Research Article
Austin J Public Health Epidemiol. 2016; 3(1): 1032.
Cervical Cancer Screening in the Municipality of Nicosia, Cyprus - Coverage and Association with Socioeconomic Determinants
Papapetrou I1,2, Charalambous G1,3, Sissouras A1,4 and Jelastopulu E1,5*
¹Postgraduate Program Health Management, Frederick University of Nicosia, Cyprus
²Strovolos Health Centre of Nicosia, Frederick University of Nicosia, Cyprus
³General Hospital of Athens “Hippocratio” of Athens, University of Patras, Greece
4Department of Operational Research and Management, University of Patras, Greece
5Department of Public Health, University of Patras, Greece
*Corresponding author: Eleni Jelastopulu, Department of Public Health, Medical School, University of Patras, 26500 Rio Patras, Greece
Received: October 12, 2015; Accepted: December 30, 2015; Published: January 04, 2016
Abstract
The aim of the present study is to determine the prevalence of Pap smear use among the women in Nicosia and to identify the factors associated with Pap test’s performance. A cross-sectional study was carried out on a representative sample of 525 women living in the municipality of Nicosia in 2014. Prevalence Ratios (PR) of Pap smear use were calculated. Information about demographic, socioeconomic and lifestyle factors was collected. About 81% had at least one Pap test in their life, with 70% having been tested in the previous three years. Women aged 25-64 were more likely to have had a recent Pap test than women aged 20-24. Furthermore, married/partnered women, employed women, women with higher education were more likely to have had a recent Pap test. Compared to women with a monthly household income of >1000€, those with lower income were less likely to have had a recent Pap test. Finally non-Cypriot women are less likely to have had a recent Pap test than Cypriot females. The prevalence of Pap testing in Nicosia is high. However, efforts to establish a cervical cancer screening in Cyprus should be planned and implemented in the framework of a comprehensive cancer control program taking into account overall health care needs and priorities emphasizing mainly in women with socioeconomic disadvantages.
Keywords: Cervical cancer screening; Prevalence of pap test
Introduction
The Health Profile of the city of Nicosia, Cyprus, was conducted in 2013-2014, within the Healthy Cities Programme, with the aim to collect and analyse information about the current socioeconomic and demographic situation of its citizens, their living conditions and health status as well as health related behaviors and to evaluate and implement preventive programmes, including cervical cancer screening. The ultimate purpose was to conduct a Health Action Programme of the City of Nicosia.
Cervical cancer is one of the world’s most common cancer among women, but at the same time one of the most preventable and treatable forms if detected early and managed effectively [1].
It is estimated that over one million women worldwide currently have cervical cancer. Most of these women have not been diagnosed, nor do they have access to treatment that could cure them or prolong their lives [1]. There is an unequal burden of cervical cancer [2]. In 2012, 528,000 new cases of cervical cancer were diagnosed worldwide and 266,000 women died of the disease, nearly 90% of them in lowto middle-income countries. Without urgent attention, deaths due to cervical cancer are projected to rise by almost 25% over the next 10 years [1].
Although significant advances are being made in the fight against cervical cancer, the disease remains a key public health concern and a tremendous burden on European societies. In the European Union (EU) 34,000 new cases and more than 16,000 deaths due to cervical cancer are reported annually [3,4]. The highest annual worldstandardized mortality rates are currently reported in Romania and Lithuania (13.7 and 10/100,000, respectively) and the lowest in Finland (1.1/100,000) [5].
Among all malignant tumours, cervical cancer is the one that can be most effectively controlled by screening [6]. It has been predicted that by implementing 100% population coverage of cervical cancer screening every 3-5 years, an estimated reduction of over 94% of life years lost could be attained, and for every 152 Pap smear tests performed, one life year could be gained [7]. In countries that have established such programs – mainly countries of developed world - cervical cancer incidence has shown a marked decrease. In times of financial instability, it is all the more important to maintain investments in health, in particular through preventive actions [8].
The EU Council recommends implementation of populationbased cervical cancer screening programs with identification and personal invitation of each woman in the eligible target population to the EU member states, with quality assurance at all levels [5]. Based on these recommendations most Member States (MS) have implemented population based organized cervical cancer screening programs either nationally or regionally. The highest screening rates are achieved in the United Kingdom, Norway and Sweden (80%) while the lowest ones are observed in Hungary (36%), the Slovak Republic (23%) and Romania (14%) [9].
In Cyprus in 2012 the incidence rate for cervical cancer was 5.2 per 100,000 women and the crude mortality rate was 2.5 per 100,000 women, while the age-standardized mortality rate was 7.2 per 100,000 women [10].
Cyprus is among the few European countries that have not yet establish both a national screening program for cervical cancer and a vaccination program against Human Papilloma Virus (HPV) that is causally linked with cervical cancer. However, from 2012, a regional pilot screening program was implemented in some communities in Nicosia district area, that includes women aged 25-65 under the care of the Ministry of Health. A private organisation of women in cooperation with the governmental health services organised this screening programme in which the Ministry of Health offers all the supplies and the health centers and the women organisation the doctors, the information and invitation of the eligible target population to performance of the screening test.
Cyprus has not established yet a National Health System (NHS), thus cervical screening in Cyprus is opportunistic and can be conducted in public or private hospitals or clinics. Several private clinics, mainly in Nicosia and Limas sol, have very well organized programs but no reliable data on the percentage of women covered are available. The majority of private gynaecologists also perform Pap tests in their private practices, not free of cost. There are no reliable data on the percentage of women who perform Pap tests privately. There are plans to establish a national organized population based screening program for cervical cancer as mentioned in the National Action Plan for Cancer which has been in effect since 2008.
Materials and Methods
Study design, data collection and study population
The data were collected between May 2013 and April 2014 through a research-administered survey. An interviewer addressed the questions to a representative sample of 525 women aged 20 to 74 years old, residents of Nicosia, who were selected by stratified sampling based on the census data of Cyprus.
The outcome variable of interest for this analysis was the proportion of women who have ever had a Pap-test and the proportion of women who had had a Pap-test within the last 3 years before the study. Independent variables included demographic and socioeconomic characteristics, such as age in years, marital status, educational level, household income, house ownership, health care coverage and occupational status. Secondary characteristics included body mass index (BMI categorized as underweight [18.5-19.9 kg/m2], within acceptable limits [20-24.9 kg/m2], overweight [25-29.9 kg/m2], obese [> = 30kg/m2]), tobacco exposure (expressed in pack-years and defined as 1 pack-year corresponding to twenty cigarettes smoked every day for one year) and alcohol consumption.
Statistical analysis
The statistical analysis was conducted by using IBM SPSS Statistics for Windows, Version 22.0. (IBM SPSS Statistics for Windows, Released 2013. Armonk, NY: IBM Corp.). The relationship between cervical cancer screening behaviour and demographic, clinical, and lifestyle factors was assessed by using Pearson’s chi square tests. In addition, binary logistic regression models, using the forced entry method, were used to further assess these relationships, where the prevalence odds ratios and their 95% Confidence Intervals (CI) were estimated to determine the magnitude of the association between the specific factors and cervical cancer screening behaviour. The accepted levels of significance were 0.05 or less.
Result
The main demographic and socioeconomic characteristics of the study population are presented in (Table 1).
Characteristics
Number (n)
Percentage (%)
Ever had Pap-test
Yes
421
80,8%
No
100
19,2%
Time since last Pap-test
< 3 years ago
365
70,3%
> 3 years ago
154
29,7%
Respondent’s age
20-24
45
8,6%
25-34
123
23,4%
35-44
111
21,1%
45-54
84
16,0%
55-64
66
12,6%
65-74
51
9,7%
75+
45
8,6%
Marital status
Single
131
25,0%
Married/Partnered
291
55,4%
Formerly married
103
19,6%
BMI
Underweight
24
4,6%
Normal
298
56,8%
Overweight
158
30,1%
Obese
45
8,6%
Educational status
Primary (<6 years)
72
13,7%
Lower secondary (6-9 years)
23
4,4%
Higher secondary (9-12 years)
153
29,1%
Undergraduate (12-16 years)
224
42,7%
Postgraduate (>16 years)
53
10,1%
Occupational status
Unemployed
63
12,5%
Employed
310
61,6%
Retired
102
19,4%
Household Worker
28
5,3%
Don’t Know/No answer
22
4,2%
Home ownership
Yes
380
72,4%
No
145
27,6%
Household income (€)
< 500
37
7,0%
500=1000
95
18,1%
1000=1500
103
19,6%
1500=2000
99
18,9%
2000=2500
84
16,0%
2500=3000
54
10,3%
> 3000
52
9,9%
No response
1
0,2%
Nationality
Greek
437
83,2%
Other
88
16,8%
Presence of health problems
Yes
196
37,3%
No
328
62,5%
Don’t Know/No answer
1
0,2%
Alcohol consumption
Yes
231
44,0%
No
294
56,0%
Alcohol frequency
Never/Rare
264
50,3%
1-3 times/month
85
16,2%
1-2 times/week
141
26,9%
3-4 times/week
22
4,2%
Almost every day
13
2,5%
Smoking habits
Non Smoker
344
65,5%
Former Smoker
39
7,4%
1-5 cigarettes/day
34
6,5%
Half package per day
53
10,1%
One package or more per day
55
10,5%
Table 1: Basic demographic and socioeconomic characteristics of the study population (n=525).
The estimated prevalence rates of screening for cervical cancer are relatively high among women living in Nicosia as 80.8% out of the 525 interviewed women had a smear test at least one time in their life, whereas 19.2% have never been screened (Table 1). The overall screening coverage meaning the percentage of women screened less than three years ago was 70.3% (Table 1).
In the multivariate analysis the parameter “Having been screened in the last 3 years (Up to 3 years Pap test)” was significantly associated with age, marital status, internet access at home, alcohol consumption, smoking habits, occupational status, educational status, health problems, household income and nationality (Table 2 and 3). Women aged 25-64 were more likely to have had a recent Pap test than younger or older, as well as married/partnered women compared to single and divorced or widowed. Further, women that were able to have access to internet from their home, were more likely to have had a recent Pap test. Women that indicated none or rare consumption of alcohol, no smokers, pensioner and unemployed women, women with lower education and with health problems were less likely to have had a recent Pap test. Compared to women with a monthly household income of <1000€, those with higher income were more likely to have had a recent Pap test.
Age group
(years)
Total
Ever Pap test
Up to 3 years Pap test
N
%
95% CI
N
%
95% CI
20-24
45
43
39,5
24,3
54,8
45
37,8
23,0
52,5
25-34
123
122
83,6
76,9
90,3
122
82,0
75,0
88,9
35-44
111
111
91,9
86,7
97,0
111
89,2
83,3
95,1
45-54
84
84
89,3
82,5
96,0
84
85,7
78,1
93,4
55-64
66
66
92,4
85,9
99,0
66
84,8
76,0
93,7
65-74
51
50
72,0
59,1
84,9
50
36,0
22,2
49,8
75+
45
45
62,2
47,5
77,0
41
7,3
-1,0
15,6
Total
525
521
80,8
77,4
84,2
519
70,3
66,4
74,3
Table 2: Screening history (ever cervical smear, up to 3 years cervical smear) by age group of respondent (n=525).
The outcome “Having been screened at least one time in their life (Ever Pap test)” was significantly associated with age, marital status, occupational status and household income and health problems (Table 3). Women aged 25-64 were more likely to have had a Pap test than younger and older, as well as married/partnered women compared to single and divorced or widowed. Unemployed and retired as well as women with health problems were less likely to have had a Pap test. Compared to women with a monthly household income of <1000€, those with higher income were more likely to have had a Pap test.
Ever vs. Never Pap test
Up to 3 years vs. Never Pap test
%
OR
(95% CI)
p-value
%
OR
(95% CI)
p-value
Age
20-24
39,5
1,00
37,8
1,00
25-34
83,6
8,59
(2,54 - 29,02)
,001
82,0
5,36
(1,83 - 15,74)
,002
35-44
91,9
18,40
(4,58 - 73,94)
,000
89,2
9,04
(2,71 - 30,2)
,000
45-54
89,3
7,52
(1,67 - 33,96)
,009
85,7
4,35
(1,18 - 16,08)
,028
55-64
92,4
14,18
(2,80 - 71,84)
,001
84,8
6,54
(1,64 - 26,11)
,008
65-74
72,0
1,72
(0,15 - 19,31)
,661
36,0
0,35
(0,04 - 3,3)
,361
75+
62,2
1,44
(0,12 - 17,04)
,772
7,3
0,08
(0,01 - 0,95)
,046
Marital status
Single
59,4
1,00
55,4
1,00
Married/partnered
92,4
10,59
(4,65 - 24,1)
,000
82,1
7,53
(3,5 - 16,2)
,000
Divorced/widowed
74,8
3,53
(1,37 - 9,07)
,009
55,6
2,82
(1,11 - 7,17)
,029
Educational status
Primary (<6 years)
70,4
1,00
29,4
1,00
Lower secondary (6-9 years)
78,3
1,18
(0,29 - 4,75)
,819
36,4
1,43
(0,37 - 5,5)
,602
Higher secondary (9-12 years)
82,1
0,86
(0,30 - 2,50)
,781
73,9
2,74
(1,01 - 7,41)
,047
Undergraduate (12-16 years)
83,0
1,02
(0,34 - 3,13)
,967
81,3
4,30
(1,52 - 12,16)
,006
Postgraduate (>16 years)
82,7
0,70
(0,16 - 3,08)
,638
80,8
3,20
(0,8 - 12,78)
,100
Occupational status
Unemployed
71,0
1,00
66,7
1,00
Employed
89,0
1,71
(0,68 - 4,31)
,253
85,8
1,65
(0,72 - 3,75)
,236
Retired
70,3
2,95
(0,33 - 26,62)
,336
29,9
3,77
(0,48 - 29,7)
,208
Household Worker
82,1
0,83
(0,17 - 4,08)
,817
75,0
1,60
(0,37 - 6,86)
,525
Household income
<500€
69,4
1,00
55,6
1,00
500=1000
69,5
1,16
(0,41 - 3,3)
,774
51,6
1,52
(0,51 - 4,58)
,455
1000=1500
85,3
3,12
(0,96 - 10,11)
,058
66,3
1,37
(0,45 - 4,19)
,586
1500=2000
81,4
1,15
(0,35 - 3,83)
,820
76,5
1,17
(0,36 - 3,83)
,796
2000=2500
84,5
1,98
(0,5 - 7,91)
,331
78,6
1,29
(0,36 - 4,68)
,694
2500=3000
90,7
2,80
(0,55 - 14,37)
,216
87,0
2,61
(0,59 - 11,61)
,208
>3000€
82,7
1,86
(0,42 - 8,18)
,412
78,8
1,78
(0,43 - 7,28)
,423
Presence of health problems
Yes
75,9
1,00
55,5
1,00
Table 3: Odds ratios of screening history (ever Pap test, up to 3 years Pap test) by socio demographic characteristics (n=525).
No
83,7
1,61
(0,76 - 3,42)
,217
78,9
1,16
(0,59 - 2,31)
,663
Nationality
Cypriot
81,1
1,00
68,9
1,00
Other
79,5
0,28
(0,11 - 0,70)
,007
77,3
0,43
(0,19 - 0,96)
,039
Alcohol frequency
Never/rare
77,2
1,00
1,00
1-3 times/month
82,4
1,61
(0,66 - 3,97)
,298
81,2
2,63
(1,12 - 6,18)
,027
1-2 times/week
85,0
2,07
(0,89 - 4,82)
,092
79,4
1,84
(0,88 - 3,85)
,108
3-4 times/week
90,5
14,30
(1,52 - 134,39)
,020
77,3
2,79
(0,63 - 12,3)
,176
Almost every day
83,3
1,65
(0,29 - 9,51)
,577
69,2
1,81
(0,34 - 9,71)
,489
Smoking habits
Non Smoker
78,3
1,00
64,6
1,00
Former Smoker
87,2
2,13
(0,60 - 7,54)
,241
79,5
2,02
(0,63 - 6,5)
,239
1-5 cigarettes/day
85,3
1,01
(0,30 - 3,45)
,982
85,3
1,76
(0,52 - 5,94)
,364
Half package per day
90,6
4,02
(1,17 - 13,82)
,027
86,5
2,80
(0,96 - 8,12)
,059
One package or more per day
79,6
1,24
(0,48 - 3,23)
,658
74,5
1,03
(0,44 - 2,44)
,939
Home ownership
No
77,1
1,00
72,0
1,00
Yes
82,2
0,89
(0,45 - 1,75)
,731
69,7
0,70
(0,35 - 1,39)
,312
Table 3 of 3:
Discussion
The estimated prevalence rates of screening for cervical cancer are relatively high among women living in Nicosia, as 70.3% of women had been tested in the previous three years. Population-based cervical cancer screening programs have been promoted by the Council of the European Union and the European Commission [11,12] but the periodicity and target groups vary among member states. Screening rates for cervical cancer in the United Kingdom, Sweden and Norway achieved high coverage, with close to 80% of the target population, whereas in the Slovak Republic and Hungary the screening rates are the lowest.
This study shows that women aged 25-64 are more likely to have had a recent Pap test, than younger or older age groups and this is possibly related to the fact that screening in Cyprus is recommended for women between 25 to 65 years [10,13]. The age limits and the frequency of the checks vary by country and health system. In Greece the program is aimed at women over 18 which calls for Pap test every 2, 3or 5years [13]. In Australia the program invites women 18-69 years for Pap test every 2 years, in Lithuania women aged 30-60 years are invited to check every 3 years and Sweden provides Pap test every 3 years for women aged 23-50 years and every 5 years for women aged 51-70 years old. The majority of the cervical cancer screening programs focuses at women aged 25-65 years (England, Wales, B. Ireland, Italy, France, Belgium, Hungary, Slovenia) [14,15].
Compared to women with a monthly household income of <500€, those with higher income were more likely to have had a Pap test. Household income has been found in multiple studies to be positively correlated with screening uptake, possibly due to greater financial freedom as a result of higher income [16-18]. In the city of Patras women with household income of at least 2,000€, were 3 to 4 times more likely to have been screened compared to those with lower household income [18].
In Cyprus, the public hospitals offer free Pap test for women in their gynecological departments, but long waiting lists most likely discourage them, especially women of lower socioeconomic status to access them [10], evidence also observed in Greece where the Greek NHS offers free cervical cancer screening [18]. In EU countries most programs are financially supported by government resources. Cervical screening is a free service of the National Health System in the United Kingdom, Wales and Northern Ireland [19].
Another relevant parameter seems to be the marital status. In this study married or partnered women were twice as likely to have been screened compared to single and divorced women. Married women may be more likely to visit a doctor for reproductive health; another explanation is the belief that only sexually active women need a smear test. Furthermore, the stigma associated with extramarital sexual activity in Cypriot culture may deter unmarried women from getting Pap smears. Married women have been found in many studies to be positively correlated with screening uptake [18-24]. Jelastopulu et al., reported that married women in the city of Patras were also twice as likely to have been screened compared to single and divorced women [18]. Also Nguyen et al., reported that Vietnamese-American married women aged =18 years living in Santa Clara County, California, and Harris County, Texas, were twice as likely to have been screened compared to single women [20] and Taylor et al., reported that Vietnamese-American married women aged =18 years living in Seattle community in Washington also screened twice for Pap test compared to single women [24].
Many previous studies have shown that women with lower education were less likely to have had a recent Pap test [18,25-30]. This relationship was evident in the present study too, since women with academic education were 3 to 4 times more likely to have had a Pap test compared to women with lower education. Olesenet al., reported that women with higher education were two times more likely to have had a Pap test compared to women with lower education, mainly due to higher education and consequently higher awareness [31].
Regarding the occupational status, the present study reveals that employed women were five times more likely to have had a Pap test compared to unemployed women, a finding that is seen in several other studies, albeit not in these magnitude [18,29-31]. In the crosssectional study of Olesen et al., with 1685 women from the Australian Capital Territory and Queanbeyan Australia, unemployed women were two times less likely to have had a smear test compared to employed [31] and similar results were seen in the cross-sectional survey on a total of 8570 randomly selected women aged 25 to 64 years in Abruzzo (Italy), conducted by De Vito et al., [29].
Furthermore, screening behavior seems to be influenced by nationality, since Greek Cypriot women were 3 to 4 times more likely to have had a Pap test compared to immigrant women from other countries. An analogue result was also found in the study of Fernandez et al., where foreign-born Hispanic women residing in the Washington DC metropolitan area obtain to lesser extent screening tests due to many barriers, such as language, competing priorities, and lack of knowledge about preventive screening methods [32].
In opposite to the results of Olesen, in the present study we did not seen any association between home ownership and higher rates of screening [31].
An interesting issue was that not heavy female smokers were more likely to have had a Pap test compared to non-smokers. However, this finding was also observed in several other studies [18,33-36]. Possibly smokers tend to be more aware about the consequences due to their hazardous habits and provide for the risk of cancer in better time.
Many studies indicate that the implementation of a population based organized screening program according to the EU guidelines lead to the decrease of the incidence of cervical cancer [37-39]. The Council of the EU has recommended implementation of populationbased cervical cancer screening programs to the EU member states, with quality assurance at all levels and in accordance with European guidelines [11]. Unfortunately no such programs exist in Cyprus up until now but there are plans to implement organized population based cervical cancer screening on a national basis and according to the European Guidelines for Quality Assurance for Cervical Cancer screening.
Conclusion
There are inequalities in cervical cancer screening in the city of Nicosia despite the subsidized costs of cervical cancer screening. Utilizing these findings local leaders have the ability to implement efforts to increase awareness in female risk groups in the community, i.e. older women, unmarried or single, with low education and low income. Community mobilization and health education are essential tools for overcoming common challenges that impede access to and utilization of preventive care. These common barriers include social taboos, lack of information and lack of transportation to service sites. Health education messages about cervical cancer should reflect the national policy and should be culturally appropriate and consistent at all levels of the health system.
Acknowledgement
We would like to thank all the women participating in this study.
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