Trend in cervical cancer screening in Spain
(2003–2009) and predictors of adherence

Rocı´o Martı´n-Lo´pez, Valentı´n Herna´ndez-Barrera, Ana Lopez de Andres,
Pilar Carrasco-Garrido, Angel Gil de Miguel and Rodrigo Jimenez-Garcia

Cervical cancer remains a public health problem in
developed countries. Early detection of both premalignant

lesions and cervical cancer through an appropriate
screening programme may decrease its incidence and

mortality. High rates of participation are essential to ensure
the desired impact on the population. The aims of this

study were to assess the use of Pap smears in Spain in
2009 to identify factors associated with screening

adherence (predictors) and assess the trend from 2003 to
2009. We included women surveyed in the European Health

Interview Survey for Spain. Cervical cancer screening
included self-reported Pap smears over the last 3 years.

The target age range was 25–64 years. The following
independent variables were analysed: sociodemographic

variables, chronic conditions, and lifestyle. Predictors of
Pap smear adherence were explored using multivariate

logistic regression. The screening coverage in the target
population was 66.1% (95% confidence interval: 64.8–67.4).

Undergoing Pap smears was associated positively with the
following: being married, higher levels of education and
income, having visited a general practitioner in previous

weeks, and suffering from musculoskeletal disease.

Belonging to an older age group (55–64 years) and obesity
were associated with nonadherence to Pap smears. We did

not find significant differences when we compared cervical
cancer screening adherence over time since 2003.

Adherence to cervical cancer screening in Spain does not
seem to be improving. An effort must be made, and the

implementation of population-based programmes instead
of opportunistic screening could be considered, to recruit

women who are less likely to undergo screening.

European Journal of Cancer Prevention 21:82–88

c

2011

Wolters Kluwer Health | Lippincott Williams & Wilkins.

European Journal of Cancer Prevention

2012, 21:82–88

Keywords: adherence, compliance, mass screening, trends, Pap smear,
uterine cervical neoplasm, vaginal smears

Preventive Medicine and Public Health Teaching and Research Unit, Rey Juan
Carlos University, Alcorcon, Spain

Correspondence to Rodrigo Jimenez Garcı´a, PhD, Unidad de Docencia e
Investigacion en Medicina Preventiva y Salud Publica, Facultad de Ciencias de la
Salud. Avda. de Atenas s/n. Alcorcn, Madrid 28922, Spain
Tel: + 34 91 4888853; fax: + 34 91 4888848;
e-mail: [e-mail]

Received

21 February 2011 Accepted 7 June 2011

Introduction

Cancer is a leading cause of mortality and has a heavy
burden of disease (Mathers et al., 2008). In terms of
cancer in women, cervical cancer remains a public health
problem in many developed countries, regardless of the
fact that it is much more frequent in developing countries
(Antilla et al., 2004; Arbyn et al., 2009; Ferlay et al., 2010).
In Europe, cervical cancer is the 10th most common
cancer. According to published cancer statistics, there
were an estimated 54 800 new cases of cervical cancer
in 2008 in Europe, with 25 000 deaths. Incidence and
mortality rates vary widely across Europe, with central
and eastern European countries being of the greatest
concern (Ferlay et al., 2010). These differences may be
partially explained by the wide variation both in the
organization of cervical cancer screening activities and in
participation in screening. It has been shown that high
rates of participation in screening programmes are
necessary for an effective decrease in mortality and
incidence (International Agency for Research on Cancer,
2005). Thus, although some countries have implemented
population-based programmes, others have opportunistic
screening, and some European countries have not yet

launched any screening programmes (Anttila et al.,
2009; Nicula et al., 2009).

In Spain, the National Cancer Strategy recommends
cervical cancer screening for women aged between 25 and
64 years by having two annual Pap smears initially and
then every 3 years through opportunistic nonorganized
programmes (Ascunde et al., 2010; Cancer Strategy of
Spanish Ministry of Health, 2011).

This screening strategy in Spain is justified by the low
incidence and mortality of cervical cancer (Ferlay et al.,
2010); nevertheless, a recent study showed that Spain is
one of the few countries in Europe that has experienced a
1% increase in the incidence of cervical cancer. The
authors associated this with the lack of an organized
screening programme in the country (Bray et al., 2005).

The European Union (EU) currently recommends that
cancer screening should only be offered in population-
based, organized screening programmes with quality
assurance (Council of the European Union, 2003; Anttila
et al., 2008). These recommendations are based on
studies that showed greater effectiveness in population-
based programmes with respect to both reducing the

82

Research paper

0959-8278

c 2011 Wolters Kluwer Health | Lippincott Williams & Wilkins

DOI: 10.1097/CEJ.0b013e32834a7e46

Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.

incidence and mortality of cervical cancer and their ability
to decrease both overscreening and underscreening
(International Agency for Research on Cancer, 1986; In-
ternational Agency for Research on Cancer, 2005; Anttila
et al., 2009).

In any case, it is important to survey adherence to
screening recommendations periodically and identify
factors that influence the nonparticipation of women in
screening tests. Previous Spanish studies (Luengo Matos
and Mun

˜oz van den Eynde, 2004; Cabeza et al.,

2007; Puig-Tintore

´ et al., 2008; Ascunde et al., 2010; Mar-

tı´n-Lo

´pez et al., 2010) report adherence rates of 49.5–75%

for Pap smears. In other developed countries also, results
vary widely (Coughlin et al., 2004; Hewitt et al.,
2004; Coughlin et al., 2008; Anttila et al., 2009; Nelson
et al., 2009; Nicula et al., 2009). Sociodemographic factors
(Coughlin et al., 2004; Hewitt et al., 2004; Luengo Matos
and Mun

˜oz van den Eynde, 2004; Cabeza et al.,

2007; Coughlin et al., 2008; Johnson et al., 2008; Puig-
Tintore

´ et al., 2008; Nelson et al., 2009; Martı´n-Lo

´pez

et al., 2010) and healthcare-related variables, such as
periodic visits to the doctor or gynaecologist (Coughlin
et al., 2004, 2005; Martı´n-Lo

´pez et al., 2010), have often

been found to be linked to participation in cervical cancer
screening. Similarly, certain self-declared chronic diseases
(Kiefe et al., 1998; Martı´n-Lo

´pez et al., 2010), as well as

certain lifestyles (Coughlin et al., 2004; Gala´n et al.,
2006; Ferrante et al., 2007; Mitchell et al., 2008; Maruthur
et al., 2009; Byrne et al., 2010; Martı´n-Lo

´pez et al., 2010),

were associated with screening attendance.

The aims of this study were: (a) to estimate the
adherence to cervical cancer screening in 2009 and its
association with sociodemographic factors, chronic dis-
eases, and lifestyle behaviours; and (b) to analyse the
time trend of adherence to this screening test in Spain
from 2003 to 2009.

Methods

This study is a cross-sectional study based on data
obtained from the European Health Interview Survey for
Spain (EHISS, 2009).

The European Health Interview Survey was proposed by
the European Commission to the EU member states to
create a health information system using a comprehensive
and coordinated set of surveys performed within the
European Statistical System under the responsibility of
Eurostat. Therefore, all EU states would share common
guidelines for modules and survey design on the basis of a
common questionnaire. The European Health Interview
Survey is implemented every 5 years, with the first
wave completed between 2007 and 2009 (European
Commission, 2011).

The EHISS (2009) was conducted by the National
Statistics Institute (Instituto Nacional de Estadı´stica, INE)
under the aegis of the Spanish Ministry of Health and

Social Affairs. The EHISS is a computer-assisted, home-
based personal interview that examines a nationwide
representative sample of the non-institutionalized civi-
lian population, aged 16 years or more, who reside in
primary family dwellings (households) in Spain. Study
subjects were selected using probabilistic multistage
sampling, with the first-stage units being census sectors
and the second-stage units being primary family dwell-
ings. More details on the EHISS methodology are
described elsewhere (Insituto Nacional de Estadı´stica,
2011). The data collection period started in April 2009
and finished in March 2010. The analysis was performed
in January 2011. For this study, we selected women aged
between 25 and 64 years.

The following dependent variable was created from the
questionnaire:

(1) adherence to cervical cancer screening: this was

assessed by asking participants whether they had
received a cervical Pap smear within the last 3 years.

We also considered the following independent variables:

(1) sociodemographic variables including age, marital

status, educational level, monthly income, and im-
migrant status. Educational level was classified into
primary, secondary, or university studies; monthly
income was divided into < h1400, h1400–h2000, and

> h2000.

(2) visits to the general practitioner in the 4 weeks

preceding the interview.

(3) self-reported chronic diseases, including cardiovascu-

lar diseases (heart attack, angina, stroke, or cerebral
haemorrhage), respiratory diseases (asthma or chronic
bronchitis), musculoskeletal conditions (arthritis,
chronic cervical or lower back pain), psychiatric
diseases (depression or anxiety), hypertension, and
diabetes mellitus.These variables were created from
the ‘Yes’ or ‘No’ answers to the following questions:
‘Have you suffered from any of the following
diseases?’ and ‘Have you ever been diagnosed with
any of these diseases by a physician?’. Only those who
answered ‘Yes’ to both questions were classified as
sufferers of the disease. Obesity was assessed using
body mass index calculated from self-reported body
weight and height; an index of more than or equal to
30 was classified as obese.

(4) Lifestyle behaviours: smoking status (current smoker,

former smoker, or nonsmoker), alcohol consumption,
and physical activity were considered. Alcohol con-
sumption was measured using the question ‘Have you
consumed any alcoholic drinks, at least twice, within
the last week?’. In contrast, if a woman answered that
she practised at least moderate physical activity 3 days
a week she was classified as being physically active.
Next, we studied the main reasons for undergoing a

Cervical cancer screening trends in Spain

Martı´n-Lo´pez et al.

83

Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.

Pap smear, taking into account whether the recom-
mendation had been given by a physician (general
practitioner or gynaecologist) or by an institution such
as the city council or an autonomous region. To analyse
the time trend in the prevalence of adherence to Pap
smears, we used data from the Spanish National
Health Surveys (NHS) conducted in 2003 and 2006.
The methods and results of the 2006 survey have been
published by our group (Martı´n-Lo

´pez et al., 2010).

Statistical analysis

First, a descriptive analysis of the study variables was
performed. Thereafter, the estimated prevalence for
receiving the cervical cancer screening test, with
corresponding 95% confidence intervals (CIs) for each
study variable, was calculated. Second, we analysed the
association of these variables with screening adherence
using the w

2

-test. Third, to determine which variables

were independent predictors of adherence to Pap smear
screening, we performed multivariate logistic regression.
The adjusted odds ratio (OR) and its 95% CI were
calculated to measure the strength of association. Fourth,
we described the main reason for undergoing a Pap smear
by calculating the frequency distribution. Finally, we
combined the 2003 NHS, 2006 NHS, and 2009 EHISS
databases to estimate the time trend of the cervical
cancer screening adherence overall as well as according to
age group. To do so, we constructed both multivariate
logistic regression models using each year (2003 vs. 2006
and 2003 vs. 2009) as the main independent variable and
after adjusting by age.

Estimates were made using the ‘svy’ (survey commands)
functions of the STATA program, which enabled us to
incorporate the sampling design and weights into all of
our statistical calculations. Weights were initially derived
from selection probabilities to compensate for planned
oversampling procedures so that results would be
representative at both the national and autonomous
region levels. Weights were calibrated using comparable
population characteristics for sex, age, nationality, and
size of the household (European Commission, 2011).

Statistical significance was set as two tailed a < 0.05.

All estimates were made using the STATA 9.1 (StataCorp
LP, Lakeway Drive, College Station, Texas, USA)
statistical package.

As this investigation was conducted using nonidentified
public databases, it was not necessary to have the approval
of an ethics committee, as per Spanish legislation.

Results

There were 7634 women eligible for Pap smears (aged
25–64 years). Table 1 shows the distribution of women
eligible for the screening test in the study sample and
the prevalence of Pap smear adherence according to

sociodemographic variables. The majority of women were
married and had completed at least secondary studies.
Only 14.29% were immigrants. In terms of the prevalence
of cancer screening adherence,

66.12% (95% CI:

64.79–67.42) of women aged 25–64 years reported that
they had received a Pap test in the last 3 years. It is
important to note that women between the ages of 35
and 54 years achieved more than 70% adherence to
screening, whereas younger and older women reported
lower participation. Table 1 also shows the results of
the bivariate analyses. The following sociodemographic
covariates were significantly associated with having
received a Pap smear in the last 3 years: age group,
marital status, educational and income levels, and
immigrant status.

Table 2 shows the distribution of the study sample and
the prevalence for Pap smear adherence according to
general practitioner visits, chronic conditions, and life-
styles. It is noteworthy that greater adherence was found
in women who visited the general practitioner in the 4
weeks before survey completion. With respect to self-
declared chronic conditions, only musculoskeletal dis-
eases were associated with greater adherence, whereas
cardiovascular diseases, hypertension, diabetes mellitus,
and obesity were associated with lower screening
participation in the bivariate analysis. Obese women
were more likely to not have had a Pap smear in the past 3
years. In contrast, former smokers, and individuals who
practised physical activity in their leisure time or
consumed alcohol twice a week, were more likely to
have received preventive screening.

Table 1

Distribution of women eligible for the screening test in the

study sample and prevalence of Pap smear adherence according
to sociodemographic variables

Variables

Distribution in

the sample n (%)

% Pap smear

(confidence interval 95%)

a

Total

7634

66.12 (64.79–67.42)

Age groups*

25–34

1584 (27.60)

65.39 (62.42–68.23)

35–44

2253 (28.42)

70.58 (68.20–72.85)

45–54

1991 (24.48)

70.90 (68.45–73.24)

55–64

1806 (19.50)

54.66 (51.90–57.40)

Marital status*

Single

1277 (16.68)

51.64 (47.99–55.28)

Married

5317 (74.40)

70.32 (68.83–71.77)

Widowed

387 (3.13)

49.48 (43.18–55.80)

Divorced/separated

650 (5.78)

62.83 (57.94–67.47)

Educational level*

Primary studies

2220 (27.64)

54.34 (51.81–56.84)

Secondary studies

3573 (49.03)

68.48 (66.56–70.34)

University studies

1838 (23.34)

75.13 (72.48–77.61)

Monthly income*

< 1400 h

2432 (41.64)

57.75 (55.27–60.20)

1400 h–2000 h

1423 (22.87)

62.33 (59.17–65.38)

> 2000 h

2393 (35.50)

74.62 (72.37–76.74)

Nationality*

Immigrant

584 (14.29)

56.13 (51.29–60.85)

Nonimmigrant

7050 (85.71)

67.79 (66.47–69.07)

a

Prevalence of Pap smear adherence.

*P < 0.05 for Pap smear adherence (w

2

-test).

84

European Journal of Cancer Prevention

2012, Vol 21 No 1

Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.

Table 3 summarizes the adjusted ORs and 95% CI
obtained using the logistic regression model in which Pap
screening participation was the dependent variable. All of
the sociodemographic covariates remained significant.
Women aged 55–64 years were less likely to have
answered ‘Yes’ to the question about Pap smear
adherence in the past 3 years, as were single women.
However, being married was a positive predictor of
adherence to screening. Similarly, having completed
secondary or university education was a predictor of
compliance compared with the primary study category,
with an OR of 1.54 (95% CI: 1.29–1.85) and an OR of 2.30
(95% CI: 1.80–2.92), respectively. Higher income level
and nonimmigrant status were also associated with higher
participation. Women who had visited their general
practitioner had a 41.7% (OR: 1.42; 95% CI: 1.21–1.66)
higher probability of having undergone a Pap smear. In
contrast, those with less healthy lifestyles, such as obese
women, were less likely to comply (OR: 0.74; 95% CI:
0.61–0.91).

Table 4 provides the evolution of the adherence to cervical
cancer screening in Spain from 2003 to 2009. Globally

speaking, the data showed no significant changes in
compliance with Pap smears over the study years. Age
groups also presented no significant differences with regard
to compliance, with the exception of a younger group of
women who experienced a gradual increase in adherence to
cervical cancer screening, which was significant from 2006
to 2009 (adjusted OR: 1.26; 95% CI: 1.05–1.51).

With regard to why women decided to take the test, the
most frequently reported reason was because it was
recommended by a physician (73.78%), whereas only
10.63% received a recommendation from the health depart-
ment of the city council or autonomous region in the mail.

Discussion

This study described adherence to cervical cancer screen-
ing in Spain and was aimed at identifying the factors
associated with having undergone a Pap smear in the past 3
years in a nationally representative sample of women in
2009. We also assessed the difference between these figures
and previous figures for screening compliance in 2003 and
2006. It is relevant to obtain this type of information, as it is
known that successful cancer screening programmes
depend on the rate of adherence (International Agency
for Research on Cancer, 2005).

Table 2

Distribution of the study sample and prevalence of Pap

smear adherence according to: visits to the general practitioner,
chronic conditions, and lifestyles

Variables

Distribution in

the sample, n (%)

% Pap smear

(confidence interval 95%)

a

Total

7634

66.12 (64.79–67.42)

General practitioner visit in the last 4 weeks*

No

5263 (69.89)

64.35 (62.73–65.94)

Yes

2371 (30.11)

70.23 (67.91–72.44)

Respiratory disease

No

6817 (89.39)

65.71 (64.29–67.09)

Yes

817 (10.61)

69.61 (65.69–73.27)

Cardiovascular disease*

No

7445 (97.89)

66.33 (64.98–67.65)

Yes

189 (2.11)

56.46 (48.02–64.55)

Diabetes mellitus*

No

7334 (96.49)

66.40 (65.04–67.73)

Yes

300 (3.51)

58.54 (51.81–64.96)

Hypertension*

No

6583 (86.96)

67.11 (65.68–68.51)

Yes

1051 (13.04)

59.52 (55.92–63.03)

Psychiatric disease

No

6449 (86.09)

66.38 (64.94–67.80)

Yes

1185 (13.91)

64.48 (61.14–67.69)

Musculoskeletal disease*

No

5488 (74.01)

65.44 (63.84–67.01)

Yes

2146 (25.99)

68.05 (65.70–70.31)

Obesity*

No

6286 (87.29)

68.57 (67.13–69.98)

Yes

932 (12.71)

57.17 (53.29–60.96)

Smoking habit*

Current smoker

2272 (29.68)

66.75 (64.30–69.11)

Former smoker

1477 (18.71)

75.50 (72.82–78.00)

Nonsmoker

3742 (51.61)

63.55 (61.60–65.45)

Alcohol consumption*

No

6296 (85.10)

66.03 (64.56–67.47)

Yes

1190 (14.90)

70.74 (67.47–73.81)

Physical activity*

No

3713 (44.93)

64.14 (62.15–66.09)

Yes

3860 (55.07)

67.80 (66.00–69.54)

a

Prevalence of Pap smear adherence.

*P < 0.05 for Pap smear adherence (w

2

-test).

Table 3

Predictors of adherence to Pap smear screening.

Variables

OR (95%CI)

a

Age groups (years)

25–34

1

35–44

1.02 (0.83–1.25)

45–54

1.02 (0.82–1.26)

55–64

0.51 (0.40–0.64)

Marital status

Single

1

Married

2.26 (1.83–2.79)

Widowed

1.48 (1.02–2.15)

Divorced/separated

2.00 (1.49–2.71)

Educational level

Primary studies

1

Secondary studies

1.54 (1.29–1.85)

University studies

2.30 (1.80–2.92)

Monthly income

< 1400 h

1

1400 h–2000 h

1.06 (0.88–1.28)

> 2000 h

1.41 (1.17–1.70)

Nationality

Immigrant

1

Nonimmigrant

1.84 (1.44–2.35)

GP visit in the last 4 weeks

No

1

Yes

1.42 (1.21–1.66)

Musculoskeletal disease

No

1

Yes

1.35 (1.14–1.59)

Obesity

No

1

Yes

0.74 (0.61–0.91)

Smoking habit

Nonsmoker

1

Former smoker

1.32 (1.07–1.60)

Current smoker

0.98 (0.83–1.16)

CI, confidence interval; GP, general practitioner; OR, odds ratio.

a

OR and 95% CI estimated using multivariate logistic regression. Variables

included in the model are those with significant association in the bivariate
analysis.

Cervical cancer screening trends in Spain

Martı´n-Lo´pez et al.

85

Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.

In 2009, there was an estimated adherence of 66.1% (CI:
64.79–67.42) to cervical cancer screening in Spain. This
suggested an average participation rate in comparison with
previous Spanish studies, which obtained a wide variety of
results. Different authors have obtained different figures:
49.5% in 2000 (Luengo Matos and Mun

˜oz van den Eynde,

2004), 54% in 2005 (Cabeza et al., 2007), even 75.6% in
another study carried out in 2005 (Puig-Tintore

´ et al.,

2008), and finally 69% in 2006 (Ascunde et al., 2010).
Similarly, with respect to neighbouring countries, this
screening adherence represents an intermediate position
between European countries that achieved the highest
participation rate, approximately 70–80% in countries
such as those in northern Europe and England, and
countries with low participation rates, such as those in the
eastern region (Antilla et al., 2004; Anttila et al., 2009).
However, if we take into account middle-aged women,
participation rates in our country were close to those with
the highest adherence. In other developed countries, such
as the United States, several studies showed high results
in screening attendance of approximately 85% (Coughlin
et al., 2004; Hewitt et al., 2004; Coughlin et al., 2008; Nel-
son et al., 2009). Nevertheless, we should note that
comparisons at both levels should be made with caution,
because of the different sources for data on compliance
with screening and the coexistence of different types of
screening strategies and target populations (Puig-Tintore

´

et al., 2008; Anttila et al., 2009).

In addition, this population-based study allowed us to
analyse the factors associated with participation in
cervical cancer screening. Knowledge of both predictors
and barriers to undergoing the screening test may
contribute to the prioritization of strategies for improving
adherence. Predictors of screening attendance have
already been analysed in previous studies (Kiefe et al.,
1998; Coughlin et al., 2004; Hewitt et al., 2004; Luengo
Matos and Mun

˜oz van den Eynde, 2004; Coughlin et al.,

2005; Gala´n et al., 2006; Cabeza et al., 2007; Ferrante et al.,
2007; Coughlin et al., 2008; Johnson et al., 2008; Mitchell
et al., 2008; Puig-Tintore

´ et al., 2008; Maruthur et al.,

2009; Nelson et al., 2009; Byrne et al., 2010; Martı´n-Lo

´pez

et al., 2010). Through our results we can see that both
high educational and high economic levels continue to be
good predictors in present times for Pap smear compli-
ance (Coughlin et al., 2004; Hewitt et al., 2004; Luengo
Matos and Mun

˜oz van den Eynde, 2004; Cabeza et al.,

2007; Coughlin et al., 2008; Puig-Tintore

´ et al., 2008; Mar-

tı´n-Lo

´pez et al., 2010), whereas women with a more

disadvantaged socioeconomic status participated less
frequently in screening, as did the immigrant population
(Coughlin et al., 2004; Hewitt et al., 2004; Luengo Matos
and Mun

˜oz van den Eynde, 2004; Cabeza et al.,

2007; Coughlin et al., 2008; Johnson et al., 2008; Puig-
Tintore

´ et al., 2008; Martı´n-Lo

´pez et al., 2010). Similarly,

older women had lower attendance for cervical cancer
screening; it is important to note this as the age group
most affected by cervical cancer ranges from 45 to 64
years (Oliva et al., 2005).

As for healthcare-related variables, visiting a general
practitioner was positively associated with Pap smear
attendance in this analysis, consistent with previous
studies (Coughlin et al., 2004, 2005; Martı´n-Lo

´pez et al.,

2010). This fact may be explained by the need for an
earlier contact with the general practitioner in order to be
referred for a Pap smear, as opportunistic screening based
on primary care is still the norm in Spain. In terms of
chronic conditions, we agreed with Kiefe et al. (1998), who
found that higher comorbidity was associated with lower
screening attendance, despite greater contact with health-
care providers who are in charge of this type of patient.

Some unhealthy lifestyles were associated with lower
adherence. Previous studies have already found that
obesity was a condition for a lower participation rate in
cervical cancer screening (up to 50% less) (Coughlin et al.,
2004; Ferrante et al., 2007; Mitchell et al., 2008; Maruthur
et al., 2009), and the results in this study showed that this
barrier still exists. Several studies have found that
embarrassment among obese women and the reluctance
of physicians to perform pelvic examinations on patients
who are uncomfortable undergoing pelvic examinations,
such as obese women, may affect compliance with Pap
smears (Maruthur et al., 2009).

Bearing in mind the results, one could say that the
participation of women in cervical cancer screening has not
changed substantially in Spain since 2003. It remains in an
intermediate position, likely to improve. Although it seems
understandable that countries with lower coverage have
more opportunity for improvement (Spaczynski et al., 2010),
also, countries with greater adherence may improve with the
development of certain strategies in order to optimize
organized screening programmes (Virtanen et al., 2010).

Table 4

Evolution of adherence to Pap smear screening (2003–2009)

NHS 2003

NHS 2006

EHISS 2009

OR 2006

a

OR 2009

b

25–34

59.96 (56.92–62.92)

61.63 (59.12–64.09)

65.39 (62.42–68.23)

1.07 (0.91–1.26)

1.26 (1.05–1.51)

35–44

73.29 (70.75–75.69)

72.73 (70.63–74.74)

70.58 (68.20–72.85)

0.97 (0.82–1.14)

0.87 (0.74–1.03)

45–54

71.72 (68.84–74.45)

73.93 (71.54–76.18)

70.90 (68.45–73.24)

1.12 (0.93–1.34)

0.96 (0.80–1.15)

55–64

58.85 (55.60–62.20)

61.11 (58.50–63.66)

54.66 (51.90–57.40)

1.10 (0.92–1.30)

0.84 (0.71–1.00)

Total

66.21 (64.73–67.65)

67.43 (66.21–68.63)

66.12 (64.79–67.42)

1.05 (0.97–1.15)

0.99 (0.91–1.08)

EHISS, European Health Interview Survey for Spain; NHS, National Health Survey; OR, odds ratio.

a

Adjusted OR and 95% confidence interval (2003–2006).

b

Adjusted OR and 95% confidence interval (2003–2009).

86

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2012, Vol 21 No 1

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In contrast, it is encouraging to see increased participation
among younger women. This result in our study may be
related to the recent introduction of the human
papillomavirus (HPV) vaccination in Spain and to the
greater presence of information on this subject in mass
media, which may have acted as a pull factor for young
women. The HPV vaccine was introduced into the
Spanish vaccination schedule around 2008 and is free of
charge (Ministry of Health, 2011). It is recommended to a
single cohort of girls between the ages of 11 and 14 years,
depending on the autonomous region. Data published to
date show good coverage (Ministry of Health, 2011),
although vaccinated cohorts have not yet reached the age
for the onset of cancer of the cervix. Therefore, recently
proposed changes in screening, including HPV detection,
are likely to be generally implemented in the future
(Corte

´s et al., 2010). Similarly, the use of self-sampling for

the detection of HPV is expected to increase, when
population screening in Spain is based on the detection of
HPV, in view of the results of an interesting study that
concluded that offering self-sampling for collecting
cervicovaginal specimens for high-risk HPV testing is a
feasible and effective method for increasing coverage in a
screening programme for women who did not attend
regular screening (Go

¨k et al., 2010).

In light of these results, we believe that there is still
scope to improve cervical cancer screening in our country.
The next discussion would be the best way to achieve
this, taking into account criteria for efficiency and
equality. Improvements in cervical cancer control have
been particularly successful in countries that have
implemented organized population-based programmes
(Miller 2002; Peto et al., 2004). These population-based
screening programmes have proven to be effective in
increasing participation (Forbes et al., 2002; Miller
2002; Peto et al., 2004; Palencia et al., 2010; Spadea
et al., 2010) and decreasing overscreening (International
Agency for Research on Cancer, 2005; Anttila et al., 2009);
however, their capacity to decrease socioeconomic
inequalities (Palencia et al., 2010; Spadea et al., 2010) is
less clear. Spain currently remains a country with
opportunistic screening using primary care-based conven-
tional Pap smears. Thus, a switch to a population-based
programme strategy could be considered.

The main strength of this study is its use of a nationally
representative sample to assess adherence to cervical
cancer screening. There are, however, a number of
potential limitations. First, as it is a cross-sectional survey,
we must take into account the fact that causality cannot
be inferred, because of ‘reverse causality’. This is
because, although there truly is an association, we may
not be able to determine which came first because the
suspected cause and effect are measured simultaneously.

Second, the study is based on self-reported information.
This may lead to an overestimation of adherence to

cancer screening, as has been documented in scientific
literature (Howard et al., 2009). This potential over-
estimation is due to two types of bias: selection (higher
response rate to the specific Pap smear question among
screened women) and information (women tend to
provide more socially desirable information or to project
a screening examination to a more recent date, thereby
underestimating the time since the previous screening).
Data obtained from records are more accurate and
reliable; however, such data can be very expensive and
difficult to organize, especially in our country (public and
private health services provide screening tests) with
opportunistic nonorganized screening. Therefore, self-
reporting may be the only cost-effective and feasible
method to gather data on Pap smear adherence from large
samples of the population (Howard et al., 2009; Cancer
Strategy of Spanish Ministry of Health, 2011). In
addition, the information that can be obtained from the
EHISS may overestimate some chronic conditions
(European Commission, 2011).

Another limitation to be considered is the lack of
information on particular issues in the EHISS, such as
the type of healthcare insurance. In addition, unfortu-
nately, the EHISS questionnaire collects information only
on the time since the last Pap smear was carried out and
not on the number of tests conducted over the last 3
years. Therefore, it is not possible to calculate data on
overscreening.

Similarly, the survey does not provide detailed informa-
tion about why women did not have a Pap smear test
(European Commission, 2011). Other Spanish studies
have analysed this question and found that the main
reasons for noncompliance were: fear of the results,
unwillingness to undertake the test, and administrative
issues (Luengo Matos and Mun

˜oz van den Eynde, 2004).

Finally, the initial response rate to the EHISS was 64%;
therefore, a possible nonresponse bias should be taken
into consideration (Insituto Nacional de Estadı´stica,
2011).

We conclude that cervical cancer screening in Spain could
be improved, especially in younger and older women.
Certain factors such as lower socioeconomic status,
immigrant status, and obesity still remain barriers to
participation in screening programmes. Hence, an effort
must be made to recruit these women. Health profes-
sionals, especially general primary care physicians, must
be properly informed in order to improve medical advice
to these patients as long as an opportunistic nonorganized
screening programme remains the norm in Spain. In
contrast, a debate on the most appropriate way to
improve the outcomes of opportunistic programmes
should be launched, or even replacing the actual strategy
with a population-based screening in Spain could be
considered, as has been suggested by the EU. Further
investigation is required on this point.

Cervical cancer screening trends in Spain

Martı´n-Lo´pez et al.

87

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Acknowledgements

Conflicts of interest

There are no conflicts of interest.

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