Adherence to colorectal cancer screening: four rounds of faecal immunochemical test-based screening
British Journal of Cancer
Adherence to colorectal cancer screening: four rounds of faecal immunochemical test-based screening
Manon van der Vlugt 0
Esm e?e J Grobbee 1
Patrick MM Bossuyt 2
Evelien Bongers 3
Wolfert Spijker 4
Ernst J Kuipers 1
Iris Lansdorp-Vogelaar 5
Marie-Louise Essink-Bot 6
Manon C W Spaander 1
Evelien Dekker 0
0 Department of Gastroenterology and Hepatology, Academic Medical Centre, University of Amsterdam , Meibergdreef 9, Amsterdam 1105 AZ , The Netherlands
1 Department of Gastroenterology and Hepatology, Erasmus University Medical Centre , Gravendijkwal 230, Rotterdam 3015 CE , The Netherlands
2 Department of Clinical Epidemiology , Biostatistics and Bioinformatics , Academic Medical Center, University of Amsterdam , Meibergdreef 9, Amsterdam 1105 AZ , The Netherlands
3 Regional Organization for Population Screening Mid-West Netherlands , Hoogoorddreef 54 E, Amsterdam 1101 BE , The Netherlands
4 Regional Organization for Population Screening South-West Netherlands , Maasstadweg 124, Rotterdam 3079 DZ , The Netherlands
5 Department of Public Health, Erasmus University Medical Centre , Gravendijkwal 230, Rotterdam 3015 CE , The Netherlands
6 Department of Public Health, Academic Medical Center, University of Amsterdam , 's-Gravendijkwal 230, Amsterdam 3015 CE , The Netherlands
Background: The effectiveness of faecal immunochemical test (FIT)-based screening programs is highly dependent on consistent participation over multiple rounds. We evaluated adherence to FIT screening over four rounds and aimed to identify determinants of participation behaviour. Methods: A total of 23 339 randomly selected asymptomatic persons aged 50-74 years were invited for biennial FIT-based colorectal cancer screening between 2006 and 2014. All were invited for every consecutive round, except for those who had moved out of the area, passed the upper age limit, or had tested positive in a previous screening round. A reminder letter was sent to non-responders. We calculated participation rates per round, response rates to a reminder letter, and differences in participation between subgroups defined by age, sex, and socioeconomic status (SES). Results: Over the four rounds, participation rates increased significantly, from 60% (95% CI 60-61), 60% (95% CI 59-60), 62% (95% CI 61-63) to 63% (95% CI 62-64; P for trendo0.001) with significantly higher participation rates in women in all rounds (Po0.001). Of the 17 312 invitees eligible for at least two rounds of FIT screening, 12 455 (72%) participated at least once, whereas 4857 (28%) never participated; 8271 (48%) attended all rounds when eligible. Consistent participation was associated with older age, female sex, and higher SES. Offering a reminder letter after the initial invite in the first round increased uptake with 12%; in subsequent screening rounds this resulted in an additional uptake of up to 10%. Conclusions: In four rounds of a pilot biennial FIT-screening program, we observed a consistently high and increasing participation rate, whereas sending reminders remain effective. The substantial proportion of inconsistent participants suggests the existence of incidental barriers to participation, which, if possible, should be identified and removed.
CRC screening; faecal immunochemical test; participation; adherence; rescreening; uptake; colorectal cancer screening
Colorectal cancer (CRC) is a major cause of cancer-related death
(Jemal et al, 2011)
and its prognosis is largely dependent on stage
at diagnosis. Population-based CRC screening aims to detect CRC
in an early stage, and to detect and remove precursor lesions,
thereby reducing CRC morbidity and mortality
(Shaukat et al,
. Faecal occult blood test (FOBT)-based screening using
guaiac FOBT (gFOBT) has been shown to result in a reduction in
CRC-related mortality in a number of randomised controlled trials
(Mandel et al, 1993; Hardcastle et al, 1996; Kronborg et al, 1996)
with a 15% reduction in CRC-related mortality in a meta-analysis
(Hewitson et al, 2008)
In the last decade, several studies have shown that the
performance of the faecal immunochemical test (FIT) is superior
to that of gFOBT
(Allison et al, 2007; Hewitson et al, 2007; van
Rossum et al, 2008)
. Although FIT-based randomised controlled
trials with long-term follow-up are lacking, a recent observational
study demonstrated a 22% reduction in CRC mortality in areas,
where FIT-screening programs were implemented compared with
areas without screening
(Zorzi et al, 2015)
. However, FIT has a
relatively low sensitivity for CRC and its precursors, and one round
of FIT-screening results in a cancer miss rate of 12?25% depending
on the cutoff used
(de Wijkerslooth et al, 2012)
invitations are therefore usually repeated every 2 years, and the
effectiveness of a FIT-screening program is highly dependent on
participation in multiple rounds. Ideally, eligible invitees accept the
invitation to be screened in every screening round
participation; Gellad et al, 2011; Steele et al, 2013)
A high rate of consistent participation increases the program
sensitivity of FIT screening
(Winawer et al, 1993; Launoy et al,
1998; Zauber et al, 2012; Nishihara et al, 2013)
. On the other hand,
the succes of a biennial FIT-based screening program might be
overestimated if the willingness to participate in multiple rounds is
low. Knowing possible determinants of inconsistent participation
could help in targeting the information to specific groups. Previous
studies showed, for example, that especially socioeconomically
deprived persons are less likely to accept CRC-screening invitations
(Wee et al, 2005; Pornet et al, 2010, 2014; Moss et al, 2012;
Leuraud et al, 2013; Lo et al, 2015b)
Several studies on FOBT screening are available, usually
reporting on participation rates in a single round. We aimed to
examine patterns in participation in an invitational program of
biennial FIT-based screening over four screening rounds and to
identify possible predictors for consistent and inconsistent
MATERIALS AND METHODS
Study population/study design. This study was performed in
our ongoing pilot program of population-based CRC screening.
Details about the design of our program have been described
(van Rossum et al, 2008; Denters et al, 2013; Kapidiz
et al, 2014; Stegeman et al, 2015)
. In short, demographic data of
persons between 50 and 74 years living in the southwest and
northwest of The Netherlands were obtained from municipal
population registers. Selection of the regions in 2006 was based
on a known average uptake of invitees for the national breast
cancer screening program. For the southwest region, random
samples were taken from the target population by a
computergenerated algorithm (Tenalea, Amsterdam, The Netherlands).
In the northwest region random samples of selected postal code
areas were taken.
The study was conducted in a dynamic cohort. Persons in the
target age range that had moved into the targeted postal code area
at any time during the recruitment period were included, as well as
those that reached the lower age limit of 50 years.
No national screening program had been implemented at the
start of this pilot program, and thus the target population was
screening naive when first contacted. In the Netherlands, a national
FIT-based CRC screening program was gradually initiated from
January 2014 onwards. Invitees for our cohort were not invited for
the national program.
The selected persons were invited for each consecutive round,
except for those who had moved out of the area, those that had
passed the upper age limit, institutionalised people, invitees unable
to give informed consent, and those who had tested positive in a
previous screening round. In our information leaflet and in our
informed consent form, persons with a history of inflammatory
bowel disease, proctocolectomy, or CRC were advised not to
participate CRC screening, but report this reason for
nonparticipation back to our screening organisation via the informed
consent form. Participants reporting a colonoscopy in the past
2 years during intake after a positive FIT result were excluded from
further participation, as well as those with an estimated life
expectancy of o5 years.
Recruitment took place between June 2006 and December 2014
(first round from June 2006 to February 2007; second round from
August 2008 to June 2009; third round from February 2011 to
February 2012; and fourth round from March 2014 to December
2014). During the first round, invitees from the northwest region
were randomly allocated to receive either a gFOBT or a FIT as
screening test. Invitees who received a gFOBT in this first round
were excluded from our analyses.
Date of birth, sex, and postal codes of all invitees were collected
using the municipal population register. Socioeconomic status
(SES) was based on social status scores provided by the
Netherlands Institute of Social Research (www.scp.nl). The social status
score of a postal code area is based on the unemployment rate,
education level, average income, and position on the labour
market. Social status scores are available for almost all postal codes
in the Netherlands. The average status score of 0 and the s.d. in the
Netherlands in 2006 was used to divide persons into three
categories into high (status scores 40.96), average (status scores
between 0.96 and 0.96), and low SES (status scores o 0.96).
The first available postal code of the invitee was used to categorise
FIT screening. Every 2 years, all invitees received a
preannouncement letter about the screening program by mail,
followed 2 weeks later by an invitation kit containing an invitation
letter, information leaflet, and a single FIT device with testing
instructions. In the first, second, and third round, all invitees
received an OC-Sensor (Eiken Chemical Co, Tokyo, Japan) as a
FIT device. In the fourth round, invitees were randomised to
receive either an OC-Sensor (Eiken Chemical Co, Tokyo, Japan) or
a FOB Gold (Sentinel Diagnostics SpA, Milan, Italy). As no
differences in participation behaviour were seen between the two
tests, we included both arms in our analysis
(Grobbee et al, 2016)
The FIT devices were returned to one of our two selected
specialised laboratories and dates of return were registered. A test
positivity threshold of X10 mg Hb g 1 faeces was used. People
with a positive FIT result were referred for colonoscopy.
All non-responders received a reminder letter by mail after 2?6
weeks. Date of dispatch was registered. A positive response after
the reminder letter was defined as a FIT device arriving at the
laboratory 3 or more days after sending out the reminder letter.
This interval of 3 days was based on the mail system delivery times,
which maximally take 3 days between sending and delivering. Date
of dispatch of the reminder and date of return of the FIT device at
the laboratories were recorded for calculating return time.
Statistical analysis. The participation rate was calculated as the
number of participants relative to all eligible invitees. For each
screening round, we calculated participation rates per sex. For our
analyses of adherence to FIT screening, we only included invitees
who were eligible in at least two rounds to be able to observe the
three different screening patterns (see below).
Differences in screening behaviour were used to assign
participants to one of three groups: consistent participation
(i.e., attending all rounds when eligible), inconsistent participation
(i.e., attending at least once but less than the total times eligible),
and non-participants (not participating in any round of FIT
The percentage of consistent participants was defined as the
number of invitees attending all rounds, for which they were
eligible relative to the total number of invitees. The percentage of
inconsistent participation was defined, as the number of invitees
attending inconsistently relative to the total number of invitees.
Similarly, the percentage of non-participants was defined as the
number of invitees, who never responded to any of the screening
Differences in proportions between groups were evaluated for
statistical significance using the w2-test statistic. We evaluated
participation over rounds with the w2-test statistic for trend.
Differences in medians between groups were tested using the
Kruskal?Wallis test statistic. Po0.05 were considered to
correspond to statistically significant differences. Data analysis
was performed using SPSS22 for Windows (SPSS Inc., Chicago,
Ethics approval. The Dutch National Health Council approved
the study. All included screenees gave written informed consent to
participate in the study.
Population. Our dynamic cohort consisted of 23 339 invitees, of
whom 323 had to be excluded because they did not meet the
inclusion criteria; 49 invitees had moved out, 12 invitees had died,
and 262 invitees met one or more of the exclusion criteria
(see Materials and Methods section) leaving 23 016 eligible invitees.
Baseline characteristics of the eligible invitees are summarised in
Participation. Over the four rounds, participation rates increased
significantly, from 60% (95% CI 60?61), 60% (95% CI 59?60), 62%
(95% CI 61?63) to 63% (95% CI 62?64), respectively (Figure 1;
P for trend o0.001). Differences between men and women over
four rounds of FIT screening are shown in Figure 2, with
significantly higher participation rates for women in all four
Response after reminder
Response initial invite
Adherence to screening and determinants of adherence. A total
of 17 312 invitees were eligible for two or more rounds of FIT
screening (Table 2). In this group, 8271 invitees (48%) were
consistent participants and 4184 (24%) were inconsistent
participants. Overall, 12 455 (72%) invitees participated at least once,
whereas 4857 (28%) never participated in the FIT-screening
program. Of the 8795 invitees that were eligible for all four rounds,
4345 (49%) participated in four rounds, 2370 (27%) in one or more
rounds, and 2080 (24%) participated in none.
Table 3 lists the differences between consistent, inconsistent,
and non-participants. Consistent participants were significantly
older, more often female, and more likely to have a high SES.
Reminder letter. In the first screening round, 49% (95% CI
48?49) of the invitees responded within the first 2?6 weeks after
receiving the initial invitation kit, and 12% (95% CI 11?12)
participated after having been sent a reminder letter (Figure 1).
The percentage of participants responding to the initial invitation
increased after the first round, with participation rates of 50%,
56%, and 54% for the second, third, and fourth round, respectively.
An additional uptake of up to 10% was observed after sending a
reminder letter (Figure 1) within each round. On average, the FIT
devices were returned within 15 days after sending a reminder
letter (first round after 12 days (IQR 7?21); second round after
13 days (IQR 7?32); third round after 15 days (IQR 8?27); and
fourth round after 14 days (IQR 7?28)).
In four rounds of a pilot biennial FIT-screening program,
we observed consistently high and increasing participation rates
of 60?63% in each round. Sending a reminder letter after an initial
non-response resulted in an increased participation rate, adding
10?12% in each screening round. Almost half of the invitees that
were eligible for two or more screening rounds were consistent
participants, while almost a quarter never participated. Consistent
participants were typically older, more often female, and more
likely to have a high SES.
Strengths of our study include that our large cohort consists of
an average risk population, comprising all the age ranges that are
usually invited for CRC-screening programs worldwide. This
population was screen naive when first approached, without the
presence of any other CRC-screening initiatives in the population.
Moreover, it covers four FIT-based screening rounds, although the
majority of long-term studies so far were based on gFOBT-based
Abbreviations: CRC ? colorectal cancer; FIT ? faecal immunochemical test. Analysis restricted to invitees who were eligible at least two screening rounds. Highlighted light purple blocks
represent consistent participation.
screening. However, some study limitations have to be
acknowledged. SES could only be assigned by postal code, as a proxy for
individual-level SES. Regrettably, no data were available on the
ethnicity of all invitees, nor their marital status, both factors that
could also be associated with participation
(El-Haddad et al, 2015)
Our pilot program started in 2006, at a time when general
awareness of CRC and CRC screening in The Netherlands was
limited. That awareness has likely increased over time, especially
after 2014, when a national Dutch CRC-screening program was
launched. This might have positively affected participation rates in
the third and fourth screening round in our pilot program.
Moreover, in 2006, we selected our cohort based on uptake data
from our national breast cancer screening program that has been
implemented in 1990. We selected postal code areas within our
regions with a known average uptake in breast cancer screening.
This could have resulted in the relatively low proportion of low SES
in our cohort.
Similar participation rates, ranging between 56 and 63%, have
been reported for a pilot study over four rounds of biennial FIT
screening in Italy
(Crotta et al, 2012)
. Our percentage of consistent
participants are in line with these data. Studies reporting on
adherence to FIT screening over a longer time interval are scarce
(Crotta et al, 2012; Kapidzic et al, 2014; Jensen et al, 2016)
reports are based on studies using gFOBT, reporting consistent
adherence rates over multiple rounds, ranging from 39?44%
(Steele et al, 2013; Pornet et al, 2014; Lo et al, 2015a)
As in several studies, women were more likely to participate in
our FIT-screening program than men. A study from the United
Kingdom also described sex differences in participation within a
gFOBT-screening pilot consisting of three rounds
(Moss et al,
. Denis et al (2015) reported an overall 6% higher
participation rate for women in a first screening round within a
gFOBT-screening program that consisted of four rounds, with a
gradually decreasing difference over time. In contrast to these
studies, the sex difference in our study remained comparable and
significantly different, though this difference was small. A possible
explanation could be that women are generally more familiar with
the concept of screening. In The Netherlands, women are invited
for cervical cancer screening every five years, since 1996
(invitations between the age of 30?60 years), and for breast cancer
screening every 2 years, since 1990 (invitations between the age of
50?75 years). So far, no other national screening programs have
targeted men. Yet the fact that the difference between participation
in men and women did not decrease over four rounds, in contrast
to what Denis et al reported, suggests that there may be other
factors involved. Possibly, men are less likely to respond the mailed
invitations as compared to women and would, for instance,
endorsement of the test by their general practitioner encourage
them to participate.
A higher SES and older age were also significantly associated
with consistent participation. These determinants for adherence to
FIT screening are comparable with those in the previously reported
one-time FOBT-screening studies and gFOBT-based
(Wee et al, 2005; Pornet et al, 2010, 2014; Moss et al,
2012; Leuraud et al, 2013; Hurtado et al, 2015; Lo et al, 2015b)
Pornet et al compared occasional participants with compliant
participants in a gFOBT-screening program and also reported that
occasional adherence was positively associated with living in
socioeconomically deprived areas.
Response times for participation varied over screening rounds,
with prompter participation in later screening rounds. A potential
explanation could be that most invitees grew familiar with the
program and the FIT as a screening test over successive rounds,
thereby lowering the barrier to participate and to perform the test.
An alternative, additional factor could be the increased awareness
of CRC and CRC screening over time.
Response rates further increased after sending reminder letters
to non-participants, and this effect was seen in each of the four
rounds. Previous one-time screening studies with varying intervals
for sending reminder letters also showed a positive effect on uptake
from sending a reminder letter
(Baron et al, 2008)
Santare et al
) reported a very high proportion of 29% FIT devices
returned (OC-Sensor) after sending a reminder letter after 21 days,
but this was studied in Latvia, which has an opportunistic
screening program with very low uptake (7.6%).
Tinmouth et al
) reported a 9.7% increase in participation after sending a
reminder letter in a gFOBT-based CRC screening after 6 months.
Participation rates doubled after sending a new gFOBT kit. Our
results indicate that sending a reminder letter to all non-responders
after 6 weeks, in every screening round, consistently results in a
positive contribution to overall participation and that reminders
remain effective over multiple rounds.
About one in four invitees eligible for more than one round
participated once or more often, but not in all screening rounds for
which they had been invited. This indicates that the decision to
participate in screening is not always the outcome of a one-time
assessment. It is possible that eligible citizens change their
behaviour in time, and one must acknowledge that also practical
issues, such as work-related responsibilities, could prevent
Although screening uptake was high and increased over rounds,
and about half of the FIT invitees were consistent participants,
almost a quarter of the invitees never participated in any of the
rounds of FIT screening. It would be relevant to investigate
whether these invitees made an informed decision not to
participate, or whether participation was hampered by barriers,
such as limited health literacy, distrust of government initiated
health initiatives, cost considerations, or other issues. Health
literacy is an individual?s capacity to obtain, process, and
understand basic health information and services needed to make
appropriate health decisions. Limited health literacy has been
shown to be associated with a restricted use of preventive health
services, such as cancer screening
(Kobayashi et al, 2014)
A questionnaire study performed in the second round of our pilot
program of FIT screening showed that one of the more frequently
reported reasons for non-participation in FOBT screening was lack
of abdominal complaints, which suggests limitations in CRC
knowledge in this group
(Denters et al, 2015)
. Adequate CRC
knowledge was found to be a strong predictor for participation in
(van Dam et al, 2013)
. It is conceivable that we
need to diversify our invitation and information strategy, taking
into account differences between groups, to achieve equity,
enabling men and women, in all age groups, and socioeconomic
layers, in making well-informed decisions about participation in
We thank The Netherlands Organization for Health Research and
Development of the Dutch Ministry of Health (ZonMW) for
funding (project numbers 120710007, 63000004, 12010095420, and
200340001). Also, we acknowledge Karin de Groot, research nurse,
for her professional work. The authors especially thank Mieke
Janssen and Kirsten Izelaar, and all involved co-workers of the
Regional Organization for Population Screening Mid-West and
South-West (Bevolkingsonderzoek MiddenWest,
Bevolkingsonderzoek ZuidWest) for their important contributions to the study. The
Netherlands Organisation for Health Research and Development
of the Dutch Ministry of Health was not involved in the analysis
and interpretation of the data nor in the writing of the manuscript
or decision to submit the paper.
CONFLICT OF INTEREST
The authors declare no conflict of interest.
M van der Vlugt: study concept and design, acquisition of data;
analysis and interpretation of data; drafting of the manuscript; and
statistical analysis. EJ Grobbee: study concept and design; and
analysis. Critical revision of the manuscript for important
intellectual content. PMM Bossuyt: study concept and design;
and statistical analysis. Critical revision of the manuscript for
important intellectual content. E Bongers: made substantial
contributions to the acquisition of data. Critical revision of the
manuscript for important intellectual content. W Spijker: made
substantial contributions to the acquisition of data. Critical
revision of the manuscript for important intellectual content.
EJ Kuipers: study concept and design. Critical revision of the
manuscript for important intellectual content. I
LansdorpVogelaar: study concept and design. Critical revision of the
manuscript for important intellectual content. M-L Essink-Bot:
study concept and design. Critical revision of the manuscript for
important intellectual content. MCW Spaander: study concept and
design. Contributed to the acquisition of data. Critical revision of
the manuscript for important intellectual content. E Dekker: study
concept, and design and interpretation of data. Contributed to the
acquisition of data. Critical revision of the manuscript for
important intellectual content.
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