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��ࡱ�>��	������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������	��lsbjbj���	A"����@k+�������ff������������8���4�8D��:��
�C�C�C�C�C�C�C�E�|H6�C����C����CH$H$H$n���B$H$�CH$H$�I0|�1������Ox�{���#��0�BD08D�0��H$.�H$�1�1��H��2H$�C�CH$8D���������������������������������������������������������������������Hf	o:	Cervical cancer rates and screening program characteristics: an ecological analysis of European data
Lovney, Kangurua*., Sohinee, Bhattacharyab., Shona, Fieldingc., Julia, Husseina., Amudha, Poobaland
a IMMPACT, 2nd Floor Health Sciences Building, School of Medicine & Dentistry, University of Aberdeen, UK
b Dugald Baird Centre for Research on Women's Health, Aberdeen Maternity Hospital, University of Aberdeen, UK
c Medical Statistics Team, Polwarth Building, School of Medicine & Dentistry, University of Aberdeen, UK
d Public Health Nutrition Research Group, Polwarth Buidling, School of Medicine & Dentistry, University of Aberdeen, UK
*Corresponding Author. Lovney Kanguru. Telephone: +44(0)1224 438114; Fax: +44(0)1224 438110; email: HYPERLINK "mailto:l.n.kanguru@abdn.ac.uk"l.n.kanguru@abdn.ac.uk











Abstract
Background: Cervical cancer causes the deaths of 275,000 women worldwide. It is the third leading cancer in women globally. Early detection by regular screening can prevent premature deaths of women. We examined associations between cervical cancer incidence/mortality rates and characteristics of screening programmes in European Union countries.
Method: Ecological analysis using data from Global Cancer (GLOBOCAN), International Agency for Research on Cancer, the European Commission and studies within the European Network for Information on Cancer and European Cancer Health Indicator Projects. Appropriate statistical tests followed by multiple linear regressions were used to identify relationships. 
Results: 27 European Union countries were included. Incidence was highest in Romania and lowest in Malta, while mortality was highest in Romania and lowest in Finland. Incidence (r= -0.416, p=0.031) and mortality (r= -0.459, p=0.016) rates were negatively correlated with duration of cervical screening programs. Multiple linear regression showed statistical significance for duration of cervical screening programs with mortality (p=0.046). The regression model for incidence included duration of screening programs (p=0.027) and general practitioners as the smear taker (p=0.034). 
Conclusion: Associations between some screening characteristics and incidence/mortality rates exist. This implies that screening is still an important public health strategy for reduction of cervical cancer. Relationship between smear taker and incidence rates need further investigation.

Key words: cervical cancer, non-communicable diseases, screening, incidence, mortality, Europe, European Union




List of abreviations
GLOBOCAN:		Global Cancer 
IARC:			International Agency for Research on Cancer
EC:			European Commission
EUROCHIP:		European Cancer Health Indicator Projects
HPV:			Human Papilloma Virus
HIV:			Human Immunodeficiency Virus
Pap smear:		Papanicolaou smear 
EU:			European Union
EUNICE:		European Network for Information on Cancer
GPs:			General Practitioners
SB:			Sohinee Bhattacharya
Introduction
Cancers are the second leading cause of death in women among the non-communicable diseases [1, 2]. Cervical cancer is ranked as the third most common cancer in women after colorectal and breast cancers [3]. Every year, an estimated 530,000 women worldwide are newly diagnosed with cervical cancer and 275,000 die from the condition [3]. In the European Union, the second commonest cause of death is cancer [4]. Cervical cancer claims the lives of 28,000 women out of the 61,000 new cases diagnosed every year [3]. Incidence of cervical cancer and consequently the mortality has increased by approximately 50% since 2004 [5]. This can be attributed to factors such as promiscuity, level of education, financial inequalities, immigration influence and possibly due to screening implementation, where more prevalent cases will be detected [6,7]. 
The development of cervical cancer is associated with human papilloma virus (HPV) alongside other risk factors [8]. These include cigarette smoking, age of onset of coitarche, multiple sexual partners, multi-parity, long-term use of oral contraceptives and poor nutrition [8, 9, 10]. Apart from these, sexually transmitted infections like Human Immunodeficiency Virus (HIV), Herpes Simplex Virus type 2, Chlamydia Trachomatis and Neisseria Gonorrhea have also been shown to increase the risk of the disease [8, 11]. 
Cervical cancer is reported to affect women who are less than 45 years of age more than any of the other major cancers, and yet, it is easily preventable12. Early detection of cervical cancer through regular screening has a potential of consequent reductions in mortality [4, 13]. Usually, screening for cervical cancer is done using the Papanicolaou smear (Pap smear) test to detect precancerous changes in the cervix. However, only a few countries continue to include cervical screening in family planning clinics particularly targeting young women [4, 14]. 
Screening for cervical cancer can either be organized or opportunistic. In organized screening, also known as �programs�, a program policy exists which clearly defines the target population, test for screening and interval period between tests. Organized programs are population based and eligible individuals are identified through general practitioners� files, population registries or electoral registries and sent invitations using a call-recall system [4, 14], as in the United Kingdom and Finland [14, 15]. Other important elements include trained healthcare providers, quality assurance at different levels of the service, wide coverage, clear referral pathway and management of abnormal findings and follow up [14]. Conversely, opportunistic screening is seen as �non program� screening, and is based on the doctor�s or women�s own initiative to request for screening. Although no systematic invitation is sent out to women in this type of screening, there is some form of policy guidance outlining the target age group, tests to be used and screening intervals [14]. Good examples are countries like United States of America and Switzerland [13, 14]. In both screening programs, cervical smears are usually taken by general practitioners, gynecologists and nurses or midwives who are specially trained [14]. 
In the European Union (EU), the EU council first recommended cervical screening programs for its member states in 1987 [14]. It was not until 1993 that quality assurance was introduced into the recommendations. In 2003, the council took the opportunity to emphasize population based screening programs with quality assurance at every level [4, 14]. They saw screening as a potential tool to control for cancers, especially cervical cancer. In addition, the council recommended screening of women from 25 years of age, and stopping at the age of 64 or 65 years [14]. Another recommendation was to include screening intervals between 3 to 5 years, depending on each country�s resources available [4, 14].
To date, the organization of screening for cervical cancer across the EU countries varies greatly, as do the incidence and mortality rates from cervical cancer. It has not been established whether differences in the organization of screening have led to a variation in population health outcomes. This paper seeks to examine the associations between incidence and mortality rates of cervical cancer with screening program characteristics in all the EU countries. 

 Methods
Study design, population and ethics
We conducted an ecological analysis of 27 European Union countries: Austria, Belgium, Bulgaria, Cyprus, Czech Republic, Denmark, Estonia, Finland, France, Germany, Greece, Hungary, Ireland, Italy, Latvia, Lithuania, Luxemburg, Malta, Netherlands, Poland, Portugal, Romania, Slovakia Republic, Slovenia, Spain, Sweden and United Kingdom. Published national level data that was summarized from cancer registries of all the women screened for cervical cancer were used. Ethical approval was not needed as the data were available in the public domain.
Outcomes and data sources 
Incidence and mortality rates were obtained from the latest estimates provided by GLOBOCAN (2010). Age standardized incidence and mortality rates was used in-order to make comparisons across different population profiles possible.
For the screening program characteristics, age of screening onset and cessation, time interval between tests, type of screening (organized or opportunistic), person taking the smear and duration of screening programs were considered. These characteristics were selected based on information from World Health Organization HPV preventive strategies and from primary studies of characteristics influencing the occurrence of cervical cancer [13, 14, 16, 17]. Other characteristics such as screening coverage were not included due to reliability of the data available which could not be counterchecked with other sources. In addition, some of the EU countries did not have data on screening coverage. Data for the characteristics included were obtained from European Commission (EC) studies on cervical cancer, EC studies within the European Network for Information on Cancer (EUNICE), European Cancer Health Indicator Projects (EUROCHIP studies) [18, 19, 20, 21, 22, 23, 24, 25, 26] and International Agency for Research on Cancer (IARC) handbook [14]
Quality check and analysis 
All relevant data collected were counterchecked with a second source for consistency. For example, data from EC and EUROCHIP studies were counterchecked with information provided by EUNICE and IARC. Any discrepancies that arose were resolved through discussion with Sohinee Bhattacharya (SB). 
Statistical analyses were carried out using SPSS version 17 (Chicago, Illinois). Associations between burden of cervical cancer (incidence and mortality rates) and categorical screening program characteristics were investigated using Independent t-test, ANOVA, Mann Whitney and Kruskal Wallis tests as appropriate. Pearson and Spearman�s (due to non-normality) correlation coefficients were calculated for continuous variables. Multiple linear regression was used to model incidence and mortality rates using significant predictors (p<0.05). 

Results
A summary of the incidence, mortality and screening program characteristics for the 27 European Union (EU) countries is shown in Table 1.
The incidence rate for cervical cancer was highest in Romania (23.9 per 100,000) and lowest in Malta (2.1 per 100,000). Romania also had the highest mortality rate while Finland had the lowest (11.8 per 100,000 and 1.2 per 100, 000 respectively). There was some variation in age at which women were first screened. Bulgaria had the latest onset for screening women at 31 years old, while Luxembourg started screening women at 15 years of age. In most of the EU countries, screening for older women stopped between the ages of 60 and 70 years, the exceptions being Estonia and Poland who stopped at 59 years of age. Only in Luxembourg, screening did not have an upper age limit. Twelve countries in the EU had three year screening interval, while the remaining fifteen countries ranged between 1 to 5 years. Thirteen (48%) EU countries had organized screening programs. Variation was also seen in the person who took the smear ranging from gynecologists to general practitioners and trained nurses or midwives. Duration of regular cervical screening programs varied within countries with the Czech Republic having the shortest period (4 years) and Luxembourg the longest (50 years).
Incidence was negatively correlated to duration of cervical screening programs (r= -0.416, p=0.031) (Table 2), demonstrating that countries which had screening programs running for longer time were more likely to have lower incidence of cervical cancer. Mortality rate was negatively correlated with duration of the screening programs (r= -0.459, p=0.016). This indicated that mortality rate was more likely to be lower in countries that had longer screening programs (Figure 1). However there were a few outliers, for example Bulgaria, Slovak Republic and Latvia which had screening programs running as long as 42, 36 and 40 years respectively, and yet, their cervical cancer mortality rates were high and ranked among the top ten countries listed (Table 1). Age of screening onset, age when screening stops and screening interval showed no statistically significant correlation with incidence or mortality rates (Table 2). 
The incidence or mortality rates were not found to statistically differ between countries that used opportunistic or organized screening or between the different types of smear taker (Table 3).
Table 4 - model A, shows the multiple linear regression model for mortality rate with all the screening program characteristics as predictors. Duration of cervical screening remained significant when adjusted for the other program characteristics (p=0.046). Thus indicating, mortality rate was expected to decrease by 0.078% for every year increase in duration of screening program. Using a forward selection process rather than the full model with all characteristics, only duration of cervical screening remained significant with a coefficient of -0.07 (95% CI -0.13, -0.007), but R2 = 17.2% compared to R2 = 41.4% for the full model, suggesting that the full model explains more of the variation in mortality. The multiple linear regression model undertaken for incidence with all the screening characteristics found none of the predictors to be statistically significant (data not shown). However a forward selection process, suggested duration of cervical screening and whether or not GPs were the smear takers were important predictors of incidence with R2 = 0.32 (Table 4 - model B). This suggests that a year longer duration of cervical screening would decrease incidence by 0.15% (95% CI 0.02 to 0.28)%. Having GPs as the only smear taker would increase incidence by 5.5% (95% CI 0.44 to 10.5)%.
Discussion
The importance of screening as a strategy in reducing cervical cancer burden of disease is well documented, and has a potential of reducing it up to 80% of the burden [4, 17, 27]. The compiled data on incidence and mortality rates from this study showed striking differences between countries in Eastern and Western Europe, with higher rates being seen in Eastern Europe. This difference is perhaps not that surprising, and could plausibly be explained by factors such as; when countries joined the EU, implementation of screening policies, resources available, screening coverage and quality assurance some of which could not be assessed in the study [14, 28]. 
Duration of screening program: There was an inverse relationship found between duration of screening programs and incidence or mortality rates; implying that countries which had screening programs running for longer time were more likely to have lower mortality and lower incidence rates. When these findings were compared with those from other developed countries such as Australia, New Zealand, Canada, USA and Japan which had screening programs running for 25 years or more, a similar inverse relationship with incidence and mortality rates was seen [3, 14]. In contrast, countries like Cuba and Costa Rica with screening programs ongoing for about 40 years (as Slovak Republic, Bulgaria and Latvia) had not managed to reduce the mortality from cervical cancer [29]. This could be because of the variation in screening coverage, organization of screening or lack of quality assurance. For any effective screening programs, recruitment of target population, infrastructure for screening tests, confirmation tests and management of abnormal findings and patient compliance are crucial which might not have been possible in these countries. 
Health personnel taking the smear: During the univariate analysis, we found no association between incidence or mortality rate and the smear taker. However, an unexpected association was evident in the forward selection adjusted regression model between incidence and general practitioners (GPs) as the smear taker. This finding could be due to chance, interdependence between cadres or better detection of the disease by GPs. One would expect higher incidence rates among gynecologists who screen populations presenting with abnormal gynecological problems more than midwives or GPs who screen populations where precancerous lesions are uncommon. 
Organized or opportunistic screening: No association was found between opportunistic or organized screening programs with incidence or mortality rates. This could be due to chance or possible confounders such classification of screening programs by different countries, populations targeted or invited for screening or variations in program definitions which were not assessed in the study. The majority of countries within the EU had some form of cervical screening policy in place; however, the real challenge was in its implementation at a national scale4, 14. A review by Antilla, et al, [18] showed that opportunistic screening in Latvia was ineffective following it�s re-introduced in 2005. Lack of clear management framework, coordination of the program and control of cervical cancer were reported. Formerly, Latvia had implemented an organized screening program which was later terminated in 1989 due to political instability. Outside the European Union, reduced cervical cancer rates have been reported in countries like Iceland, Norway, Chile and Colombia as clear benefits of the health system�s functionality that incorporated organized screening program [14]. This is further supported by a study done in Hong Kong which showed that organized screening programs were more effective and cost-effective compared to opportunistic ones [30]. A good framework, infrastructure, management facilities, trained healthcare providers, clear referral pathway, follow up, adequate surveillance and education of the population are all important contributors [14, 30].
Women�s age at onset and cessation of screening: Age of onset of screening and cessation were not associated with incidence or mortality rates. There was some variation, for example, Luxembourg started screening women at 15 years of age with no upper age for stopping while Finland started at 30 years and stopped at 60 years, and yet, Finland had lower incidence and mortality rates than Luxembourg (table 1). These findings when compared to other developed countries further confirm the lack of a clear association. For example in Israel, women are first screened at the age of 35 years and stopped at 54 years, and yet Israel, has lower incidence rate (5.6 per 100,000 respectively) compared to Luxembourg (6.3 per 100,000)14. These differences or lack of association observed may not only be due screening programmatic elements but also due to other factors such as HPV vaccination, marital status, access to screening services influenced by rurality in some regions, women�s interaction with the health system, culture, literacy rates, prostitution, role of the male partner, and religion [14, 31]. For example, Scotland recently announced plans to increase the age of screening onset from 20 to 25 years by 2015 [32]. This change was largely influenced by HPV vaccination, as the first cohort of 12-13 year old girls who had been immunized in 2008 will be due for their first cervical screening. 
Strengths and limitations: Overall, the strengths of this study are seen in the uniformity of screening recommendations at policy level, all the countries studied had some form of a screening program, there was homogeneity of data capture, data used was quality cross checked, similarity of populations studied (predominantly Caucasian), and the study design (ecological design) used was the most appropriate to study country level screening programs. However, our study was also prone to limitations of ecological fallacy with only 27 countries used, cultural and population differences. In addition, uptake of cervical screening, screening coverage, financial constraints and the time period in the EU by different countries were other possible limitations.
Lessons learnt and recommendations
The functionality of a screening program within the health system cannot be viewed in isolation. There was no association with age of screening onset and cessation, time periods between two screenings and type of screening, which in this analysis were possibly limited by the small numbers. However, these factors should not be undermined due to the interdependence of these variables and the complex nature of screening programs. The association found with duration of screening programs only goes to show the critical role screening plays in prevention of cervical cancer. From a wider action plan against all non communicable diseases, the World Health Organization recognizes the need for setting up a reliable population based monitoring and surveillance system, which also targets cervical cancer.  
While different EU countries continue to invest in screening programs, this work urges health policy makers, planners and managers to ensure monitoring and evaluation of these programs by means of quality assurance and evidence based operational research e.g. through randomized controlled trials where a significant gap still exists. Additionally, a few grey areas exist especially for countries employing opportunistic screening around screening processes, frameworks and discontinuation of screening for women immunized against HPV. 
In conclusion, screening is a key strategy in reducing cervical cancer. This work show that incidence and mortality rates of cervical cancer can be lowered by screening programs that were running for longer periods. Further investigation is needed on the association between incidence rates and the smear taker. 
Funding
None 

Conflicts of interest 
The authors declare they have no conflict of interest

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