Factors Associated with the Use of Pap Smear Testing in Greece

Abstract

Objective:

The purpose of this study was to describe the rate of Papanicolaou (Pap) smear test use among women participating in a breast cancer screening program in Greece and to determine related factors.

Methods:

Between March 2004 and July 2009, 9682 women aged between 40 and 69 years were recruited into the program. Baseline sociodemographic and lifestyle characteristics were recorded, together with familial medical history and the last time they had undergone a Pap test.

Results:

Almost 7% of the participants had never had a Pap test, and 28.8% had not had one within the last 3 years. Factors that were found to be independently associated with never receiving a Pap test or with not having one within the last 3 years included age, educational status, marital status, area of residence, health insurance, nationality, oral contraceptive use, cancer family history, body mass index (BMI), and stability of menstrual cycle.

Conclusions:

The rate of Pap test use is high among women who reside in Greece, although it is possible that this rate is a little overestimated. Specific programs should be developed and implemented that aim to increase awareness of the benefits of regular cervical cancer screening among specific subgroups of women.

Introduction

Cervical cancer is still a common cancer and an important cause of mortality in Europe and the United States.^1,2 In European countries, estimates for the year 2004 showed that almost 34,500 women in the European Union (EU) developed this disease, and about 16,500 died from it.¹ The incidence and mortality rates ranged from 4.7/100,000 and 1.1/100,000, respectively, in Finland to >16/100,000 and 10/100,000, respectively, in Lithuania.¹ In Greece, the corresponding rates were estimated at about 8.9/100,000 and 3.9/100,000, respectively, indicating that cervical cancer constitutes a considerable public health problem in this country.¹ Over the past decades, a significant reduction has been detected in cervical cancer mortality rates, specifically in the old member states of EU. However, it should be noted that in other European countries, these rates have remained constant, have decreased nonsignificantly, or have increased.³

Several studies have shown that organized screening programs using the Papanicolaou (Pap) smear test, which is a well-established cervical cancer screening tool, are effective in decreasing the incidence and mortality of this disease.^4,5 Moreover, an effect of nonorganized screening on cervical cancer rates has been shown, although not of the same magnitude.^6
–8 This may be attributed to the fact that a considerable proportion of women with specific sociodemographic and other characteristics may be underscreened. It has been shown that uninsured women, those with a low annual income, and those with very low educational status are less likely to undergo a Pap test on a regular basis in several populations.^9

–13

The European guidelines for quality assurance in cervical cancer screening recommend an age range beginning at 20–30 years and extending to 60–65 years, with a 3-year or 5-year screening interval.¹⁴ The American Cancer Society (ACS) guidelines recommend that women aged >30 years who have had three normal Pap test results in a row may be screened every 2–3 years.¹⁵

In Greece, there is a lack of published data about the proportion of women who follow the European recommended guidelines for Pap testing and the factors that determine women's behavior in this respect. Therefore, the aim of this work was to quantify the rates of Pap test use and to investigate the factors related to the use of this cervical cancer screening tool among women residing in Greece. The data and the conclusions derived from this study may be used to help health policymakers in this area to design intervention programs to improve women's cervical cancer screening behaviors, which may improve health outcomes over time.

Materials and Methods

Data for this study come from a Breast Cancer Screening Programme organised by the nongovernmental organization, Friends of General Oncology Hospital “Agioi Anargyroi” and the General Oncology Hospital “Agioi Anargyroi,” located in Athens, Greece.

Study population

This is an ongoing program initiated in March 2004. Until July 2009, 9682 women aged between 40 and 69 were enrolled on a voluntary basis. At this point, it should be mentioned that this age group (i.e., 40–69 years) only partly overlaps with the target group for cervical cancer screening, which in most EU countries is 25–64 years. The participating women were residents of two adjacent administrative regions of Greece: Attica, the most populous region in the country, and Voiotia. A previous diagnosis of breast cancer, mastectomy, and mammography within the last 12 months were considered as exclusion criteria of this screening program. Women were informed about the screening program through TV and radio advertisements, by advertisements in newspapers and magazines, and by friends and relatives. The aims, design, and ethics of the present screening program have been approved by the Institutional Review Board of the General Oncology Hospital “Agioi Anargyroi.”

Data collection

A structured questionnaire developed specifically for the purposes of the current study was used to retrieve several data from women. This questionnaire was used during scheduled interviews conducted when each woman had her first free mammography screening. In particular, women were asked to report their age (divided into six groups: 40–44, 45–49, 50–54, 55–59, 60–64, 65–69 years old), marital status (married, single, divorced/separated, or widowed), educational status (years of education), nationality (Greek; Albanian and Bulgarian, which represent the majority of immigrants in Greece; other immigrants), area of residence (urban, rural), occupational status (housewife, retired, unemployed, self-employed, servant, manual worker, employee in healthcare sector, employee in education and training sector, other), health insurance (Social Insurance Institute [IKA], Organization of Agricultural Insurance [OGA], Fund for Merchants, Manufacturers and Small Businessmen [OAEE] and Organisation for Care and Insurance of Public Sector [OPAD]—which cover almost the entire population—uninsured, other), number of deliveries, and number of abortions. In addition, women's body mass index (BMI) scores (kg/m²) were calculated as the ratio of self-reported weight (kg) to height (m). Based on these values, women were divided into normal weight (18.5 < BMI < 25 kg/m²), overweight (25 < BMI < 29.9 kg/m²), and obese (BMI > 29.9 kg/m²).

Women were asked to report if there was any cancer history in their family and were asked for information about the stability of their menstrual cycle, the use of oral contraceptives, their smoking habits (nonsmoker, former smoker, current smoker), and alcohol consumption. They were requested to report if they had had a mammography before their enrollment in the current screening program and if they had ever performed breast self-examination (BSE). Finally, women were asked to state the last time they had undergone a Pap test. The potential answers to this question were: never, sometimes, 6 months ago, 1 year ago, 2 years ago, 3 years ago, more than 3 years ago. Based on this answer, women were divided into those who never had a Pap test and the rest, who were subdivided into those who had a Pap test within the last 3 years and those who had one longer than 3 years ago.

Statistical analysis

Categorical variables are presented as relative frequencies (%). The chi-square test without the correction of continuity was used to evaluate the associations between categorical variables. Simple logistic regression analyses were conducted to examine the relation between several factors (i.e., sociodemographic characteristics, individual medical history, family history of cancer, and lifestyle characteristics) and the probability of (1) not having had any previous Pap test and (2) not having had a Pap test within the past 3 years (dependent variables). In addition, the factors that are independently related to the dependent variables were determined through stepwise backward logistic regression analysis. Factors that were found to be significantly associated with the dependent variables in the simple analyses were used as independent variables in the initial logistic regression models. From all these analyses, odds ratios (ORs) with 95% confidence intervals (CIs) were derived. The final models were tested for goodness of fit using the Hosmer-Lemeshow statistic.¹⁶ A probability value of 5% was considered as statistically significant. All statistical calculations were performed using SPSS version 14.0 software (SPSS Inc, Chicago, IL).

Results

Characteristics of participants

The sociodemographic characteristics, as well as other health-related variables of the women who participated in the program, are summarized in Table 1. Regarding educational status, 33.6% of the participants had <6 years of education, and 42% had <12. The vast majority of participants were Greek (91.3%), married (78.8%), and inhabitants of urban regions (74.9%). The main occupational categories were housewives (38.9%), retired (14.3%), or servants (12.2%). Only 6.4% of the sample were uninsured. Of the participants questioned, 44.4% reported they had a family history of cancer in general. Only 38.8% had normal weight, and 10.6%, 15.5%, and 53.1% had none, one, and two deliveries, respectively. Almost 40.0% had never had an abortion, and only 4.1% claimed to have a stable menstrual cycle. Finally, 38.0% of participants had never undergone mammography before their enrollment in the study screening program, and almost 32% of women reported they had never performed BSE. Although it was expected (from the design of the current study) that this sample would not be representative of the population of these two Greek regions, it transpired that our sample was almost representative in terms of age and marital status but not in terms of educational status; we found that the educational status of the study population was better than that of the total population.

Table 1.

Study Population Characteristics (n = 9682)

Characteristic	% of sample	% of whole population ^*
Age (years)
40–44	20.5	20.3
45–49	20.6	19.8
50–54	19.0	19.0
55–59	17.2	15.9
60–64	13.2	13.0
65–69	9.5	12.0
Educational status (years)
Very low (≤6)	33.6	45.1
Low (6–12)	42.0	36.8
Moderate (12–14)	5.9	3.7
High (14–16)	13.6	13.4
Very high (>16)	5.1	0.9
Marital status
Married	78.8	75.3
Single	5.0	6.5
Divorced/separated	8.9	9.6
Widowed	7.3	8.5
Area of residence
Urban	74.9
Rural	25.1
Nationality
Greek	91.3
Albanian	3.8
Bulgarian	1.5
Other	3.4
Occupational status
Housewife	38.9
Retired	14.3
Servant	12.2
Healthcare professionals	1.3
Unemployed	1.3
Education and training occupations	3.1
Manual worker	12.5
Self-employed	5.0
Other	11.6
Health insurance status
OGA	13.6
IKA	56.0
OAEE	7.6
OPAD	7.1
Uninsured	6.4
Other	9.4
Smoking habits
Nonsmoker	56.3
Former smoker	8.2
Current smoker	35.5
Alcohol consumption
No	86.2
Yes	13.8
Oral contraceptive use
No	81.6
Yes	18.4
Family history of cancer
No	55.6
Yes	44.4
BMI
Normal weight	38.8
Overweight	37.2
Obese	24.1
Number of deliveries
0	10.6
1	15.5
2	53.1
3	16.3
≥4	4.5
Number of abortions
0	42.0
1	21.7
2	17.7
3	8.8
4	3.9
≥5	5.8
Last mammography
Never	38.0
Earlier than 2 years ago	36.8
Within the last 2 years	25.2
Frequency of breast self-examination
Never	32.0
Occasionally	19.5
Once/6 months	0.9
Once/2 months	8.4
Once/1 month	39.2
Menstrual cycle stability
Always stable	4.1
Usually stable	16.5
Never stable	79.4

BMI, body mass index; IKA, Social Insurance Institute; OAEE, Fund for Merchants, Manufacturers and Small Businessmen; OGA, Organization of Agricultural Insurance; OPAD, Organisation for Care and Insurance of Public Sector.

Based on Census of 2001.

Factors associated Pap testing

Of the 9682 participants, 6.6% never had a Pap test, 6.4% reported they had one sometime, 15.8% had one >3 years ago, 5.3% had one 3 years ago, 14.5% had one 2 years ago, and 51.2% had one within the last year. Tables 2 and 3 depict the percentages of women in each of the questionnaire's subcategories who never had a previous Pap test (Table 2) and those of women who had not undergone one within the last 3 years (Table 3), together with the results from univariate and multiple logistic regression analysis. It was observed that the percentage of women who never had a previous Pap test or not had one within the last 3 years increased with age (p < 0.001). Moreover, it was found that women with a very low or very high educational level, residents of rural areas, immigrants, uninsured, insured with OGA, nonsmokers, overweight women, obese women, those with more than four pregnancies, those who had always had a stable menstrual cycle, those who had never taken oral contraceptives, those who had not had mammography before their recruitment into the current program, those who declared they had never performed BSE, and those without a general family history of cancer were more likely to have had no previous Pap test or to have not had one within the last 3 years, compared with their counterparts. Finally, manual workers were more likely to have never had a Pap test, and retired women were more likely to have not undergone one within the last 3 years, compared with women in the remaining occupations.

Table 2.

Percentages of Women in Each Questionnaire Subcategory Who Had Never Had a Pap Test, and Results from Univariate and Multiple Logistic Regression (N = 9,682)

Characteristics	% of sample	Unadjusted OR (95% CI)	Adjusted OR (95% CI)
Age (years)
40–44	4.5^*	1.00	1.00
45–49	4.8	1.06 (0.79-1.44)	0.95 (0.70-1.31)
50–54	6.4	1.45 (1.09-1.93)	1.29 (0.95-1.76)
55–59	7.3	1.68 (1.27-2.23)	1.37 (0.99-1.89)
60–64	7.6	1.76 (1.31-2.38)	1.29 (0.91-1.84)
65–69	13.2	3.26 (2.45-4.34)	2.48 (1.71-3.59)
Educational status (years)
≤6	9.1^*	1.00	1.00
6–12	4.7	0.50 (0.41-0.60)	0.65 (0.52-0.82)
12–14	4.8	0.50 (0.33-0.75)	0.81 (0.52-1.28)
14–16	4.4	0.46 (0.34-0.62)	0.68 (0.48-0.98)
>16	14.1	1.65 (1.24-2.18)	1.26 (0.91-1.76)
Marital status
Married	6.0^*	1.00	1.00
Single	8.4	1.44 (1.03-2.01)	2.33 (1.44-3.76)
Divorced/separated	6.2	1.03 (0.77-1.39)	1.35 (0.96-1.89)
Widowed	12.6	2.27 (1.78-2.89)	1.64 (1.24-2.15)
Area of residence
Urban	4.6^*	1.00	1.00
Rural	12.6	2.97 (2.53-3.50)	2.94 (2.33-3.70)
Nationality
Greek	5.8^*	1.00	1.00
Albanian	15.8	3.06 (2.27-4.12)	3.99 (2.71-5.89)
Bulgarian	18.6	3.73 (2.43-5.73)	4.90 (2.90-8.27)
Other	14.0	2.66 (1.92-3.68)	3.69 (2.46-5.52)
Occupational status
Housewife	6.3^*	1.00
Retired	8.5	1.38 (1.09-1.73)
Servant	2.0	0.31 (0.20-0.47)
Healthcare professional	4.7	0.73 (0.32-1.68)
Unemployed	4.1	0.63 (0.26-1.56)	-
Education and training occupations	2.4	0.36 (0.17-0.77)
Manual worker	11.5	1.93 (1.55-2.40)
Self-employed	5.2	0.81 (0.53-1.24)
Other	7.3	1.19 (0.91-1.53)	-
Health insurance
OGA	12.5^*	1.00	1.00
IKA	5.6	0.41 (0.34-0.51)	0.99 (0.76-1.29)
OAEE	3.8	0.28 (0.18-0.42)	0.72 (0.45-1.18)
OPAD	3.7	0.27 (0.17-0.41)	0.98 (0.60-1.61)
Uninsured	12.9	1.03 (0.77-1.37)	1.89 (1.29-2.76)
Other	4.4	0.32 (0.23-0.46)	0.99 (0.66-1.50)
Smoking habits
Nonsmoker	8.2^*	1.00
Former smoker	4.4	0.51 (0.36-0.73)	-
Current smoker	4.6	0.54 (0.45-0.65)
Alcohol consumption
No	6.9^*	1.00	-
Yes	5.2	0.74 (0.57-0.96)
Oral contraceptive use
No	7.4^*	1.00	1.00
Yes	2.9	0.37 (0.27-0.49)	0.57 (0.42-0.77)
Family history of cancer
No	7.8^*	1.00	1.00
Yes	5.2	0.64 (0.54-0.76)	0.77 (0.64-0.92)
BMI
Normal weight	4.9^*	1.00	1.00
Overweight	6.9	1.43 (1.17-1.74)	1.04 (0.84-1.29)
Obese	8.8	1.86 (1.51-2.29)	1.37 (1.09-1.72)
Number of deliveries
0	7.2^*	1.00
1	5.5	0.76 (0.54-1.05)
2	5.8	0.79 (0.60-1.04)	-
3	8.0	1.13 (0.83-1.53)
≥4	14.6	2.23 (1.55-3.20)
Number of abortions
0	8.4^*	1.00
1	5.8	0.67 (0.54-0.83)
2	5.0	0.57 (0.45-0.73)	-
3	4.3	0.49 (0.35-0.70)
4	8.0	0.95 (0.65-1.41)
≥5	5.1	0.59 (0.40-0.87)
Last mammography
Never	13.9^*	1.00	1.00
At least some time	2.2	0.14 (0.11-0.17)	0.14 (0.11-0.17)
Frequency of breast self-examination
Never	7.4^*	1.00	-
At least some time	6.3	0.84 (0.71-0.99)
Menstrual cycle stability
Always stable	8.6^*	1.00	1.00
Usually stable	5.3	0.60 (0.39-0.91)	0.62 (0.40-0.96)
Never stable	6.7	0.76 (0.53-1.10)	0.68 (0.46-1.00)

Numbers in bold indicate statistical significance.

p < 0.05.

CI, confidence interval; OR, odds ratio.

Table 3.

Percentages of Women in Each Questionnaire Subcategory Who Had Not Had a Pap Test Within Last 3 Years, and Results from Univariate and Multiple Logistic Regression (n = 9682)

Characteristics	% of sample	Unadjusted OR (95% CI)	Adjusted OR (95% CI)
Age (years)
40–44	15.2^*	1.00	1.00
45–49	20.0	1.39 (1.18-1.64)	1.32 (1.11-1.57)
50–54	26.5	2.01 (1.71-2.36)	1.84 (1.55-2.18)
55–59	33.8	2.85 (2.43-3.34)	2.49 (2.08-2.97)
60–64	43.3	4.24 (3.60-5.01)	3.49 (2.88-4.22)
65–69	53.2	6.33 (5.29-7.56)	5.28 (4.25-6.55)
Educational status (years)
≤6	37.0^*	1.00	1.00
6–12	24.4	0.55 (0.49-0.61)	0.88 (0.78-0.99)
12–14	22.2	0.48 (0.39-0.60)	0.92 (0.73-1.16)
14–16	20.9	0.45 (0.39-0.52)	0.88 (0.73-1.06)
>16	41.4	1.21 (0.99-1.46)	1.16 (0.93-1.45)
Marital status
Married	27.9^*	1.00	1.00
Single	26.3	0.92 (0.75-1.13)	1.41 (1.06-1.87)
Divorced/separated	26.6	0.94 (0.80-1.10)	1.24 (1.04-1.48)
Widowed	43.1	1.96 (1.67-2.29)	1.30 (1.09-1.54)
Area of residence
Urban	24.8^*	1.00	1.00
Rural	41.1	2.11 (1.92-2.33)	1.72 (1.51-1.96)
Nationality
Greek	28.4^*	1.00	1.00
Albanian	34.6	1.34 (1.07-1.67)	2.08 (1.60-2.70)
Bulgarian	33.8	1.29 (0.91-1.82)	1.70 (1.15-2.51)
Other	32.0	1.19 (0.94-1.51)	1.69 (1.29-2.21)
Occupational status
Housewife	30.6^*	1.00
Retired	40.5	1.54 (1.36-1.75)
Servant	14.7	0.39 (0.33-0.47)
Healthcare professional	23.4	0.69 (0.46-1.05)
Unemployed	17.9	0.49 (0.31-0.79)	-
Education and training occupations	14.2	0.38 (0.27-0.52)
Manual worker	28.4	0.90 (0.78-1.03)
Self-employed	27.4	0.86 (0.69-1.06)
Other	30.3	0.98 (0.85-1.14)
Type of health insurance
OGA	43.8^*	1.00	1.00
IKA	26.3	0.46 (0.40-0.52)	0.96 (0.82-1.14)
OAEE	25.5	0.44 (0.36-0.54)	1.00 (0.79-1.28)
OPAD	21.4	0.35 (0.28-0.43)	0.86 (0.66-1.10)
Uninsured	35.3	0.70 (0.57-0.85)	1.47 (1.15-1.87)
Other	26.0	0.45 (0.38-0.54)	0.98 (0.79-1.23)
Smoking habits
Nonsmoker	32.5^*	1.00
Former smoker	26.6	0.75 (0.64-0.89)	-
Current smoker	23.4	0.64 (0.58-0.70)
Alcohol consumption
No	29.2	1.00	-
Yes	26.6	0.88 (0.77-1.00)
Oral contraceptive intake
No	30.8^*	1.00	1.00
Yes	20.1	0.56 (0.50-0.64)	0.80 (0.69-0.91)
Family history of cancer
No	30.5^*	1.00	-
Yes	26.7	0.83 (0.76-0.91)
BMI
Normal weight	21.5^*	1.00	1.00
Overweight	30.6	1.62 (1.45-1.80)	1.19 (1.06-1.33)
Obese	37.8	2.21 (1.97-2.48)	1.63 (1.44-1.85)
Number of deliveries
0	27.4^*	1.00	1.00
1	23.8	0.83 (0.68-0.99)	0.88 (0.70-1.12)
2	27.7	1.01 (0.87-1.18)	0.92 (0.74-1.13)
3	34.1	1.37 (1.15-1.63)	1.00 (0.80-1.27)
≥4	43.5	2.03 (1.61-2.57)	1.38 (1.04-1.84)
Number of abortions
0	31.7^*	1.00
1	26.8	0.79 (0.70-0.89)
2	25.6	0.74 (0.65-0.84)	-
3	25.9	0.75 (0.64-0.89)
4	30.1	0.93 (0.74-1.17)
≥5	29.4	0.89 (0.74-1.08)
Last mammography
Never	40.5^*	1.00	1.00
At least some time	21.7	0.41 (0.37-0.44)	0.32 (0.28-0.35)
Frequency of breast self-examination
Never	30.7^*	1.00	-
At least some time	27.9	0.87 (0.80-0.96)
Menstrual cycle stability
Always stable	36.5	1.00	1.00
Usually stable	26.6	0.63 (0.50-0.80)	0.72 (0.56-0.93)
Never stable	28.7	0.70 (0.56-0.87)	0.69 (0.55-0.66)

Numbers in bold indicate statistical significance.

p < 0.05.

Sociodemographic factors found to be independently associated with the probability of not having any Pap test included age, educational status, marital status, area of residence, health insurance, and nationality. In addition, several health-related variables, such as oral contraceptive use, cancer family history, elevated BMI, stability of menstrual cycle, and the use of mammography, were independently related to the probability of never having a Pap test (Table 2). The same factors, together with the number of pregnancies, were found to be independently associated with the probability of not having a Pap test within the last 3 years (Table 3).

Discussion

The purpose of the present study was to examine the use of the Pap smear test among women participating in breast cancer screening in Greece and to determine the factors related to this cervical cancer screening method. This topic has been extensively investigated among several populations in the United States, Europe, and other countries.^{10,11,17

–30} However, there are no data from Greece, as this is the first study of its kind in this country.

The findings of the current study revealed that almost 93% of the participating women had a Pap test at some time. Among those women, almost 76% had one within the last 3 years, and approximately 55% had one within the last 1 year. These rates are almost equal to or higher than those reported in studies conducted in other populations.^{10,11,17

–27} In particular, Puig-Tintore et al.²⁸ reported that almost 76% of women aged 18–65 years in Spain had undergone a Pap test in the last 3 years. Much lower (almost 50%) was the percentage of French women aged 18–70 years who had a Pap test in the past 3 years.²⁹ The discrepancies in the aforementioned rates may be accounted for by differences in study design; sample characteristics, such as age, race, ethnicity, socioeconomic status; or the level of knowledge about the importance of having regular cervical screening. The high rates of Pap test use among women participating in a breast cancer screening in Greece may reflect the high awareness of women about the benefits of having a regular cervical cancer screening. However, this does not mean that there is not a need to develop national cervical cancer screening programs, as it was found that the underscreening rate exceeds 30% among specific subpopulations of the current study.

Several sociodemographic characteristics were found to be independently related to Pap test use (i.e., age, educational status, marital status, health insurance, nationality, area of residence). In particular, we found that older women were less likely to have undergone a Pap test ever or within the last 3 years. These results are in line with those from previous studies.^{10,19,26
–28} At this point, however, it should be mentioned that women aged 65 + do not belong to the target age group for cervical cancer screening. Moreover, it is possible that a large number of women after the age of 45 years have undergone hysterectomy. Therefore, it is reasonable that the percentage of women who have not undergone a Pap test within the last 3 years is higher among women aged 65–69 years. It was found that immigrants were less likely to have undergone a Pap test (ever or within the last 3 years) compared with Greek women who participate in a breast cancer screening program. This could be attributed to the fact that these women might have limited access to medical care because of their low socioeconomic status; they may not have health insurance to cover the cost of a Pap test. This potential explanation is supported by the finding in the current and previous studies indicating that lack of health insurance is associated with lower rates of Pap test use.^10,11,20,23 A further explanation may be the inability of immigrant women to communicate properly with healthcare providers in Greece because of language barriers.

It was found that women with <6 years of education were less likely to undergo a Pap test compared with those with 6–16 years of education. This finding is in agreement with those reported by other investigators.^{19,23,25
–27,31} The lack of knowledge of cervical cancer risk factors and the benefits of having regular cervical cancer screening to reduce cervical cancer-related mortality and morbidity may account for the low use of the Pap test among poorly educated women.^25,32 Paradoxically, however, it was found that women with very high levels of education (>16 years of education) were less likely to have ever had a Pap test or to have had one within the last 3 years before their enrollment in this screening program compared with the rest of the women. As far as we know, this is the first study to detect such an association. In the vast majority of previous studies, however, women with >12 years of education were included in the highest educational level, whereas in the current study, women with a master's degree or Ph.D. were classified in a different category from those with standard college studies. When a different categorization (<6 years, 6–12 years, and >12 years) was used in this study, the percentage of women not having had a Pap test within the last 3 years was significantly higher in the first category (37%) compared with the third category (25.5%). Women with very high educational status may have increased occupational responsibilities, resulting in a lack of time for use of preventive services on a regular basis.

Two additional demographic factors found to be significantly associated with the use of the Pap test were marital status and area of residence. It was found that women who were living in rural regions were less likely to have undergone a Pap test; this finding confirms the results of previous studies.^24,28,33 Limited access to medical care providers because of the small number of physicians or health care centers may account for this finding.³³ In addition, we detected that married women are more likely than other women to be screened through a Pap test. There is no consensus in the findings of previous works about the effect of marital status on Pap test use.^{9,19,20,25,31,34} Therefore, further research should be conducted to examine this association.

Finally, the current results revealed a significant association between established cervical cancer risk factors and Pap test use. We observed that women with a family history of any type of cancer, those who used oral contraceptives, and former or current smokers were more likely to have had a Pap test at some time or within the last 3 years. These findings may indicate that women with these risk factors are more likely to be counseled by their healthcare provider about the importance of having regular cervical cancer screenings to increase the likelihood of early detection of cervical cancer and, consequently, to improve the prognosis and health outcomes.

These results should be considered in the light of the study's design limitations. First, although a large sample of volunteers was recruited into the current study, they do not adequately represent the entire female population of the two geographical regions or the entire country. Thus, the findings should be generalized with some caution to the overall Greek population. Second, the outcome variable (use of Pap test) was measured by self-report from women who participate voluntarily in a breast cancer screening program. Therefore, it is probable that the percentage of Pap test use is overestimated because of recall bias³⁵ and because of correlation between attendance in mammography screening and in cytological cervical cancer screening. Third, the age range of the study population does not include the youngest half of the population for whom organized screening for cervical cancer is recommended. Finally, other factors that may be significant determinants of cervical cancer screening use were not recorded in the current study. For instance, Pap test recommendation by a healthcare provider, family history of cervical cancer, age at first sexual intercourse, and knowledge and attitudes about cervical cancer risk factors and the benefits of the Pap test were not recorded.

Conclusions

The results of the present study indicate that the rate of Pap test use is high among women who reside in Greece, although it is possible that this rate is somewhat overestimated because Pap test use is self-reported and data are obtained from women voluntarily participating in a breast cancer screening. Moreover, it was found that this rate needs to be improved in older women, immigrants, the unmarried, inhabitants of rural areas, those having very high or very low educational status, those without health insurance, those without a previous mammography, and those without cervical cancer risk factors (e.g., those without a family history of cancer, many pregnancies, no oral contraceptive use, nonsmokers). These findings highlight the need to develop and implement policies and programs aimed at raising awareness of these women about the benefits of having a regular cervical cancer screening through a Pap test. Local and nationwide public programs that will provide free or low-cost cervical cancer screening should be organized. Finally, although the estimation of cervical cancer screening coverage is biased, the factors determining attendance are probably reliable.

Footnotes

Acknowledgments

We thank the members of the board of directors of the non-governmental organization, Friends of General Oncology Hospital “Agioi Anargyroi,” M. Grigoropoulou, V. Spyrou, G. Kourti, A. Xrisostali, and M. Pantazi, as well as S. Lampadari, for their contribution to the completion of the study.

Disclosure Statement

The authors have no conflicts of interest to report.

References

Arbyn

, Raifu

, Autier

, Ferlay

. Burden of cervical cancer in Europe: Estimates for 2004. Ann Oncol, 2007; 18:1708–1715.

National Cancer Institute. Surveillance, epidemiology, and end results. SEER cancer statistics. Incidence of cervix uteri cancer, 2009. http://seer.cancer.gov/statfacts/html/cervix.html. 2009 11 18.

Arbyn

, Raifu

, Weiderpass

, Bray

, Anttila

. Trends of cervical cancer mortality in the member states of the European Union. Eur J Cancer, 2009; 45:2640–2648.

International Agency for Research on Cancer. Screening for cancer of the uterine cervix. From the IARC working group on cervical cancer screening and the UICC project group on the evaluation of screening programmes for cancer. IARC Sci Publ, 1986; 1–315.

International Agency for Research on Cancer. IARC/WHO handbooks of cancer prevention: Cervix cancer screening. Lyon: IARC Press, 2005.

Magnus

, Langmark

, Andersen

. Mass screening for cervical cancer in Ostfold county of Norway 1959–77. Int J Cancer, 1987; 39:311–316.

Nieminen

, Kallio

, Anttila

, Hakama

. Organised vs. spontaneous Pap smear screening for cervical cancer: A case-control study. Int J Cancer, 1999; 83:55–58.

Ronco

, Pilutti

, Patriarca

et al. Impact of the introduction of organised screening for cervical cancer in Turin, Italy: Cancer incidence by screening history 1992–98. Br J Cancer, 2005; 93:376–378.

Arbyn

, Quataert

, Van Hal

, Van Oyen

. Cervical cancer screening in the Flemish region (Belgium): Measurement of the attendance rate by telephone interview. Eur J Cancer Prev, 1997; 6:389–398.

10.

Bazargan

, Bazargan

, Farooq

, Baker

. Correlates of cervical cancer screening among underserved Hispanic and African-American women. Prev Med, 2004; 39:465–473.

11.

Sambamoorthi

, McAlpine

. Racial, ethnic, socioeconomic, and access disparities in the use of preventive services among women. Prev Med, 2003; 37:475–484.

12.

Hiatt

, Pasick

, Stewart

et al. Community-based cancer screening for underserved women: Design and baseline findings from the Breast and Cervical Cancer Intervention Study. Prev Med, 2001; 33:190–203.

13.

Jennings-Dozier

, Lawrence

. Sociodemographic predictors of adherence to annual cervical cancer screening in minority women. Cancer Nurs, 2000; 23:350–356.

14.

Arbyn

, Anttila

, Jordan

et al. European guidelines for quality assurance in cervical cancer screening, 2nd. Luxembourg: Office for Official Publications of the European Communities, 2008.

15.

American Cancer Society. American Cancer Society guidelines for the early detection of cancer. http://www.cancer.org/docroot/ped/content/ped_2_3X_acs_cancer_detection.guidelines_36.asp. 2009 11 17.

16.

Hosmer

, Lemeshow

. Applied logistic regression, 2nd. New York: Wiley Interscience, 2000.

17.

Uysal

, Birsel

. Knowledge about cervical cancer risk factors and Pap testing behaviour among Turkish women. Asian Pac J Cancer Prev, 2009; 10:345–350.

18.

Taylor

, Yasui

, Nguyen

et al. Pap smear receipt among Vietnamese immigrants: The importance of health care factors. Ethn Health, 2009; 14:575–589.

19.

Martins

, Valente

, Thuler

. Factors related to inadequate cervical cancer screening in two Brazilian state capitals. Rev Saude Publica, 2009; 43:318–325.

20.

, Toubbeh

, Wang

, Shive

, Cooper

, Pham

. Factors associated with cervical cancer screening compliance and noncompliance among Chinese, Korean, Vietnamese, and Cambodian women. J Natl Med Assoc, 2009; 101:541–551.

21.

, Taylor

, Burke

, Yasui

, Schwartz

, Jackson

. Knowledge about cervical cancer risk factors, traditional health beliefs, and Pap testing among Vietnamese American women. J Immigr Minor Health, 2007; 9:109–114.

22.

Bessler

, Aung

, Jolly

. Factors affecting uptake of cervical cancer screening among clinic attendees in Trelawny, Jamaica. Cancer Control, 2007; 14:396–404.

23.

Islam

, Kwon

, Senie

, Kathuria

. Breast and cervical cancer screening among South Asian women in New York City. J Immigr Minor Health, 2006; 8:211–221.

24.

Johnston

, Boyd

, MacIsaac

. Community-based cultural predictors of Pap smear screening in Nova Scotia. Can J Public Health, 2004; 95:95–98.

25.

Siahpush

, Singh

. Sociodemographic predictors of Pap test receipt, currency and knowledge among Australian women. Prev Med, 2002; 35:362–368.

26.

Chan

, Ho

, Chan

, Yip

, Wong

, Cheng

. Factors affecting uptake of cervical and breast cancer screening among perimenopausal women in Hong Kong. Hong Kong Med J, 2002; 8:334–341.

27.

Maxwell

, Bancej

, Snider

, Vik

. Factors important in promoting cervical cancer screening among Canadian women: Findings from the 1996–97 National Population Health Survey (NPHS) Can J Public Health, 2001; 92:127–133.

28.

Puig-Tintore

, Castellsague

, Torne

et al. Coverage and factors associated with cervical cancer screening: Results from the AFRODITA study: A population-based survey in Spain. J Low Genit Tract Dis, 2008; 12:82–89.

29.

Grange

, Malvy

, Lancon

, Gaudin

, El Hasnaoui

. Factors associated with regular cervical cancer screening. Int J Gynaecol Obstet, 2008; 102:28–33.

30.

von Karsa

, Anttila

, Ronco G

, Malila

, Arbyn

. Cancer screening in the European Union: Report on the implementation of the Council Recommendation on cancer screening. Luxembourg: Office for Official Publications of the European Communities, 2008; 1–118.

31.

Nguyen

, McPhee

, Nguyen

, Lam

, Mock

. Predictors of cervical Pap smear screening awareness, intention, and receipt among Vietnamese-American women. Am J Prev Med, 2002; 23:207–214.

32.

Hislop

, Teh

, Lai

, Ralston

, Shu

, Taylor

. Pap screening and knowledge of risk factors for cervical cancer in Chinese women in British Columbia, Canada. Ethn Health, 2004; 9:267–281.

33.

Coughlin

, Leadbetter

, Richards

, Sabatino

. Contextual analysis of breast and cervical cancer screening and factors associated with health care access among United States women, 2002. Soc Sci Med, 2008; 66:260–275.

34.

Chee

, Rashidah

, Shamsuddin

, Intan

. Factors related to the practice of breast self examination (BSE) and Pap smear screening among Malaysian women workers in selected electronics factories. BMC Womens Health, 2003; 3:3.

35.

Arbyn

, Simoens

, Van Oyen

et al.

Analysis of 13 million individual patient records pertaining to Pap smears, colposcopies, biopsies and surgery on the uterine cervix (Belgium, 1996–2000)

Prev Med, 2009; 48:438–443.