Increasing participation in cervical cancer screening: Telephone
contact with long-term non-attendees in Sweden. Results from
RACOMIP, a randomized controlled trial

Gudrun Broberg

1,2

, Junmei Miao Jonasson

1,3

, Joy Ellis

2

, Dorte Gyrd-Hansen

4,5

*, Birgitta Anjemark

6

, Anna Glantz

2

,

Lotta S€

oderberg

7

, Mare-Liis Ryd

1

, Mikael Holtenman

1

, Ian Milsom

2

and Bj€

orn Strander

1,2

1

Regional Cancer Centre, Western Health Care Region, Gothenburg, Sweden

2

Department of Obstetrics and Gynecology, Institute of Clinical Science, Sahlgrenska Academy at University of Gothenburg, Sweden

3

Nordic School of Public Health, NHV, Gothenburg, Sweden

4

ACERH, University of Queensland, Brisbane, Oueensland, Australia

5

COHERE, University of Southern Denmark, Odense, Denmark

6

Fr€

olunda Torg Antenatal Clinic, Gothenburg, Sweden

7

Bora˚s Antenatal Clinic, Bora˚s, Sweden

Non-participation is the foremost screening-related risk factor for cervical cancer. We studied the effectiveness and cost-

effectiveness of an intervention to increase participation in the context of a well-run screening program. Telephone contact

with non-attendees, offering an appointment to take a smear, was compared with a control group in a population-based

randomized trial in western Sweden. Of 8,800 randomly selected women aged 30–62, without a registered Pap smear in the

two latest screening rounds, 4,000 were randomized to a telephone arm, another 800 were offered a high-risk human

papillomavirus (HPV) self-test by mail (not reported in this article) and 4,000 constituted a control group. Endpoints were

frequency of testing, frequency of abnormal smears and further assessment of abnormal tests. Participation during the

following 12 months was significantly higher in the telephone arm than in the control group, 718 (18.0%) versus 422 (10.6%)

[RR: 1.70, 95% confidence interval (CI): 1.52–1.90]. The number of detected abnormal smears was 39 and 19, respectively

(RR: 2.05, 95% CI: 1.19–3.55). The respective numbers of further assessed abnormalities were 34 and 18 (RR: 1.89, 95% CI:

1.07–3.34). Twice as many high-grade intraepithelial neoplasia (CIN21) were detected and treated in the telephone arm: 14

and 7, respectively. Telephone contact with women who have abstained from cervical cancer screening for long time increases

participation and leads to a significant increase in detection of atypical smears. Cost calculations indicate that this

intervention is unlikely to be cost-generating and this strategy is feasible in the context of a screening program.

Cervical cancer is considered to be a preventable disease.

1

Screening by Papanicolaou (Pap) smear has markedly
reduced incidence and mortality.

2–4

Vaccines to prevent

infection with specific oncogenic human papillomavirus
(HPV), the main cause of cervical cancer,

5

are available but it

will be long before effects on cancer will be measurable.

6,7

At

least until then, screening programs will remain the key
defense against this disease.

8

A recent audit of the Swedish

screening program, in which all cases of invasive cervical epi-
thelial carcinoma during 3 years were evaluated, showed that

Key words:

mass screening, Papanicolaou smear, cervical intraepithelial neoplasia, telephone reminder, non-attendance

Abbreviations:

ASCUS: atypical squamous cells of undetermined significance; CI: confidence interval; CIN: cervical intraepithelial neoplasia;

FIGO: International Federation of Gynaecology and Obstetrics; HPV: human papillomavirus; HSIL: high-grade squamous intraepithelial
lesion; Pap: Papanicolaou; RACOMIP: randomized controlled trial to study methods to increase participation in the cervical cancer screening
program; RR: relative risk; SAS: statistical analysis software
Additional Supporting Information may be found in the online version of this article.
Authors’ contributions: G.B. and B.S. designed the study. All authors contributed to the collection of data and the analysis. D.G.H., B.S. and
G.B. performed the health-economic analysis. G.B., D.G.H. and B.S. wrote the first draft of the article. All authors contributed to the final
manuscript.

Grant sponsors:

The Swedish Cancer Society, The Health & Medical Care Committee of the Regional Executive Board, V€astra G€

otaland

Region, The Swedish Association of Local Authorities and Regions, The Gothenburg Medical Society and Assar Gabrielsson’s Fund

DOI:

10.1002/ijc.27985

History:

Received 25 Sep 2012; Accepted 12 Nov 2012; Online 11 Dec 2012

Correspondence to:

Bj€

orn Strander, Regional Cancer Centre, Sahlgrenska University Hospital, Gothenburg SE-413 45, Sweden, Tel.:

þ46-31-34-39072, Fax: þ46-31-209250, E-mail: [e-mail]

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International Journal of Cancer

IJC

the foremost risk factor for cervical cancer in the context of
the program was non-participation.

9

Other studies have con-

firmed that population coverage is vital for success and that
women who participate are well protected from cervical can-
cer.

10,11

For Swedish women aged 23–50, coverage of screen-

ing, including opportunistic smears taken outside the screen-
ing program, was 78% during a 3.5-year period ending
2009.

12

This is high coverage in an international context,

13

but regional differences are substantial (range 64–91%).

12

Strategies to increase participation, such as invitation with a
scheduled appointment,

14

reminder letter

15,16

and telephone

reminder,

16

have been studied. Offering a HPV self-test has,

in some studies, increased participation in the screening pro-
gram.

17–20

In western Sweden, annual reminders and sched-

uled appointments have already been implemented and
women in parts of the region can now re-book appointments
on the Internet.

To study the effectiveness and cost-effectiveness of interven-

tions to increase participation in a population-based, well-run
screening program, we designed a large-scale randomized trial
in the context of the existing screening program in western
Sweden. The aim of the trial was to assess the effectiveness of a
telephone call offering an appointment for a Pap smear or by
mail offering a HPV self-test. Our hypothesis was that the
intervention increases participation, the number of detected
abnormal smears and the number of further assessments of
abnormal smears, thereby preventing morbidity and mortality
related to invasive cervical cancer. In this article, we present
the results of the telephone intervention arm.

Material and Methods

Randomized controlled trial to study methods to increase
participation (RACOMIP) in the Cervical Cancer Screening
Program) is a clinical trial conducted in the context of a
Swedish population-based screening program, in the western
region of Sweden. The program adheres to the Swedish
National Board of Health and Welfare recommendation of
Pap smears at 3-year screening intervals for women aged 23–
50 and at 5-year intervals for women aged 51–60.

21

The sys-

tem for invitation, registration and follow-up is computerized
and linked by personal identification numbers to the National
Population Register which includes all residents of Sweden.
All organized and opportunistic tests are registered and coor-

dinated in the Register for Prevention of Cervical Cancer in
Western Sweden. The woman receives an invitation for
organized screening when, depending on her age, 3 or 5
years have passed since the last Pap smear. Annual re-invita-
tion until a smear has been registered was introduced in the
area between 2002 and 2007. The invitation includes the time
and place for an appointment at an Antenatal Health Clinic
where midwives takes the smears. The scheduled time for
each appointment is approximately 7 minutes. On December
31, 2010, regional coverage, i.e., the percentage of women
aged 25–49 who had had a Pap smear during the previous
three and a half years ,was 77%.

22

The coverage varies among

areas in the region and the range among parishes in
Gothenburg, the major city in the region, is 54–83%. The
lowest coverage rates are in areas with high unemployment
and many immigrants.

The western region of Sweden had 371,027 female resi-

dents aged 30–62 years in August 2009 when we initiated
our trial. We included women with no Pap smear registered
for more than 6 years if aged 30–53 years, more than 7 years
if aged 54 years and more than 8 years if aged 55–62 years.
We defined these women as ‘‘non-attendees.’’ According to
regional guidelines, women are not invited for screening after
total hysterectomy if they have had no high-grade dysplasia
for at least 10 years. The women who had not been invited
for screening due to hysterectomy and those not confirmed
to be residents of the region during the whole period were
excluded from the study. Statistical Analysis Software (SAS)
9.2, the Plan procedure, was used to select and randomize
8,800 women in parallel groups with a 5:1:5 ratio into two
intervention arms, i.e., telephone contact and self-test for
HPV (not reported in this article), as well as a control group.

In the telephone arm, a letter was sent to 4,000 women

informing them of the aim and procedure of the study and
that a midwife would contact them by telephone in 14 days
to offer an appointment to take a Pap smear. A response
form and a stamped addressed envelope were enclosed, to be
returned within 7 days if the woman declined the offer.
Alternatively, the women could use the form to provide con-
tact information. Telephone numbers were produced from a
database by a commercial directory service and manually
retrieved from Internet telephone directories. Midwives repre-
senting all 71 Antenatal Health Clinics in western Sweden

What’s new?

Improvements in cancer screening techniques won’t prevent disease if people don’t show up to get screened. This

study evaluated whether calling women on the telephone to remind them to get Pap smears would increase

participation and lead to more detection of potential cancers. The authors compared data from 4,000 women who

received phone calls with those of 4,000 control women. Significantly more women from the telephone group came in

for screening, and almost twice as many abnormalities were detected in that group. Telephoning women to encourage

them to make screening appointments, therefore, could improve cancer detection and prevention without greatly increasing

costs.

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received lists of names and telephone numbers. They sorted
out those who declined and tried to get in contact with the
others, to help and encourage them to book a Pap smear
appointment. If there were missing or erroneous telephone
numbers the midwives were instructed to search maternity
records if available. A maximum of 10 attempts to make con-
tact was set and a total of 20 minutes was to be spent on
each woman, including searching for telephone numbers and
the actual time spent on the call. Whether and at what time
contact was made, the number of attempts and the total time
spent on each woman were all noted in the study protocol.
Although regular screening appointments were generally
offered, women sometimes made special requests for booking
an appointment; the midwives noted the requests and
whether they could be met in the protocol. Whether or not
an

appointment

was

booked

and

any

spontaneously

expressed reasons for not booking were also noted in the
protocol. Abnormal smears were followed up by referral to a
gynecologist according to the normal screening routine. The
control group consisted of 4,000 women who were not sub-
ject to any particular intervention. According to ordinary
screening program routines, these women received annual
invitations until a smear was registered. A reference group
was established for comparisons of atypical smears. This con-
sisted of all women participating in the regular screening
program, aged 30–62 years, with smears taken during the
same period, Sept 9, 2009-Sept 8, 2010. The control group
was included but the intervention groups were excluded from
this reference group. Moderate and severe squamous atypia
(HSIL) and high-grade glandular atypia were defined as high-
grade atypical smears.

Resource use was registered for both the control and

intervention arm in order to ascertain costs. We calculated
the cost of the intervention as the cost of sending out infor-
mation letters, finding telephone numbers and making calls,
including time spent by midwives (valued at the hourly wage
rate). The cost of the Pap smear in the ordinary screening
program (identical in all arms) was calculated on the basis of
the time spent per smear (15 minutes) multiplied by the mid-
wives’ hourly wage (€ 29/h) plus laboratory analysis cost (€
23). The costs of further diagnostic assessment was estimated
on the basis of current clinical guidelines.

23

The cost of the

triage HPV test for atypical squamous cells of unknown sig-
nificance

(ASCUS)

or cervical intraepithelial neoplasia

(CIN)1 was € 44 and colposcopy cost € 167. The cost of
CIN2þ was assumed to be € 400 per treatment, according to
current prices in the region. We report our results as cost per
CIN2þ detected and eradicated.

Statistical analysis

The primary outcomes analysis, followed up after 12 months,
was the difference in frequency of testing, i.e., Pap smears, in
the telephone arm and control group. Testing frequency was
also calculated retrospectively after 3 months. The frequency
of abnormal smears, frequency of further assessment of

abnormal smears, frequency of treated CIN and number of
invasive cancers detected (classified by FIGO stage) and
treated were the secondary outcomes, followed up after 15
months. The study was dimensioned so that a 30% difference
in the outcome of the primary final endpoint, based on an
expected 20% participation in the control group, could be
detected with 80% statistical power at a 5% level of signifi-
cance for both interventions. Assuming a 7% proportion of
abnormal Pap smears in the control group, 4,000 invited
women in the telephone arm yields a statistical power of 80%
to detect a relative difference, calculated as relative risk (RR),
of 1.6 in the frequency of abnormal smears, compared with
the control group. Unless otherwise stated, the results are
presented as intention to treat. Differences in frequencies of
abnormal smears were calculated with the screening popula-
tion as the reference in a logistic regression model adjusted
for age. The RRs and 95% confidence intervals (CIs) were
calculated. The SPSS package 19.0 and R ver. 2.11.1 were
used for the data analysis.

The study was approved by The Regional Ethical Review

Board at Gothenburg University and conforms to the Con-
sort Statement and checklist for randomized studies.

24

The

study is registered at ClinicalTrials.gov (NCT01029990).

Results

An overview of the study is shown as a flow chart (Fig. 1).
24,755 women fulfilled the inclusion criteria, constituting 7%
of female population of the age in question in the region. It
was from this cohort that the 8,800 women in the trial were
randomly selected. The distributions of age and Pap smear
history in the telephone intervention arm and control group
were similar (Table 1).

Midwives tried to contact the 4,000 women during 4

weeks in September and October, 2009. Most of the midwives
(63%) had less than 40 (range 6–555) women to call. They
called 2,586 (65%) women, contact was made with 2,110
(53%) women and 1,176 (29%) appointments were booked
(Fig. 1). By making one to four attempts to call, the midwives
reached 64% (1,655 of 2,586) of the women they attempted
to call and almost 80% (1,655 of 2,110) of all women who
finally answered the call. The mean time used to search for
missing telephone numbers and to make calls was 7 minutes
per woman. The midwives made the calls during normal
working hours, usually 8 AM to 5 PM. The telephone calls
resulting in contact were evenly distributed during the work-
day (data not shown). Some women spontaneously expressed
requests related to appointments (Table 2), mostly related to
practical problems and most of which were met. They some-
times also expressed their reasons for declining to book an
appointment. Hysterectomy was reported in 265 cases and
669 had other reasons, such as unavailability of a convenient
time, physical or mental illness, disability or mental retarda-
tion. Some women reported that they felt healthy, while
others did not want to know if they had cervical dysplasia,

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had a history of sexual abuse, had never had sexual contact
or were not comfortable with gynecologic examinations or
with seeking health care in general. Some women stated they
had already had a Pap smear and others intended to have
one later. Sex reassignment surgery was a rare reason. A few
women stated that they could not afford the fee, some had
moved out of the region and others had problems making
themselves understood.

A significantly higher number of women participated

within 3 months of follow-up, 519 (13.0%) compared to 154
(3.9%) in the control group, yielding RR 3.37 (95% CI 2.83–
4.01). The rate was still significantly higher 12 months after
the intervention: 718 (18.0%) and 422 (10.6%), respectively
(RR 1.70, 95% CI 1.52–1.90) (Table 3). Women aged 30–40
responded to the telephone intervention to a higher extent
than women aged 41–62. We also found that women who

Figure 1.

Flow chart of the study.

*Some of the women who had declined participation were nonetheless called as the midwife had received the response note too late.

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had a Pap smear registered in the last 10 years, participated
to a greater extent than those who had not. These two find-
ings correspond to a higher spontaneous participation in the
control group as well (Table 3). Abnormal cytology was
found in 39 cases in the telephone arm, compared to 19
in the control group (RR: 2.05, 95% CI: 1.19–3.55).
Further assessment of an abnormal test was made in similar

proportions, i.e., 34 (two of the five who were not followed
up had moved out of the region) vs. 18 (Table 3). Sixteen
and 11 histopathologically verified CIN1 or more severe
lesions, respectively, were detected and 14 and 7 high-grade
intraepithelial lesions, (CIN2þ), respectively, were detected
and treated (RR: 2.0, 95% CI: 0.81–4.95). Two carcinomas,
one FIGO stage IA1 and one stage IIB, were found in the tel-
ephone arm and one, FIGO stage IA1, was found in the con-
trol group. The frequency of abnormal cytology was 5.4% in
the telephone arm, 4.5% in the control arm and 2.7% among
all women aged 30–62 in the regular screening program. A
multiple logistic regression model, adjusted for age, showed
that there were significantly increased risks for abnormal cy-
tology in both the telephone arm (RR: 1.97, 95% CI: 1.45–
2.69) and in the control arm (RR: 1.59, 95% CI: 1.03–2.48),
compared with women 30 to 62 years of age in the regular
screening program (Table 4). The RR for a woman in the tel-
ephone arm to have a high-grade abnormal smear, compared
with women in the reference group of regularly screened
women, was 3.93 (95% CI: 2.39–6.46).

The total cost of the intervention was € 15,843, including

costs for information letters (€ 3,806), searching for telephone
numbers (€ 724), midwives’ salaries (€ 11,036) and telephone
calls (€ 278). The intervention resulted in a higher rate of
smear-taking, a higher detection rate of abnormal cytology and
thus additional treatments for CIN2þ, which generated addi-
tional health care costs: 296 extra smear tests (unit cost: € 31),
11 extra HPV tests (unit cost: € 44), 11 extra colposcopies
(unit cost: € 167) and seven additional treatments of CIN2þ
(unit cost: € 400). The total additional costs generated by the
intervention amounted to € 30,142, corresponding to € 4,927
per extra detected and eradicated case of CIN2þ.

Discussion

Our findings show that, in the context of a well-run cervical
screening program, long-term abstainers can be encouraged
by a telephone call to take a smear. In this randomized study,
we found a 70% increase in smear-taking, compared with a
control group and calculated as intention to treat, when pro-
fessional health care providers (midwives) tried to reach non-
attendees by telephone. The impact of the actual calls made
was even greater, as 47% of the women in the intervention
group were never reached.

There was a two-fold increase in the number of atypical

smears in the intervention group, compared with the controls,
which is a significant finding in evaluating the effectiveness of
this intervention. In the entire group of women without a Pap
smear for 6 years or more (telephone arm and control group),
there was a twofold increase in the frequency of atypical smears
and an almost fourfold increase of highly abnormal smears,
compared with an age-adjusted reference group consisting of
all women in the regular screening program. This indicates
that women who have abstained from screening have a high
incidence of atypical smears, and underlines the importance of
facilitating testing in this group of women. Furthermore the

Table 1.

Age at randomization and history of previous Pap smears

Telephone arm

(n

¼ 4,000)

Control arm
(n

¼ 4,000)

Age

Mean (SD)

46.8 (9.42)

46.8 (9.49)

30–40

1,170 (29%)

1,210 (30%)

41–51

1,418 (35%)

1,343 (34%)

52–62

1,412 (35%)

1,447 (36%)

Pap smear history

No registered Pap smear

1,612 (40%)

1,584 (40%)

At least one registered Pap
smear, more than 10 years ago

1,414 (35%)

1,423 (36%)

At least one Pap smear
within the last ten years

974 (24%)

993 (25%)

Table 2.

Requests related to taking a Pap smear, made

spontaneously by the women to the midwives

Requests

N

Request could

be met

Yes

Partly

No

A suitable time for the appointment

135

122

2

11

A special appointment, outside
screening routines

72

71

1

To obtain contraceptive advice at
the same time

31

28

1

2

To be treated kindly

22

20

2

To have a Pap smear taken at
another clinic

20

10

6

4

To have a Pap smear taken by a
specific professional

17

14

3

To see a physician

13

12

1

To have a ‘‘drop in’’ appointment

12

12

To call back later

11

11

To have the services of an interpreter

8

8

Extraordinary interventions,
e.g., anesthesia

8

1

4

3

To have the midwife call back

7

7

A preparatory consultation

6

4

1

1

To be reminded about the
booked appointment

4

2

2

To take a self-test

1

1

To have Pap smear taken free of charge

1

1

Total

368

322

21

25

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increase in atypical smears is almost fully attributed to the
increase in high-grade smears. In a classical metaanalysis O

¨ st€or

showed a higher regression rate of low grade lesions compared
with high grade,

25

and with longer observation time, as in our

study, this trend of accumulation of high-grade lesions can be
expected to be even stronger. We had a hypothesis and a con-
cern that women who have abstained from taking smears
despite repeated offers might, to a high extent, refuse follow-up
of atypical tests. It was thus encouraging to note that 34 of 39
women (87%) with atypical smears did participate in follow-
up, either by colposcopy or repeat smear. If the two women
who were not traceable because they moved out of the area are
excluded, 92% participated in follow-up. The number of high-
grade cervical lesions (CIN2þ) treated was doubled in the
telephone group, compared to the control group. As expected,
this is not a statistically significant difference since the study
was not powered to find a significant difference in this
outcome.

Costs were estimated to be in the range of € 5,000 per

extra CIN2þ detected and eradicated. Barken conservatively
suggests that one cancer is prevented per six CIN2þ eradica-
tions, implying that the intervention costs € 30,000 per
avoided cancer.

26

Prevention of cervical cancers and associ-

ated treatment involves significant cost savings. Based on
prior treatment cost estimates

27

and a recent publication on

stage distributions of detected symptomatic cancer,

28

the av-

erage cost of treating cervical cancer in a unscreened popula-
tion is € 38,889. Although this study is not based on large
numbers, these cost calculations suggest that the intervention
is likely to be cost-neutral and perhaps even cost-saving.

We find this intervention to be not only effective and

potentially cost-effective but also feasible in the context of a
regional screening program. The telephone calls were made
by midwives within the regular program. They were assigned
a limited time for making telephone calls, 20 minutes per
woman, and actually used an average of only 7 minutes per

Table 3.

Primary and secondary outcomes and CIN detected and treated. Comparison between telephone arm and control group. Relative

difference in participation rate between age and Pap smear history groups in respective arm

Telephone arm

Controls

n (%)

RR

95% CI

n (%)

RR

95% CI

RR

95% CI

Primary outcome:

Participation in screening

718/4,000 (18.0)

422/4,000 (10.6)

1.70

1.52–1.90

Age distribution

1

30–40

294 /1,170 (25.1)

1

Reference

198/1,210 (16.4)

1

Reference

41–51

273 /1,418 (19.3)

0.77

0.66–0.89

143/1,343 (10.6)

0.65

0.53–0.80

52–62

151/1,412 (10.7)

0.38

0.32–0.46

81/1,447 (5.6)

0.32

0.27–0.44

Pap smear history

2

A Pap smear in ten years

275/974 (28.2)

1

Reference

168/993 (16.9)

1

Reference

A Pap smear > ten years ago

192/1,414 (13.6)

0.48

0.41–0.57

100/1,423 (7.0)

0.42

0.33–0.52

No registered Pap smear

251/1,612 (15.6)

0.55

0.47–0.64

154/1,584 (9.7)

0.57

0.47–0.70

Secondary outcomes:

Abnormal cytology

39 (1.0)

19 (0.5)

2.05

1.19–3.55

Further assessment

33 (0.8)

18 (0.5)

1.83

1.03–3.25

Off the protocol:

CIN1

þ lesions detected and treated

3

16 (0.4)

11 (0.3)

1.45

0.68–3.13

CIN2

þ lesions detected and treated

3

14 (0.4)

7 (0.2)

2

0.81–4.95

1

Participation in age groups are compared within respective group. Reference youngest age group.

2

Participation in relation to Pap smear history.

Reference least time since last Pap smear.

3

Study not powered to detect difference between groups.Abbreviations: RR: relative risk; CI: confidence

interval.

Table 4.

Abnormal Pap smears, low-grade and high-grade atypical smears in the telephone arm and the controls, compared to the regular

screening population. Adjusted for age in logistic regression model

Pap smear

All abnormal cytology

Low-grade abnormality

1

High-grade abnormality

2

n

n (%)

RR

95% CI

n (%)

RR

95% CI

n (%)

RR

95% CI

Regular screening

3

55,983

1,514 (2.7)

1

1,197 (2.1)

1

317 (0.6)

1

Telephone arm

718

39 (5.4)

1.97

1.45–2.69

21 (2.9)

1.49

0.99–2.24

18 (2.5)

3.93

2.39–6.46

Control arm

422

19 (4.5)

1.59

1.03–2.48

11 (2.6)

0.97

0.51–1.86

8 (1.9)

4.06

2.18–7.56

1

Includes Koilocytosis, ASC-US, CIN1, AGUS.

2

Includes CIN2–3, ASC-H, Atypia of uncertain origin, AIS.

3

Entire routine screening population in west

Sweden 2010, study interventions excluded.

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accessible telephone number. Although calls were made dur-
ing normal working hours, 80% of the women with a known
telephone number could be reached. In a smaller Swedish
study with different inclusion criteria, no reported time limits
and two investigators making all calls, 71% of non-attendees
were reached by telephone.

16

If the telephone calls in our

study had been made during the evening as well, more might
have been reached as many women work daytime and are
unable to answer their home telephones.

29

The telephone calls made it clear that the reasons for

not participating varied greatly and that various efforts are
required to increase participation. Practical obstacles domi-
nated, as seen in other studies,

30–32

especially among young

women.

33

The most common special request was for a con-

venient appointment and more than half actually booked
outside the regular screening schedule. This may be a mani-
festation of poor accessibility in the regular screening pro-
gram and scheduling of appointments can no doubt be
improved.

34

Offering appointments at different times of the

day and the week and simplifying re-booking would make
it easier for women who wish to attend. Twenty-nine per-
cent of women made an appointment, but about a third of
them never showed up to take a Pap smear. This is not
surprising, since these non-participating women have, as a
group, already shown a strong reluctance to take a smear.
Furthermore, there will always be some women who are
unwilling to participate in any screening program.

35

We found, incidentally, that almost 8% of the women

were hysterectomized, a valid reason for not attending. This
can be one explanation of the fact that older women, who
are more often hysterectomized,

36

were less inclined to

respond, although the intervention was effective at all ages.
The regional invitation systems have procedures for exclud-
ing women who have undergone total hysterectomy but they
obviously rely on incomplete data, indicating that a substan-
tial number of invitations are unnecessarily distributed annu-
ally. An immediate effect of this study is that routines to
exclude totally hysterectomized women from invitation for
screening have been improved in western Sweden. Thus, even
in a setting in which attempts have been made to systemati-
cally exclude hysterectomized women; this category of
women might constitute a substantial proportion of those
assumed to be at risk of cervical cancer.

The strengths of our study are the population-based,

randomized design and access to a database covering all cyto-
logical screening activities in the region. Data on earlier
smear-taking is thus reliable and includes all tests taken out-
side the screening program as well, in contrast to studies that
calculate participation based only on reports from organized

screening or self-reported interval since the last smear,

18,19

which tends to be underestimated.

31,37

In this study, previous

non-participation is defined as the absence of any smear,
within or outside the screening program. All Antenatal
Health Clinics in the region were involved, which increased
the study’s possibility to credibly demonstrate the effective-
ness of the telephone intervention. It is also a strength that
we can present detailed data of importance for implementing
the intervention as a clinical routine.

Requests for participation and reasons not to book an

appointment were not always asked for or documented by
the midwives. These parameters cannot be precisely quanti-
fied, but the variety of comments listed indicates a need for
multiple interventions to reach this group of non-attendees.
The conditions for making calls, e.g., the possibility to sched-
ule specific appointments and the number of women to be
called, varied. These are limitations but also a consequence of
measuring the effectiveness of the interventions related to an
existing screening program rather than experimental efficacy.

Our findings have general importance for prevention of cer-

vical cancer, regardless of the screening method. Investments in
more sophisticated screening tests such as liquid-based cytology
or HPV testing will have limited effect unless participation is
high. Very few advanced cervical cancers develop among
women who participate in screening, even with conventional
cytology.

9

The impact of a telephone call in this population

might seem somewhat more limited than in some other stud-
ies

16,18,19

but the intervention was undertaken in the context of

a program in which more convenient and cheap methods, such
as scheduled appointments, annual reminders and, to a limited
extent, re-booking on the Internet, have already been imple-
mented. Moreover, as we have shown that short follow-up du-
ration yields biased results, long-term follow-up (one year) and
calculations based on the entire target population (intention to
treat) in this study should yield more valid results.

Conclusions

Telephone contact with women, who have abstained from
cervical cancer screening for long time, increases participa-
tion. The intervention yields a significant increase in detected
and followed up atypical smears. This strategy of contacting
non-attending women by telephone, in the context of a well-
run screening program, is also practically feasible and does
not seem to increase costs.

Acknowledgements

The authors thank all the midwives involved in the study for conducting the
telephone calls.

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