers Prev; 21(9) September 2012 1425



to 65 years, with a 3- or 5-year screening interval. Cancerscreening should be offered only through population-based, organized screening programs, with quality assur-ance at all levels (16). Although a population-based policyfor screening has been adopted by several EU memberstates, at the moment, key elements of the comprehensiverecommendations on program implementation are notfulfilled by many European countries (Table 3; ref. 17).

Substantial reductions in incidence and mortality,observed in United Kingdom, Finland and Iceland, cor-related with the level of implementation of organizedscreening (18). The best example is Finland where orga-nized screening was already established in the 1960s andwhere age-standardized corrected mortality rates havedropped by 80% over the last 45 years (19). It was esti-mated from an age period cohort model that withoutscreening, standardized cervical cancer mortality, in2003–2007 in Finland, would have been 6 times higher(20).

Opportunistic screening also resulted in a reduction ofcervical cancer incidence and mortality in other countriessuch as France or Austria (21).

Among the new member states, only Slovenia has thenationally organized screening program from 2003. Thecoverage reached even 82.1% in the first 5-year periodafter the implementation. Consequently, the incidence ofcervical cancer in Slovenia decreased for 40% in the periodfrom 2003 to 2009. Although Hungary also implementedorganized screening in 2004, the country is still strugglingwith low coverage of target population in organizedsettings and more than 60% attendance outside the pro-gram (17).

Other newmember countries (Czech Republic, Poland,Estonia, Lithuania, and Latvia) have already establishedat least partially functioning organized screening pro-grams but are dealing with several important obstacles,such as low coverage (less than 20%) of target populationwithin the program (22). Although cervical cancer isrecognized as the most urgent public health care problemin Romania, the screening infrastructure in the country isinsufficient andfinancial resources are less than10%of thenecessary amount (17).

Cervical cancer screening practices in non-EUEastern European countries and countries of theformer Soviet Union

Cervical cancer prevention in non-EU Eastern Europe-an countries, Russia, and other countries of the formerSoviet Union relies on opportunistic screening. This typeof screening has been characterized by high coveragein younger and very low coverage in middle-aged andolder women. Screening of selected groups of womenemployed in large companies is conducted annually bymany regional hospitals. This approach, however, hashadsmall effect on morbidity and mortality.

The opportunistic screening is based on the decision ofindividual woman to visit gynecologist for any reason.The cost of annual smear is covered by health care insur-

ance in most of Eastern European countries. This meansthat for any reason, women comes to gynecologist, sheshould be offered Pap smear. Such a system relies onawareness of women about cervical cancer, which isgenerally low (23). In countries where women are wellinformed about the importance of screening, the coveragein opportunistic screening is reaching 70% (Belgium,France, Slovenia), but in countries where the knowledgeis relatively poor, not more than 20% of women visitgynecologist regularly (Table 3).

The implementation of organized screening has startedin all countries of formerYugoslavia. Proposed age to startscreening varies from 20 to 30 years, with the age to stopscreening being between 55 and 69 years. A 3-year screen-ing interval is implemented in all countries and womenare screenedmainly by conventional cytology, with smallproportion of women screened by liquid-based cytologyin Croatia and FYR Macedonia. Unfortunately, there areno published data on cervical cancer screening practice inAlbania.

After cytology was introduced in the Soviet Union, inLeningrad Region, in 1964, the prevalence of invasivecervical cancer decreased from 31.61 to 8.13 per 100,000women, during the following decade (24). Later, suchsystem of opportunistic screening beginning from the ageof 18 years with no upper age limit has been expanded tothe whole country, and to a certain extent, is still main-tained in the Russian Federation, Ukraine, Republic ofBelarus, Moldova, and to much lesser degree in Armenia,Azerbaijan, and Georgia. However, these opportunisticscreening programs that are currently in place are notsufficient.

The national strategies on cervical cancer preventionare under development in all these countries (25). Screen-ing procedures, follow-up, and treatment services areprovided free of charge to all eligible women and arecovered through mandatory health care insurance.Although prevention programs are not yet availableinmany locations (Armenia, Azerbaijan), somewell-orga-nized pilot programs of organized screening wereinitiated (such as in Tbilisi, Georgia) with the plan forexpansion to the whole country.

In conclusion, there are large variations in cervicalcancer screening policies, coverage, and quality of screen-ing across Europe. Being the member of EU is helpful buthas no direct consequence on the efficacy of the cervicalscreening. The European cervical cancer screening guide-lines (16) were prepared for all European countries (notonly for EU members), but many of them failed in imple-mentation (including Germany, currently the economi-cally leading European country). On contrast, some ofnon-EU countries (Norway, Switzerland, Iceland)achieved good results in screening for cervical cancer.

Decisions on the target age group and frequency ofscreening are usually made at the national level, on thebasis of local incidence and prevalence of cancer, HPVprevalence, availability of resources and infrastructure(Table 3). However, continued unavailability of

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Tab

le3.

Anov

erview

ofsc

reen

ingpractices

inEurop

e

Typ

eof

screen

ing

Statusof

screen

ing

Started

(yea

r)Scree

ning

test

Agerang

eScree

ning

interval

(y)

Cove

rage

Alban

iaNodata

Nodata

Noda

taNodata

Noda

taNodata

Nodata

Arm

enia

Opportunistic

Nationa

l20

07Con

ventiona

lcy

tology

30–60

3N/A

Aus

tria

Opportunistic

Nationa

lN/A

Con

ventiona

lcy

tology

18—no

tsp

ecified

1N/A

Aze

rbaijan

Noprogram

Noprogram

——

——

—

Belarus

Opportunistic

Nationa

lN/A

Con

ventiona

lcy

tology

18—no

limit

1N/A

Belgium

Opportunistic

Nationa

lN/A

Con

ventiona

lcy

tology

25–64

370

%

Bos

niaan

dHerze

govina

Opportunistic

Nationa

l19

53Con

ventiona

lcy

tology

HPV

20—no

limit

1(exten

ded

to3yafter3

cons

ecutivene

gativ

esm

ears

Nodata

Bulga

riaOpportunistic

Nationa

lMid

1990

sCon

ventiona

lcy

tology

30–59

3Nodata

Croatia

Opportunistic

Nationa

l19

53Con

ventiona

lcy

tology

LBC

25–64

335

%–42

%

Cyp

rus

Noprogram

Noprogram

——

——

—

Cze

chRep

ublic

Organ

ized

Nationa

l20

08Con

ventiona

lcy

tology

25–60

148

%

Den

mark

Organ

ized

Nationa

lCon

ventiona

lcy

tology

23–65

3in

age23

–50

(5for

50þ)

69%

Eston

iaOrgan

ized

Nationa

l20

06Con

ventiona

lcy

tology

30–59

312

.7%

Finlan

dOrgan

ized

Nationa

l19

63Con

ventiona

lcy

tology

(25)

30–60

(65)

573

%

Fran

ceOpportunistic

Organ

ized

in5

region

s

Nationa

lN/A

Con

ventiona

lcy

tology

20(25)-not

spec

ified

371

%

FYRMac

edon

iaOpportunistic

Nationa

l19

67Con

ventiona

lcy

tology

LBC

30–55

315

%–25

%

Geo

rgia

Opportunistic

Organ

ized

in1

region

Nationa

lN/A

Con

ventiona

lcy

tology

25–60

320

%

German

yOpportunistic

Nationa

lN/A

Con

ventiona

lcy

tology

20—no

tsp

ecified

1N/A

(Con

tinue

don

thefollo

wingpag

e)





Tab

le3.

Anov

erview

ofsc

reen

ingpractices

inEurop

e(Con

t'd)

Typ

eof

screen

ing

Statusof

screen

ing

Started

(yea

r)Scree

ning

test

Agerang

eScree

ning

interval

(y)

Cove

rage

Greec

eOpportunistic

Nationa

lN/A

Con

ventiona

lcy

tology

20—no

tsp

ecified

1N/A

Hun

gary

Organ

ized

Nationa

l20

02Con

ventiona

lcy

tology

25–65

328

–31

%

Icelan

dOrgan

ized

Nationa

l19

64Con

ventiona

lcy

tology

20–69

2up

toag

e39

(4ye

ars

afterw

ardto

65–69

)80

%

Ireland

Organ

ized

Reg

iona

l;na

tiona

lpa

nned

2008

LBC

25–65

3in

age25

–44

(5for

45þ)

62%–66

%

Italy

Organ

ized

Nationa

l20

04Con

ventiona

lcy

tology

25–64

3>5

9%

Latvia

Organ

ized

Nationa

l20

09Con

ventiona

lcy

tology

25–70

342

%

Lithua

nia

Organ

ized

Nationa

l20

04Con

ventiona

lcy

tology

25–60

39%

–17

%(39%

)

Luxe

mbo

urg

Opportunistic

Nationa

lN/A

Con

ventiona

lcy

tology

15—no

tsp

ecified

1N/A

Malta

Noprogram

Noprogram

——

——

Moldov

aOpportunistic

Nationa

lN/A

Con

ventiona

lcy

tology

20—no

limit

2N/A

Mon

tene

gro

Opportunistic

Nationa

lN/A

Con

ventiona

lcy

tology

25–64

3Noda

ta

TheNethe

rland

sOrgan

ized

Nationa

lN/A

Con

ventiona

lcy

tology

30–60

577

%

Norway

Organ

ized

Nationa

l19

95Con

ventiona

lcy

tology

25–69

375

%

Polan

dOrgan

ized

Nationa

l20

06Con

ventiona

lcy

tology

LBC

25–59

322

.6%–26

.8%

Portuga

lOrgan

ized

in3

region

sNationa

lN/A

Con

ventiona

lcy

tology

25–64

358

%

Rom

ania

Opportunistic

Organ

ized

pilo

tin

oneregion

Nationa

l19

65Pilo

t20

02–

2006

Con

ventiona

lcy

tology

LBC

25–64

318

.4%

(10%

inregion

al

Rus

sia

Opportunistic

Nationa

lCon

ventiona

lcy

tology

18—no

limit

115

%–20

%

(Con

tinue

don

thefollo

wingpag

e)

CEBPFOCUS




Tab

le3.

Anov

erview

ofsc

reen

ingpractices

inEurop

e(Con

t'd)

Typ

eof

screen

ing

Statusof

screen

ing

Started

(yea

r)Scree

ning

test

Agerang

eScree

ning

interval

(y)

Cove

rage

Serbia

Opportunistic

(organ

ized

inproce

ssof

implemen

tatio

n)

Nationa

l19

70Con

ventiona

lcy

tology

25–65

(69)

320

%

Slova

kia

Opportunistic

Nationa

l19

80Con

ventiona

lcy

tology

23–64

317

%–20

%

Slove

nia

Organ

ized

Nationa

l20

03Con

ventiona

lcy

tology

20–64

370

%–74

%

Spain

Opportunistic

Organ

ized

inregion

s

Reg

iona

lN/A

Con

ventiona

lcy

tology

30–65

3N/A

Swed

enOrgan

ized

Nationa

lN/A

Con

ventiona

lcy

tology

23–60

373

%

Switz

erland

Opportunistic

Nationa

lN/A

Con

ventiona

lcy

tology

20—no

limit

380

%(age

22–44

)65

%(age

45–

64)

Turkey

Opportunistic

Nationa

lN/A

Con

ventiona

lcy

tology

18—no

limit

1N/A

Ukraine

Opportunistic

Nationa

lN/A

Con

ventiona

lcy

tology

18–65

1N/A

UnitedKingd

omOrgan

ized

Nationa

l19

88LB

C(20)

25–60

(64)

374

%

NOTE

:Sou

rces

aretheworks

ofAntillaan

dco

lleag

ues(17),A

rbyn

andco

lleag

ues(18),N

iculaan

dco

lleag

ues(22),c

ervica

lscree

ning

inEurop

e(http://w

ww.ecc

a.info/en/ce

rvical-

canc

er-preve

ntion/ce

rvical-scree

ning

/cse

1/table-2.htm

l),an

dbyco

urtesy

ofM.P

oljakan

dS.R

ogov

skay

a:sc

reen

ingin

Cen

tral/Eas

tern

Europ

ean

dRus

sia/form

erSov

ietUnion

coun

tries(unp

ublishe

dda

ta).

Abbreviation:

N/A,n

otav

ailable.





population-based, systematically organized screeningprograms to women who may benefit from screeningremains to be the major obstacle in control of cervicalcancer in Europe.

Status report on HPV vaccination disseminationrates

The implementation of organized programs to vacci-nate adolescent girls against HPV infection is an impor-tant strategy for the prevention of cervical cancer. Assummarized in Table 4, almost all European countrieshave approved both HPV vaccines, have national recom-mendations, and offer vaccines covered by health careinsurance for target group of females and given ondemand. Most of EU member countries have decided tointroduce HPV vaccination into their national immuni-zation schedule or have started the decision-making pro-cess with a recommendation favoring introduction (26).Yet, only a few of them have actually implemented HPVvaccination in their national immunization program andcurrently provide routine vaccination free of charge to theprimary target population.

Thevaccinationwas successfully implemented throughcompulsory school-based programs, with the excellentcoverage (>90%) in United Kingdom and Norway (27).

In Slovenia, HPV vaccination is conducted in schoolhealth care service network, reaching the coverage for 3doses of 55.0% for the school year 2010–2011. In Latvia,HPV vaccination is conducted in local public health carecenters and school health care services. In Romania, anational school-based program to vaccinate femalesaged 11 was first launched in 2008 but was stopped atthe endof year 2011due tonegativepublic reaction, lack ofproper communication, and resulting in low coverage intarget population which did not reach 5%. Most of othercountries offer free vaccination to the primary targetpopulation, with different coverage rates (Portugal,89%; Netherlands, 50%; Greece, 9%; Table 4). In contrastto other European countries, in Finland where cervicalcancer is effectively controlled by the national screeningprogram, the authorities decided to run a long-term pro-spective study to evaluate the bivalent HPV vaccine in arandomized community trial, before any decision onnational program is made (28).

In Central and East Europe, both HPV prophylacticvaccines are registered in all countries except Montene-gro. However, only FYR Macedonia actually integratedthe HPV vaccination in its national immunization pro-gram and currently provides routine vaccination freeof charge to primary target population. The coverage for3 doses in FYR Macedonia increased from 36.5% for theschool year 2009–2010 to 67% for the school year 2009–2010.

In Russia, HPV vaccination has been implemented insome regional immunization programs and more than20,000 girls have been vaccinated. However, is notincluded in national immunization program. The initi-ation of the HPV vaccination program in Moscow

region showed a lack of knowledge about HPV, amongadolescents, parents, and teachers. Immunization wasoften negatively perceived by the society as a potentialencouragement for adolescents to initiate sexual activ-ity. Only in Ukraine, HPV vaccination is now in theprocess of implementation in the immunization calen-dar. There are regional or pilot vaccination programsin Moldova, Georgia, Belarus and no national dataabout HPV immunization programs in Armenia andAzerbaijan.

The key reasons for lack of implementation of HPVvaccination on national level in majority of Europeancountries are high vaccine cost, financial constraints, andnegative public perception. In summary, the HPV vac-cines are beingdelivered to the low-incidencepopulationsthat already have extensive cervical cancer screeningprograms, whereas the high-incidence countries have notimplemented vaccination programs.

Recommendations for reducing burden of cervicalcancer in region

It has been almost 10 years since the Council of EUstarted to focus the attention toproblemof breast, cervical,and colorectal cancer screening (29). Despite of well-defined screening policy, by 2007, only 8 countries hadorganized screening.

European Guidelines for Quality Assurance in Cer-vical Cancer Screening have been initiated in the EuropeAgainst Cancer Program (16). It established the princi-ples of organized population-based screening and stim-ulated numerous pilot projects. It is hoped that theseguidelines will have a greater impact on countriesin which screening programs are still lacking and inwhich opportunistic screening has been preferred in thepast. As a result, today 16 countries and 9 regions havenationally organized population-based screening pro-grams in Europe.

Among all preventive public health care interven-tions, high coverage of the target population with cytol-ogy screening and HPV vaccines is essential to achievemaximum reduction of cancer cases. Therefore, toobtain the maximum coverage and future visible ben-efit, immunization programs targeting adolescentsbefore exposure to HPV should be preferred and pop-ulation-based. Also, effective communication strategiesmust be adopted.

The resolution of the problem of cervical cancer inEurope will not be a matter of further scientific researchbut rather the implementation of public health careprograms. All European countries must be encouragedto implement these programs as a priority. Substantiallyhigher dimension of this public health care problem inthe Eastern Europe requires special attention andpossibly unique approach. Redesigning the service andchanging attitudes in public, medical profession,and government will be the main ways to improvecurrent unsatisfactory cervical cancer outcomes at ourcontinent.

CEBPFOCUS




Tab

le4.

Anov

erview

ofstatus

ofHPVva

ccinationin

Europ

e

Vac

cine

sap

prove

dNationa

lreco

mmen

dations

Vac

cina

tion

program

Typ

eofprogram

Start

(yea

r)

Agerang

e(primary

target

group

)Agerang

e(catch

-up)HPVva

ccine

registration

Fina

ncing

Alban

iaNodata

Nodata

Nodata

——

—Nodata

Nodata

Arm

enia

Yes

No

Noprogram

Ava

ilable

ondem

and

—Nodata

No

Priv

atefund

ing

Aus

tria

Yes

Yes

Noprogram

—20

069–

1516

–26

No

Priv

atefund

ing

Aze

rbaijan

Yes

Yes

Noprogram

Ava

ilable

ondem

and

—Nodata

No

Priv

atefund

ing

Belarus

Yes

No

Noprogram

Ava

ilable

ondem

and

2010

11No

Priv

atefund

ing

Belgium

Yes

Yes

Reg

iona

lSch

ool-bas

ed20

0710

–13

13–18

Yes

Free

ofch

arge

(Flemishco

mmun

ity)

Bos

niaan

dHerze

govina

Yes

No

Noprogram

Ava

ilable

ondem

and

——

Yes

Priv

atefund

ing

Bulga

riaYes

Yes

Tobeim

plemen

ted

in20

12Ava

ilable

ondem

and

—12

–25

Yes

Priv

atefund

ing

Croatia

Yes

Yes

Noprogram

Ava

ilable

ondem

and

—15

–26

Yes

Priv

atefund

ing

Cyp

rus

No

No

Noprogram

——

——

—

Cze

chRep

ublic

Yes

Yes

Noprogram

Ava

ilable

ondem

and

—9–

26Yes

Priv

atefund

ing

Den

mark

Yes

Yes

Nationa

lInvitatio

ns20

0912

–15

15–17

Yes

Free

ofch

arge

Eston

iaYes

Yes

Noprogram

Ava

ilable

ondem

and

—>1

2Yes

Priv

atefund

ing

Finlan

dYes

Yes

Noprogram

Ava

ilable

ondem

and

Long

-term

prosp

ectiv

estud

yon

theway

—No

Priv

atefund

ing

Fran

ceYes

Yes

Nationa

lOnde

man

d20

0714

15–23

No

Hea

lthinsu

ranc

eGeo

rgia

Yes

No

Reg

iona

lSch

ool-bas

edN/A

10–13

Free

ofch

arge

German

yYes

Yes

Nationa

lOnde

man

d20

0712

–17

Nodata

Hea

lthinsu

ranc

eGreec

eYes

Yes

Nationa

lOnde

man

d20

0812

–14

15–26

Nodata

Free

ofch

arge

Hun

gary

Yes

Yes

Noprogram

Ava

ilable

ondem

and

—9–

26Yes

Priv

atefund

ing

Icelan

dYes

Yes

Noprogram

Ava

ilable

ondem

and

—12

No

Priv

atefund

ing

Ireland

Yes

Yes

Nationa

l—

Propos

edin

2009

,but

postpon

ed;

reac

tivated

2010

1213

–15

No

Free

ofch

arge

Italy

Yes

Yes

Reg

iona

lInvitatio

ns20

0712

Yes

Free

ofch

arge

Latvia

Yes

Yes

Nationa

lSch

ool-bas

ed20

1012

Yes

Free

ofch

arge

Lithua

nia

Yes

Yes

Tobeim

plemen

ted

in20

12Onde

man

d20

1212

Yes

Priv

atefund

ing

Luxe

mbo

urg

Yes

Yes

Nationa

lOnde

man

d20

0812

13–18

No

Free

ofch

arge

Mac

edon

iaYes

Yes

Nationa

lSch

ool-bas

ed20

099–

26Yes

Free

ofch

arge

Malta

No

No

——

——

——

(Con

tinue

don

thefollo

wingpag

e)





Tab

le4.

Anov

erview

ofstatus

ofHPVva

ccinationin

Europ

e(Con

t'd)

Vac

cine

sap

prove

dNationa

lreco

mmen

dations

Vac

cina

tion

program

Typ

eofprogram

Start

(yea

r)

Agerang

e(primary

target

group

)Agerang

e(catch

-up)HPVva

ccine

registration

Fina

ncing

Moldov

aYes

No

Reg

iona

lInvitatio

ns9–

15No

Priv

atefund

ing

Mon

tene

gro

No

No

Noprogram

——

—No

—

TheNethe

rland

sYes

Yes

Nationa

lInvitatio

ns20

1012

13–16

Yes

Free

ofch

arge

Norway

Yes

Yes

Nationa

lSch

ool-bas

ed20

0912

Yes

Free

ofch

arge

Polan

dYes

Yes

Noprogram

Ava

ilable

ondem

and

—12

–13

Yes

Priv

atefund

ing

Portuga

lYes

Yes

Nationa

lOndem

and

2009

1314

–17

Yes

Free

ofch

arge

Rom

ania

Yes

Yes

Nationa

lSch

ool-bas

ed20

08–20

1012

–24

Yes

Free

ofch

arge

Rus

sia

Yes

No

Reg

iona

l(2

pilo

tprog

rams)

Sch

ool-bas

ed(program

s)Ava

ilable

ondem

and

outof

program

—11

–14

No

Free

ofch

arge

with

intheprogram

Serbia

Yes

No

Noprogram

Ava

ilable

ondem

and

—12

–14

No

Priv

atefund

ing

Slova

kia

Yes

Yes

Noprogram

Ava

ilable

ondem

and

—12

Yes

10%

cove

redby

insu

ranc

eSlove

nia

Yes

Yes

Nationa

lSch

ool-bas

ed20

0911

–12

Yes

Free

ofch

arge

Spain

Yes

Yes

Reg

iona

lSch

ool-bas

ed20

0811

–14

Yes

Free

ofch

arge

Swed

enYes

Yes

Nationa

lSch

ool-bas

ed20

1010

–12

Yes

Free

ofch

arge

Switz

erland

Yes

Yes

Reg

iona

lInvitatio

ns20

0810

–14

15–19

No

Free

ofch

arge

with

intheregion

alprogram

Turkey

No

No

No

——

——

Priv

atefund

ing

Ukraine

Yes

No

Noprogram

Ava

ilable

ondem

and

——

No

Priv

atefund

ing

UnitedKingd

omYes

Yes

Nationa

lSch

ool-bas

ed20

0812

–13

13–18

Yes

Free

ofch

arge

NOTE

:Sou

rces

aretheworks

ofNiculaan

dco

lleag

ues(22),L

� evy-Bruhlan

dco

lleag

ues(26),D

avies(27),a

ndbytheco

urtesy

ofM.P

oljakan

dS.R

ogov

skay

a:va

ccinationinCen

tral/

Eas

tern

Europ

ean

dRus

sia/form

erSov

ietUnion

coun

tries(unp

ublishe

ddata).

Abbreviation:

N/A,d

atano

tav

ailable.

CEBPFOCUS




Disclosure of Potential Conflicts of InterestM.Poljak hasHonoraria fromSpeakers Bureau fromAbbott,Merck and

Co., and Roche and is a Consultant/Advisory Board member for Abbott,GlaxoSmithKline, Roche, and Merck and Co. No potential conflicts ofinterests were disclosed by the other authors.

Authors' ContributionsConception and design: V. Kesic, M. Poljak, S. RogovskayaDevelopment of methodology: V. KesicAcquisition of data (provided animals, acquired and managed patients,provided facilities, etc.): M. Poljak, S. RogovskayaAnalysis and interpretation of data (e.g., statistical analysis, biostatis-tics, computational analysis): V. Kesic, M. Poljak

Writing, review, and/or revision of themanuscript:V. Kesic, M. Poljak, S.RogovskayaAdministrative, technical, or material support (i.e., reporting or orga-nizing data, constructing databases): S. RogovskayaCollection of data from various countries mentioned: S. Rogovskaya

Grant SupportInternational Agency for Research on Cancer has kindly granted the

authors permission for print and electronic rights to use data fromGLOBOCAN available at http://globocan.iarc.fr.

Received February 14, 2012; revisedMay 9, 2012; acceptedMay 29, 2012;published online September 6, 2012.

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2012;21:1423-1433. Cancer Epidemiol Biomarkers Prev Vesna Kesic, Mario Poljak and Svetlana Rogovskaya Cervical Cancer Burden and Prevention Activities in Europe

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