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REGULAR ARTICLE
Use of Two Self-referral Reminders and a Theory-Based Leaet to
Increase the Uptake of Flexible Sigmoidoscopy in the English Bowel
Scope Screening Program: Results From a Randomized Controlled
Trial inLondon
Robert S.Kerrison, MSc1 • Lesley M.McGregor, PhD1 • NicholasCounsell, MSc2 • SarahMarshall, BA3 •
AndrewPrentice, MSc3 • JohnIsitt, BA4 • Colin J.Rees, FRCP5 • Christianvon Wagner, PhD1
Published online: XX XXXX 2018
© The Society of Behavioral Medicine 2018
This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/
by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
Abstract
Background We previously initiated a randomized con-
trolled trial to test the effectiveness of two self-refer-
ral reminders and a theory-based leaflet (sent 12 and
24months after the initial invitation) to increase participa-
tion within the English Bowel Scope Screening program.
Purpose This study reports the results following the sec-
ond reminder.
Methods Men and women included in the initial sam-
ple (n=1,383) were re-assessed for eligibility 24months
after their invitation (12months after the first reminder)
and excluded if they had attended screening, moved
away, or died. Eligible adults received the same treat-
ment they were allocated 12 months previous, that is,
no reminder (“control”), or a self-referral reminder with
either the standard information booklet (“Reminder and
Standard Information Booklet”) or theory-based leaflet
designed using the Behavior Change Wheel (“Reminder
and Theory-Based Leaflet”). The primary outcome was
the proportion screened within each group 12 weeks
after the second reminder.
Results In total, 1,218 (88.1%) individuals were eligible.
Additional uptake following the second reminder was
0.4% (2/460), 4.8% (19/399), and 7.9% (29/366) in the
control, Reminder and Standard Information Booklet,
and Reminder and Theory-Based Leaflet groups, respec-
tively. When combined with the first reminder, the
overall uptake for each group was 0.7% (3/461), 14.5%
(67/461), and 21.5% (99/461). Overall uptake was signifi-
cantly higher in the Reminder and Standard Information
Booklet and Reminder and Theory-Based Leaflet groups
than in the control (odds ratio [OR]=26.1, 95% confi-
dence interval [CI]=8.1–84.0, p<.001 and OR=46.9,
95% CI=14.7–149.9, p<.001, respectively), and signifi-
cantly higher in the Reminder and Theory-Based Leaflet
group than in the Reminder and Standard Information
Booklet group (OR=1.8, 95% CI=1.3–2.6, p<.001).
Conclusion A second reminder increased uptake among
former nonparticipants. The added value of the theo-
ry-based leaflet highlights a potential benefit to review-
ing the current information booklet.
Trials Registry Number ISRCTN44293755.
Keywords Colorectal cancer • Screening • Uptake •
Flexible sigmoidoscopy • Behavioral science
Robert Kerrison
robert.kerrison.13@ucl.ac.uk
1 Research Department of Behavioural Science and Health,
University College London, London, UK
2 Cancer Research UK & UCL Cancer Trials Centre,
University College London, London, UK
3 St Mark’s Bowel Cancer Screening Centre, St Mark’s
Hospital, Middlesex, UK
4 Partners in Creation, Top Studio, London, UK
5 South Tyneside NHS Foundation Trust, South Tyneside
School of Medicine, Pharmacy and Health, Durham
University, Durham, UK
ann. behav. med. (2018) XX:1–11
DOI: 10.1093/abm/kax068
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Introduction
Colorectal cancer is a leading cause of morbidity and
mortality throughout the world [1]. Several large rand-
omized controlled trials have shown that a single flex-
ible sigmoidoscopy screen between the ages of 55 and
64 can significantly reduce the incidence and mortality
of the disease among people who complete the test [2].
As a result, several countries have begun piloting flexible
sigmoidoscopy-based screening programs for the pre-
vention of colorectal cancer [3], with England currently
rolling out a national program (referred to as the Bowel
Scope Screening program) set to reach full population
coverage in2018.
One of the key determinants of successful screening
programs is the ability to achieve high population up-
take. In England, all screening and treatment is offered
automatically and free of charge through the National
Health Service. However, despite being offered automat-
ically and for free, the uptake of bowel scope screening is
both low and socioeconomically graded [4]. One recent
study found that only 43% of men and women invited
for bowel scope screening during the initial implementa-
tion of the program attended an appointment, and that
uptake was lowest among individuals living in the most
deprived areas (uptake ranged from 32% in the most
deprived areas to 52% in the least deprived) [4]. This is
not a problem exclusive to the UK [5]. In the USA, for
example, nearly half (48%) of eligible adults are not up
to date with screening recommendations, despite avail-
able guidelines and evidence demonstrating their effect-
iveness [6].
As with other screening programs, the National
Health Service bowel scope screening program incorpo-
rates specific strategies to maximize uptake (e.g., preno-
tification letters, reminder letters, timed appointments)
[7–9]. Invitees receive a prenotification letter shortly
after their 55th birthday. They then receive an invitation
with a timed appointment 2 weeks thereafter. Anyone
who does not respond to their invitation within 2weeks
is sent a reminder. If there is no response within an add-
itional 2weeks, the appointment is cancelled, and the in-
dividual is notified via direct mail. Anyone who confirms
an appointment, but does not attend, is similarly noti-
fied. In both cases, the recipient is informed that they can
self-refer for bowel scope screening up until age of 60,
when they are eligible for a fecal occult blood test once
every 2years up until the age of74.
Previous research exploring nonparticipation and
decision making in the English Bowel Scope Screening
program has identified a number of barriers to uptake,
including “a perceived or actual lack of need to have the
test”, “an inability to attend the appointment offered”,
and “a lack of understanding about the harms and bene-
fits of screening” [10]. One of the subsequent suggestions
to improve uptake has been to send nonparticipants an
additional reminder at a later date [10], and already there
is some evidence to suggest that this may be effective [11].
We ourselves have previously examined the feasi-
bility of sending bowel scope screening nonparticipants
a reminder letter and leaflet 12 months after their ini-
tial invitation [11]. More specifically, we have previously
investigated the feasibility of sending nonparticipants a
theory-based leaflet (designed according to principles put
forth by the Behavior Change Wheel) [12] and reminder
letter (hereafter referred to as a “self-referral reminder”)
that gave instructions for how to self-refer and included
options for the day and time of the appointment and the
gender of the practitioner performing the test [11]. On
the basis that: (i) the reminder letter and leaflet could be
implemented and (ii) would be more effective if sent a
second time (i.e., 24months after the initial invitation)
[13–15], we performed a formal randomized controlled
trial to test their effectiveness against usual care (i.e., no
reminder).
Results from the first stage of the randomized con-
trolled trial (i.e., the first reminder) demonstrated that
sending nonparticipants a single self-referral reminder,
12 months after their initial invitation, significantly
increased participation against usual care, and that
reminders were more effective when sent with the theo-
ry-based leaflet, as opposed to the standard information
booklet used by the bowel scope screening program [16].
Results from the second stage of the randomized con-
trolled trial have not previously been examined.
This study reports the “additional” and “overall” up-
take of bowel scope screening following the second re-
minder. Our specific aims were to (i) examine whether
a second self-referral reminder increased the uptake
of screening among former nonparticipants; (ii) assess
the cumulative effect of the two self-referral reminders
combined; and (iii) test whether the effect of the theo-
ry-based leaflet on participation was sustained after the
delivery of a second reminder.
Methods
Study Population, Design, and Trial Setting
We performed a single-blinded, randomized, controlled
trial with three parallel arms in the London boroughs
of Brent and Harrow. One thousand three hundred and
eighty-three men and women randomly selected from a
weekly variable total of nonparticipants were randomized
(using simple pseudo-random allocation methods) to
receive either (1:1:1) no reminder (control, n = 461), a
12-month self-referral reminder and standard infor-
mation booklet (Reminder and Standard Information
Booklet, n =461), or a 12-month self-referral reminder
and theory-based leaflet designed using the Behavior
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Change Wheel (Reminder and Theory-Based Leaflet,
n = 461). Anyone who did not attend an appointment
within 12weeks of being sent the 12-month reminder (or
no reminder in the case of the control) was re-assessed
for eligibility 24months after their initial invitation (i.e.,
12months after the first reminder). Individuals who had
(i) taken part in screening, (ii) registered with a general
practice outside of the London boroughs of Brent and
Harrow, or (iii) died were excluded. The remaining popu-
lation were considered “eligible” and assigned to receive
the same treatment they received 12months previous.
Because individuals were assigned to receive no re-
minder or a self-referral reminder with one of two leaf-
lets, it was not possible to blind them to the treatment
they received. In terms of the study setting, the London
boroughs of Brent and Harrow have below-average up-
take and contain some of the most ethnically diverse and
socioeconomically deprived areas in England [17].
Procedures
Eligibility was re-assessed using routine data stored on
the National Health Service Bowel Cancer Screening
System: an electronic system that provides up-to-date up-
take data for individuals enrolled in the national screen-
ing program [18]. Individuals in both reminder groups
were able to book an appointment by returning an
“appointment-request-slip” to St Mark’s Bowel Cancer
Screening Centre (the screening center where appoint-
ments for people living in Brent and Harrow take place),
thereby initiating a call from a member of the admin-
istrative team to arrange an appointment, or by calling
the screening center directly on the Freephone number
provided in the reminder letter. Anyone not responding
to the “24-month” self-referral reminder within 4weeks
was sent a “follow-up” reminder, which also included
an appointment-request slip, the allocated information
leaflet, and a Freepost return envelope addressed to St
Mark’s Bowel Cancer Screening Centre. Individuals
were given an additional 8weeks to respond before their
attendance was assessed on the Bowel Cancer Screening
System. Anyone referring for an appointment after this
time was excluded from the study results, but was still
offered an appointment. Individuals who referred for
bowel scope screening were sent a pre-appointment text
message and telephone call (where a mobile/home tele-
phone number was available), as per routine practice.
Intervention Development
The intervention strategy was informed by the Behavior
Change Wheel [12], which was used (in conjunction with
the Behavior Change Technique Taxonomy [19]) to iden-
tify the putative targets for change and the behavior
change techniques likely to affect those targets. We began
by defining the problem in behavioral terms (see online
Supplementary material for the completed worksheets),
before selecting and specifying the target behavior and
identifying what needed to change (in COM-B terms) for
the behavior to occur. We then identified the intervention
functions and policy categories that would be most likely
to bring about the desired change and reviewed the pos-
sible behavior change techniques and modes of delivery
that could be used to deliverthem.
After identifying the intervention strategy (Table 1),
we developed the intervention content. We did this by
the following methods: (i) reviewing the literature exam-
ining the perceived barriers and benefits of screening, (ii)
interviewing previously screened adults, and (iii) contact-
ing the local primary care cancer leads to obtain a local
primary care endorsement. An overview of these activi-
ties and how they were used to develop the intervention
content/deliver the behavior change techniques under-
pinning the intervention strategy is provided in Table2.
Initial versions of the intervention materials were
developed by Partners in Creation: a social marketing
company that specializes in the development of health be-
havior change interventions [20]. We provided them with a
Table1 Summary of the intervention strategy arrived at through the behavior change wheel intervention design process
Intervention functions
COM-B components
served by the intervention
functions
Selected behavior change
techniques
Policy categories through which
behavior change techniques can be
delivered Mode of delivery
Modeling Social opportunity Demonstration of the
behavior
Adding objects to the
environment
Prompts/cues
Credible source
Information about health
consequences
Instruction on how to per-
form behavior
Pros and cons
Communication/marketing Leaets
Environmental
restructuring
Physical opportunity
Social opportunity
Persuasion Reective motivation
Education Psychological capability
Reective motivation
Enablement Psychological capability
Physical opportunity
Social opportunity
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brief outlining the intervention strategy/content described
in Tables 1 and 2. The drafted materials were then tested
in a co-design workshop in which screening eligible adults
from the London boroughs of Brent and Harrow (n=4;
3 men, 1 woman; aged 55–58years) gave feedback to in-
form future iterations of the materials. Revised versions
were then presented to individuals who were either the
eligible age or approaching the eligible age for screening
(n=20; 12 women, 8 men, aged 50–59years) and feed-
back obtained through interviews conducted by a member
of the University College London (UCL) research team.
The final materials used in the trial are described under
Intervention Development.
24-Month reminder
The 24-month reminder was a personally addressed letter
from St Mark’s Bowel Cancer Screening Centre that
invited recipients to make an appointment by returning
an “appointment-request-slip” or calling the Freephone
number for St Mark’s Bowel Cancer Screening Centre
(see online Supplementary material). The reminder also
gave recipients the option to express a preference for the
day and time of the appointment and the gender of the
practitioner performing the test.
Theory-based leaet
The theory-based leaflet was a locally tailored leaflet
designed to promote bowel scope screening attendance
at St Mark’s Hospital in London. The leaflet included
testimonials from individuals previously screened at the
center, as well as a primary care endorsement of the
screening test and a list of the benefits of having the test
(see online Supplementary material).
Follow-up reminder
The follow-up reminder was a personally addressed
letter from St Mark’s Bowel Cancer Screening Centre
that reiterated the opportunity to self-refer for screen-
ing up until the age of 60 (see online Supplementary
material). It was included on the basis that additional
reminders/prompts have been shown to have benefits
over and above those of single reminders used by them-
selves [21]. The timing for the follow-up reminder was
based on the program reminder, which is sent 4weeks
after the first contact.
Standard information booklet
The standard information booklet was the same 16-page
booklet sent with the initial invitation as part of the na-
tional screening program (available from https://www.
gov.uk/government/uploads/system/uploads/attach-
ment_data/file/423928/bowel-scope-screening.pdf). The
standard information booklet was developed by King’s
Health Partners, who developed the booklet in accord-
ance with the principles put forth by England’s National
Health Service informed choice initiative [22].
Table2 Overview of the intervention design
Behavior change technique Denition Examples of use
Pros and cons Advise the person to identify reasons for
wanting (pros) or not wanting (cons) to
change behavior
A list of the benets of bowel scope screening was added
to the leaet
Demonstration of the
behavior
Provide an observable sample of the
performance of the behavior, directly in
person or indirectly (e.g., via lm, pictures)
for the person to aspire to or imitate
Testimonials of people who had performed the behavior
were added to the leaet
Credible source Present verbal or visual communication from a
credible source in favor or against the
behavior
A primary care endorsement from the General Practice
Cancer Lead endorsing the National Health Service
Bowel Scope Screening program was added to the
leaet
Prompts/cues Introduce or dene environmental or social
stimulus with the purpose of prompting
or cueing the behavior. The prompt or cue
would normally occur at the time or place of
performance
A prompt was added to the intervention strategy by
developing a “self-referral” reminder letter and a
“follow-up” reminder letter
Instruction on how to
perform a behavior
Advise or agree on how to perform a behavior Instructions on how to self-refer for bowel scope screen-
ing were added to the reminder letter
Adding objects to the
environment
Add objects to the environment in order to
facilitate performance of the behavior
Several “objects” or facilitators were added to the re-
minder letters, including an “appointment-request
slip” and a Freepost return envelope
Information about health
consequences
Provide information (e.g., written, verbal,
visual) about health consequences of
performing the behavior
Information about the health consequences of bowel
scope screening (e.g., reduced risk of colorectal cancer
incidence and death) was added to the reminder letters
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Measures
Routinely available data stored on the Bowel Cancer
Screening System were used to verify self-referral and
attendance 4 and 12weeks following the distribution
of the 24-month self-referral reminder letter. The
Bowel Cancer Screening System was also consulted to
obtain the eligibility of each person, as well as their
gender (male, female), area (Brent, Harrow), and ini-
tial episode status (did not respond, did not attend).
For individuals who self-referred for an appointment,
the Bowel Cancer Screening System was additionally
consulted to obtain the method of referral (by letter,
by telephone) and whether they received a pre-ap-
pointment text message and/or telephone call (coded
as “received a pre-appointment reminder: yes/no”).
Lastly, for individuals who attended an appointment,
the Bowel Cancer Screening System was consulted to
obtain the clinical outcome and thereby the proportion
of people who had one or more precancerous lesions
(adenomas) detected.
An area-based socioeconomic deprivation score was
generated for each person by converting their postcode
into a score on the 2010 Index of Multiple Deprivation
[23]. Area-level Index of Multiple Deprivation scores
were then categorized into tertiles of their regional dis-
tributions to enable comparisons between the most and
least deprived areas.
SampleSize
The primary outcome was the overall uptake of screen-
ing within each group 12weeks after the delivery of the
second reminder (sent 24 months after the initial invi-
tation). Asample size of 420 men and women per trial
arm was required to detect a difference in uptake from
10.7% to 17.7% [24] in the Reminder and Standard
Information Booklet and Reminder and Theory-Based
Leaflet groups, respectively (α=0.05; β=0.2). This was
increased to 460 per arm to account for dropout during
reminder intervals, giving a total sample size require-
ment of n=1,380.
Analysis
The number and percentage of patients screened within
12weeks of the second reminder are presented with two-
sided 95% confidence intervals (CIs), constructed using
exact methods based on the binomial distribution. Odds
ratios (ORs), adjusted ORs (aORs), and 95% CIs com-
paring the uptake in each group were calculated using
univariable and multivariable logistic regression to adjust
for baseline characteristics. Bonferroni corrections and
an adjusted significance level of 0.015 were used to
account for multiple comparisons. Subgroup analyses
were carried out to explore possible associations between
not attending a confirmed appointment and (i) baseline
characteristics, (ii) method of referral, and (iii) receipt
of a pre-appointment text/telephone call. The adenoma
detection rate was reported using descriptive statistics.
The cumulative data were analyzed on an intention-to-
treat basis using SPSS (ver.24).
Cost Analysis
We calculated the cost per additional attendee by divid-
ing the cost of the self-referral reminder and follow-up
reminder (with the standard information booklet and
theory-based leaflet separately) by the number of people
who attended screening at 12 and 24 months. We also
performed a sensitivity analysis by calculating the range
of variation of the cost estimates within the CIs of the
participation rates (calculated using exact methods based
on the binomial distribution).
Ethics
The study was approved by the North-East Tyne &
Wear South Research Ethics Service (Ref: 15/NE/0043)
and was registered with the International Standard
Randomized Controlled Trials Number Registry for
transparency (trial ID: ISRCTN44293755).
Results
Sample Characteristics
This study took place between February and August,
2016, with follow-up until October, 2016. In total,
1,264 (91.4%) out of 1,383 men and women from the
initial sample were re-assessed for inclusion in this
analysis (Fig. 1). One hundred and nineteen (8.6%)
were known to have already taken part in screening
and were not assessed for this reason. Of the 1,264
adults who were re-assessed, 8 (0.6%) had died, and 38
(2.8%) were no longer registered with a general prac-
tice in the London boroughs of Brent and Harrow,
leaving a total sample size of 1,218 men and women
who were eligible for inclusion across all three study
groups (control, n = 453; Reminder and Standard
Information Booklet, n=399; Reminder and Theory-
Based Leaflet, n=366).
The basic attributes of each group are presented in
Table 3. All participants were aged 57 because of the
study design. Most (53.4%) were females (n = 650),
registered with a general practice in the London borough
of Brent (n=816; 67.0%), and did not respond to the ini-
tial invitation (n=1,072, 88.0%).
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Uptake (24-Month Reminder)
In total, 50 (4.1%) men and women who received the
24-month reminder attended a screening appointment
across all three study groups. A further 7 (0.6%) made
an appointment, but either did not attend (n=4) or can-
celled (n=3), leaving 1,161 (95.3%) individuals who nei-
ther made nor attended an appointment.
The percentage of people who booked and attended
an appointment within each group was 0.4% (n=2, 95%
CI=0.0–1.6), 4.8% (n=19, 95% CI=2.9–7.3), and 7.9%
(n = 29, 95% CI = 5.4–11.2) in the control, Reminder
and Standard Information Booklet, and Reminder and
Theory-Based Leaflet groups respectively. Sending a
second self-referral reminder 24months after the initial
invitation therefore further increased screening uptake
and was significantly more effective than usual care.
Uptake (12- and 24-Month Reminder Combined)
In the combined data, we found that 169 (12.2%) men
and women had booked and attended an appoint-
ment across all three study groups (Table4). Afurther
43 (3.1%) made an appointment, but subsequently did
not attend (n=25) or canceled (n = 18), leaving 1,171
(84.7%) who neither made nor attended an appointment.
There was strong evidence of differences in booked and
attended appointments between the reminder groups and
the control (Table5). Atotal of 67 individuals (14.5%)
in the Reminder and Standard Information Booklet
group and 99 individuals (21.5%) in the Reminder and
Theory-Based Leaflet group attended an appointment,
compared with only 3 (0.7%) in the control (OR=25.96,
95% CI = 8.10–83.18, p < .001 and OR = 41.75, 95%
CI = 13.13–132.76, p < .001 for the Reminder and
Standard Information Booklet and Reminder and
Theory-Based Leaflet groups, respectively). There was
also strong evidence of a difference in uptake between
the reminder groups, with individuals in the Reminder
and Theory-Based Leaflet group being significantly
more likely to attend an appointment than individuals in
the Reminder and Standard Information Booklet group
(OR=1.61, 95% CI=1.14–2.26, p=.006).
Results were similar after adjusting for baseline
characteristics in the multivariable analysis (Table 5),
with strong evidence of differences in uptake between
Fig.1. CONSORT diagram.
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the reminder groups and the control (Reminder and
Standard Information Booklet vs. control: aOR=26.14,
95% CI = 8.14–83.95, p < .001; Reminder and
Theory-Based Leaflet vs. control: aOR = 46.91, 95%
CI=14.68–149.93, p<.001). After adjusting for base-
line characteristics, there remained a significant dif-
ference in participation between intervention groups,
with individuals in the Reminder and Theory-Based
Leaflet group being more likely to book and attend
an appointment than individuals in the Reminder and
Standard Information Booklet group (aOR=1.80, 95%
CI=1.26–2.55; p<.001). There was also strong evidence
of a difference in uptake by initial episode status after
adjusting for study group and other baseline character-
istics, with former nonattenders (i.e., people who did not
attend) being more likely to book and attend an appoint-
ment than former nonresponders (i.e., people who did
not respond); uptake was 11.4% and 20.3%, respectively
(aOR=2.60, 95% CI=1.55–4.36; p<.001). There was
no evidence of an association between screening uptake
and gender, regional Index of Multiple Deprivation ter-
tile, or area (Table6).
Confirmed Appointments (12- and 24-Month Reminder
Combined)
A total of 43 individuals booked an appointment but did
not attend. Asignificant difference in attendance among
people who self-referred was observed between men and
women (84.4% vs. 74.5%), with men being more likely to
attend their appointment than women (aOR=2.06, 95%
CI=1.01–4.23, p=.05). A similar difference in uptake
was observed between people who received a pre-appoint-
ment reminder and people who did not (83.6% vs. 73.6%),
although this did not reach statistical significance in the
multivariable analysis (aOR=1.70; 95% CI=0.84–3.44,
p= .14). There was no evidence of differences in nonat-
tendance for any of the other variables included in the
analysis, including initial episode status, method of refer-
ral and area (see online Supplementary material).
Adenoma Detection Rate (12- and 24-Month Reminder
Combined)
Of the 169 men and women who attended an appoint-
ment and were screened, 14 (8.3%) had one or more ade-
nomas detected, 7 of whom had adenomas that met the
clinical criteria for colonoscopy and subsequently under-
went further examination. One person was diagnosed
Table3 Baseline characteristics
Control
(n=453)
Rem-SIB
(n=399)
Rem-TBL
(n=366)
Total
(n=1,218)
χ2
(p Value)
Gender n (%)
Female 255 (56.3) 213 (53.4) 182 (49.7) 650 (53.4) 3.51
(.173)
Male 198 (43.7) 186 (46.6) 184 (50.3) 568 (46.6)
Area n (%)
Brent 300 (66.2) 259 (64.9) 257 (70.2) 816 (67.0) 2.62
(.269)
Harrow 153 (33.8) 140 (35.1) 109 (29.8) 402 (33.0)
Tertile of deprivation (Index of Multiple Deprivation Score) n (%)
Tertile 1
(0.00–17.68)
148 (32.7) 128 (32.1) 104 (28.4) 380 (31.2) 2.14
(.710)
Tertile 2
(17.69–27.50)
164 (36.2) 141 (35.3) 142 (38.8) 447 (36.7)
Tertile 3
(27.51–80)
137 (30.2) 126 (31.6) 115 (31.4) 378 (31.0)
Missing 4 (0.9) 4 (1.0) 5 (1.4) 14 (1.1)
Initial episode status n (%)
Initial nonresponder 404 (89.2) 342 (85.7) 326 (89.1) 1,072 (88.0) 2.98
(.226)
Initial nonattender 49 (10.8) 57 (14.3) 40 (10.9) 146 (12.0)
Rem-SIB Reminder and Standard Information Booklet; Rem-TBL Reminder and Theory-Based Leaet.
Table4 Uptake at 12 and 24months by trial arm
Uptake % (95% CI)
12Months 24Months
Control (n=461) 0.2 (0.0%–1.2%) 0.7 (0.2%–2.0%)
Rem-SIB (n=461) 10.4 (7.8%–13.6%) 14.5 (11.4%–18.1%)
Rem-TBL (n=461) 15.2 (12.1%–18.8%) 21.5 (17.8%–25.5%)
CI condence interval; Rem-SIB Reminder and Standard
Information Booklet; Rem-TBL Reminder and Theory-Based
Leaet.
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with cancer and was referred for treatment because
of their diagnosis. In the multivariable regression (see
online Supplementary material), there were no statisti-
cal differences in the proportion of individuals who had
adenomas detected by trial arm or baseline characteris-
tics (all p values >.05).
Costs
The estimated cost of the interventions per additional
person attending screening at 12 months were £8.37
(range: £6.38–£11.17) in the Reminder and Standard
Information Booklet group and £8.75 (range: £7.05–
£11.14) in the Reminder and Theory-Based Leaflet
group (see online Supplementary material for a break-
down of the intervention costs for each group). Costs
for both interventions were significantly higher at
24 months (95% CIs did not overlap), with at an esti-
mated cost per additional person attending screening
of £18.31 (range: £12.00–£29.00) in the Reminder and
Standard Information Booklet group and £16.93 (range:
£11.97–£24.55) in the Reminder and Theory-Based
Leaflet group (see online Supplementary material for a
breakdown of the intervention costs).
Discussion
The results of this study provide strong evidence to sup-
port the use of a second self-referral reminder within
the National Health Service bowel scope screening
program and highlight an additional benefit to includ-
ing a bespoke theory-based leaflet designed using the
Behavior Change Wheel (the overall uptake was 0.7%,
14.5%, and 21.5% in the control, Reminder and Standard
Information Booklet and Reminder and Theory-Based
Leaflet groups, respectively).
At the current rate of attendance (43%) [4], the inclu-
sion of two self-referral reminders within the National
Health Service bowel scope screening program would
increase uptake by ~8–12 percentage-points (estimated
by multiplying the proportion of adults not attending
an initial appointment [57%] by the proportion of adults
attending an appointment following the delivery of the
24-month reminder with either the standard information
booklet [14.5%] or the theory-based leaflet [21.5%]), de-
pending on which of the two leaflets were adopted. Given
that uptake was consistent between men and women, as
well as between tertiles of area-level deprivation, it seems
unlikely that implementing these reminders with either
leaflet would exacerbate existing inequalities in uptake
[4]. Indeed, it is possible that implementing these remind-
ers could in fact reduce inequalities in uptake, given that
the proportion of nonparticipants living in the most
deprived quintile of areas is greater than the propor-
tion living in the least deprived quintile of areas (48%
vs. 68%) [4].
While uptake did not vary by gender or tertile of
area-level deprivation, it did vary by initial episode sta-
tus, with initial nonattenders being more likely to book
and attend an appointment than initial nonresponders
(20.3% vs. 11.4%). One possible explanation for this is
that initial nonattenders (who perceive fewer barriers
and more benefits to screening than initial nonrespond-
ers) are qualitatively similar to screened adults, but have
Table5 Self-referral and uptake by trial arm (12 and 24months combined)
n (%)
Unadjusted OR
(95% CI)
Adjusted OR
(95% CI)
Made an appointment comparisons
Control vs. Rem-SIB 3 vs. 83
(0.7 vs. 18.0)
33.52**
(10.51–106.92)
33.9**
(10.60–108.36)
Control vs. Rem-TBL 3 vs. 126
(0.7 vs. 27.3)
57.42**
(18.12–182.00)
65.25**
(20.48–207.90)
TMR-SIB vs. Rem-TBL 83 vs. 126
(18.0 vs. 27.3)
1.71**
(1.25–2.34)
1.93**
(1.39–2.66)
Attended an appointment comparisons
Control vs. Rem-SIB 3 vs. 67
(0.7 vs. 14.5)
25.96**
(8.10–83.18)
26.14**
(8.14–83.95)
Control vs. Rem-TBL 3 vs. 99
(0.7 vs. 21.5)
41.75**
(13.13–132.76)
46.91**
(14.68–149.93)
TMR-SIB vs. Rem-TBL 67 vs. 99
(14.5 vs. 21.5)
1.61*
(1.14–2.26)
1.80**
(1.26–2.55)
n=461 for all groups reported. Adjusted ORs and 95% CIs are adjusted for gender, area, deprivation, and initial episode status.
ORs odds ratios; CI condence interval; Rem-SIB Reminder and Standard Information Booklet; Rem-TBL Reminder and Theory-Based
Leaet.
*p≤.01; **p≤.001.
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difficulty translating their intentions into action due to
circumstantial aspects, such as poor health [25]. Indeed,
previous research by Ferrer and colleagues [26] has
shown that participation in colorectal cancer screening
is a behavioral process comprised of several qualitatively
distinct stages through which individual transition based
on their readiness to screen. Each stage is thought to be
strongly associated with a specific set of attitudes and
beliefs toward the test, and it may be that the interven-
tions used in our study were more effective at facilitat-
ing forward stage transitions in initial nonattenders by
addressing issues that were specific tothem.
Our study also found that, among individuals who
made an appointment, women were less likely to attend
screening than men (74.5% vs. 84.5%). This was con-
sistent with previous research in which women who
stated that they “probably would” or “definitely would”
attend screening were less likely to attend than their male
counterparts [25]. Given its position within the screening
pathway, it seems likely that these differences in uptake
between men and women are due to the enema, which
has previously been reported as a major barrier for
women, but not men [27].
In terms of the clinical findings, the adenoma detec-
tion rate (8.3%) was similar to that of initial attenders
(i.e., 9.8%) [7]. The rate was also consistent across re-
minder groups, irrespective of the information used,
suggesting that both materials were effective at attract-
ing individuals with colorectal pathology. With regards
to reminder intervals (i.e., 12 months vs. 24 months),
the study was underpowered to detect whether the total
number of adenomas detected increased. Further studies
with larger sample sizes are required to testthis.
Finally, few previous studies have been able to dem-
onstrate the added value of theory-based materials on
colorectal cancer screening rates [28], particularly with
regards to flexible sigmoidoscopy screening [8]. The find-
ing that the theory-based leaflet (albeit predominantly
with the first reminder) used in this study was effective is,
therefore, highly encouraging. Not only does it demon-
strate that such materials designed using theory can be
effective, but that they can be implemented in ways that
Table6 Self-referral and uptake by baseline characteristics (12 and 24months combined)
Made an
appointment
n (%)
Unadjusted OR
(95% CI)
Adjusted
OR
(95% CI)
Attended an
appointment
n (%)
Unadjusted OR
(95% CI)
Adjusted
OR
(95% CI)
Gender
Femalea (n=727) 109 (15.0) – – 82 (11.3) – –
Male
(n=656)
103 (15.7) 1.06 (0.79–1.42) 0.96 (0.71–1.32) 87 (13.3) 1.20 (0.87–1.66) 1.14 (0.81–1.60)
Area
Brenta
(n=926)
134 (14.5) – – 103 (11.1) – –
Harrow
(n=457)
78 (17.1) 1.22 (0.90–1.65) 1.26 (0.84–1.89) 66 (14.4) 1.35 (0.97–1.88) 1.44 (0.93–2.24)
Deprivation
Tertile 1a
(n=429)
70 (16.3) – – 58 (13.5) – –
Tertile 2
(n=505)
74 (14.7) 0.88 (0.62–1.26) 0.97 (0.63–1.49) 55 (10.9) 0.78 (0.53–1.16) 0.92 (0.58–1.48)
Tertile 3
(n=435)
67 (15.4) 0.93 (0.65–1.35) 1.09 (0.68–1.76) 56 (12.9) 0.95 (0.64–1.40) 1.22 (0.73–2.04)
Initial episode status
Initial
nonrespondera
(n=1,255)
181 (14.4) – – 143 (11.4) – –
Initial
nonattender
(n=128)
31 (24.2) 1.90* (1.23–2.93) 2.67** (1.63–4.37) 26 (20.3) 1.98* (1.25–3.15) 2.60** (1.55–4.36)
Adjusted ORs and 95% CIs are adjusted for trial arm and all other covariates in the table.
OR odds ratio; CI condence intervals; Rem-SIB Reminder and Standard Information Booklet; Rem-TBL Reminder and Theory-Based
Leaet.
aReference category.
*p≤.01; **p≤.001.
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do not contravene General Medical Council guidelines
for informed consent (e.g., by being sent after the full
suite of information has been received by the patient).
Furthermore, the findings from the present study pro-
vide evidence to support the use of the Behavior Change
Wheel as a framework for developing theory-based
interventions. Had we used another approach, the study
materials may have been similarly ineffective to those
described in the previous literature.
Strengths
This study had several strengths. First, it used a rand-
omized design, which is considered the gold standard
in terms of evaluating the effectiveness of public health
interventions [29]. Second, it is the first study to exam-
ine whether self-referral reminders can increase the
uptake of bowel scope screening and, as such, is the first
study to show that these are effective without being vul-
nerable to bias and confounding present in other stud-
ies. Finally, the study setting (St Mark’s Bowel Cancer
Screening Centre) serves an ethnically diverse popu-
lation from a range of socioeconomic areas and, as a
result, the findings are likely to be generalizable to other
London boroughs and international urban settings
struggling to reach the European target for acceptable
participation [30].
Limitations
As well as several strengths, this study had a number of
important limitations: the main one being that we only
examined the impact of the interventions at a single
center and another being that we only selected a pro-
portion of former nonparticipants for inclusion in the
trial—not the entire eligible population. An important
next step, therefore, would be to investigate the feasibility
of rolling out these reminders across the entire eligible
cohort of nonparticipants. On the basis that the first re-
minder was effective, the English National Health Service
have commissioned St Mark’s Hospital to carry out this
work at the London center. It is our hope that after the
publication of the current findings, the English National
Health Service will also commission St Mark’s Hospital
to implement and evaluate the use of a 24-month re-
minder aswell.
Another important caveat of our study is that, while
our leaflet was largely driven by theory-based insights,
some of its characteristics were based on anecdotal evi-
dence, or previous empirical observations. For example,
the theory-based leaflet was shorter and had a lower
readability score on the basis of previous research high-
lighting barriers to engaging with written information
about colorectal cancer screening by individuals with
both low and high literacy [31, 32]. Without additional
studies exploring the reasons why people self-referred for
screening (in both groups), it is not possible to say why
the theory-based leaflet was more effective. Future stud-
ies using questionnaires to examine which of the COM-B
components were affected by the study materials could
also help elucidate how the interventions facilitated
behavior change. Afactorial randomized controlled trial
comparing multiple versions of the theory-based leaflet
would ultimately be needed to disentangle which of the
behavior change techniques helped to facilitate behavior
change and thereby self-referral and uptake.
Finally, our study was limited to routine data stored
on the Bowel Cancer Screening System. As such, it was
not possible to include other potential predictors of
responding to the screening invite and attendance at
screening (e.g., previous bowel symptoms, andethnicity)
[25].
Conclusion
Sending former nonparticipants a self-referral reminder
12 and 24 months after their initial invitation was ef-
fective at improving uptake and was enhanced by the
inclusion of a theory-based leaflet developed using the
Behavior Change Wheel. Future studies should focus
on the feasibility of implementing these interventions
across multiple centers and the wider population of eli-
gible adults.
Supplementary Material
Supplementary material is available at Annals of
Behavioral Medicine online.
Acknowledgments We would like to acknowledge funding sup-
port from St Mark’s Hospital, University College London and
Cancer Research UK. RSK has a doctoral studentship funded by
St Mark’s Hospital and UCL; LMM is funded by a CRUK Project
Grant (C27064/A17326) Awarded to CVW. We would also like to
thank St Mark’s Hospital for supporting this project. We would
like to acknowledge the contributions of Lorraine Gorman and
Cherese Bennett, whose advice and support from initial conception
to completion were invaluable to this study.
Compliance with Ethical Standards
Authors’ Statement of Conflict of Interest and Adherence to Ethical
Standards All authors declare they have no conflicts of interest.
Primary Data The corresponding author had full access to all the
data in the study and had final responsibility for the decision to
submit for publication. The funding sources were not involved in
any part of the study, including the study design, data collection,
data analysis, writing of the report and the decision to submit the
paper for publication.
Authors’ Contribution RSK, LMM, JI, SM, and CvW conceived
the project and designed the interventions. RSK, SM, and AP man-
aged the trial. RSK and AP collected the data. RK, NC, and CvW
analysed the data. RK, LMM, NC, CR, and CvW interpreted the
data. All authors wrote the article.
10 ann. behav. med. (2018) XX:1–11
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Ethical Approval The study was approved by the North-East
Tyne & Wear South Research Ethnics Service (Ref: 15/NE/0043).
References
1. Ferlay J, Soerjomataram I, Dikshit R, et al. Cancer inci-
dence and mortality worldwide: sources, methods and
major patterns in GLOBOCAN 2012. Int J Cancer.
2015;136:359–386.
2. Elmunzer BJ, Hayward RA, Schoenfeld PS, Saini SD,
Deshpande A, Waljee AK. Effect of flexible sigmoidosco-
py-based screening on incidence and mortality of colorectal
cancer: a systematic review and meta-analysis of randomized
controlled trials. PLoS Med. 2012;9(12):e1001352.
3. Schreuders EH, Ruco A, Rabeneck L, etal. Colorectal can-
cer screening: a global overview of existing programmes. Gut.
2015;64(10):1637–1649.
4. McGregor LM, Bonello B, Kerrison RS, et al. Uptake of
Bowel Scope (Flexible Sigmoidoscopy) Screening in the
English National Programme: the first 14 months. j Med
Screen. 2016;23(2):77–82.
5. Klabunde C, Blom J, Bulliard JL, etal. Participation rates for
organized colorectal cancer screening programmes: an inter-
national comparison. j Med Screen. 2015;22(3):119–126.
6. Sabatino SA, White MC, Thompson TD, Klabunde CN;
Centers for Disease Control and Prevention (CDC). Cancer
screening test use – United States, 2013. mmwr Morb Mortal
Wkly Rep. 2015;64(17):464–468.
7. Bevan R, Rubin G, Sofianopoulou E, Patnick J, Rees CJ.
Implementing a national flexible sigmoidoscopy screen-
ing program: results of the English early pilot. Endoscopy.
2015;47(3):225–231.
8. Senore C, Inadomi J, Segnan N, Bellisario C, Hassan C.
Optimising colorectal cancer screening acceptance: a review.
Gut. 2015;64(7):1158–1177.
9. Senore C, Ederle A, DePretis G, etal. Invitation strategies
for colorectal cancer screening programmes: the impact of an
advance notification letter. Prev Med. 2015;73:106–111.
10. Hall N, Birt L, Rees CJ, et al. Concerns, perceived need
and competing priorities: a qualitative exploration of deci-
sion-making and non-participation in a population-based
flexible sigmoidoscopy screening programme to prevent colo-
rectal cancer. bmj Open. 2016;6(11):e012304.
11. Kerrison RS, McGregor LM, Marshall S, etal. Use of a
12months’ self-referral reminder to facilitate uptake of bowel
scope (flexible sigmoidoscopy) screening in previous non-re-
sponders: a London-based feasibility study. Br j Cancer.
2016;114(7):751–758.
12. Michie S, van Stralen MM, West R. The behaviour change
wheel: a new method for characterising and designing behav-
iour change interventions. Implement Sci. 2011;6(1):42.
13. Lo SH, Halloran S, Snowball J, etal. Colorectal cancer screen-
ing uptake over three biennial invitation rounds in the English
bowel cancer screening programme. Gut. 2014;64(62):1–10.
14. Steele RJ, Kostourou I, McClements P, et al. Effect of
repeated invitations on uptake of colorectal cancer screening
using faecal occult blood testing: analysis of prevalence and
incidence screening. BMJ. 2010;341:c5531.
15. Zajac IT, Whibley AH, Cole SR, et al. Endorsement by the
primary care practitioner consistently improves participation
in screening for colorectal cancer: a longitudinal analysis. j
Med Screen. 2010;17(1):19–24.
16. Kerrison RS, McGregor LM, Marshall S, et al. Improving
uptake of flexible sigmoidoscopy screening: a randomized
trial of nonparticipant reminders in the English Screening
Programme. Endoscopy. 2017;49(1):35–43.
17. Office for National Statistics. Ethnicity and National identity
in England and Wales: 2011. https://www.ons.gov.uk/people-
populationandcommunity/culturalidentity/ethnicity/articles/
ethnicityandnationalidentityinenglandandwales/2012-12-11.
Accessed May 17, 2017.
18. Halloran SP. Bowel cancer screening. Surgery. 2009;27(9):397–400.
19. Michie S, Richardson M, Johnston M, etal. The behavior
change technique taxonomy (v1) of 93 hierarchically clus-
tered techniques: building an international consensus for the
reporting of behavior change interventions. Ann Behav Med.
2013;46(1):81–95.
20. Partners in Creation. People Led Change for Better Decisions.
https://www.partnersincreation.uk. Accessed May 17, 2017.
21. Baron RC, Rimer BK, Breslow RA, et al.; Task Force on
Community Preventive Services. Client-directed interven-
tions to increase community demand for breast, cervical, and
colorectal cancer screening a systematic review. Am j Prev
Med. 2008;35(suppl 1):S34–S55.
22. Ramirez AJ, Forbes L. Approach to developing information
about NHS cancer screening programmes. King’s Health
Partners. 2012. http://www.informedchoiceaboutcancerscreen-
ing.org/wp-content/uploads/2012/04/Approach-to-informed-
choice-about-cancer-screening.pdf. Accessed January 4, 2018.
23. Department for Communities and Local Government.
English Indices of Deprivation 2010. https://www.gov.uk/
government/statistics/english-indices-of-deprivation-2010.
Accessed July 10, 2015.
24. Pearson K. On the criterion that a given system of devia-
tions from the probable in the case of a correlated system of
variables is such that it can be reasonably supposed to have
arisen from random sampling. Lond Edinb Dubl Phil Mag.
1900;50(302):157–175.
25. Power E, Van Jaarsveld CH, McCaffery K, Miles A, Atkin W,
Wardle J. Understanding intentions and action in colorectal
cancer screening. Ann Behav Med. 2008;35(3):285–294.
26. Ferrer RA, Hall KL, Portnoy DB, Ling BS, Han PK, Klein
WM. Relationships among health perceptions vary depend-
ing on stage of readiness for colorectal cancer screening.
Health Psychol. 2011;30(5):525–535.
27. Friedemann‐Sánchez G, Griffin JM, Partin MR: Gender dif-
ferences in colorectal cancer screening barriers and informa-
tion needs. Health Expect. 2007;10(2):148–160.
28. Duffy SW, Myles JP, Maroni R, Mohammad A. Rapid review
of evaluation of interventions to improve participation in
cancer screening services. j Med Screen. 2017;24(3):127–145.
29. Sackett DL. Evidence-based medicine. BMJ. 1996;312:71–72.
30. von Karsa L, Patnick J, Segnan N, etal. European guidelines
for quality assurance in colorectal cancer screening and diag-
nosis: overview and introduction to the full supplement pub-
lication. Endoscopy. 2013;45(1):51–59.
31. Peters E, Klein W, Kaufman A, Meilleur L, Dixon A. More
is not always better: intuitions about effective public policy
can lead to unintended consequences. Soc Issues Policy Rev.
2013;7(1):114–148.
32. Smith SK, Trevena L, Nutbeam D, Barratt A, McCaffery
KJ. Information needs and preferences of low and high
literacy consumers for decisions about colorectal can-
cer screening: utilizing a linguistic model. Health Expect.
2008;11(2):123–136.
ann. behav. med. (2018) XX:1–11 11
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