Mhealth Interventions To Improve Cancer Screening and Early Detection: Scoping Review of Reviews

JOURNAL OF MEDICAL INTERNET RESEARCH Schliemann et al
Review
mHealth Interventions to Improve Cancer Screening and Early

Detection: Scoping Review of Reviews
Désirée Schliemann1, PhD; Min Min Tan2,3, PhD; Wilfred Mok Kok Hoe2,3, PhD; Devi Mohan3, MD; Nur Aishah
Taib4, PhD; Michael Donnelly1, PhD; Tin Tin Su1,2,3, PhD
1
Centre for Public Health, Queen’s University Belfast, Belfast, United Kingdom
2
South East Asia Community Observatory (SEACO), Monash University Malaysia, Subang Jaya, Malaysia
3
Global Public Health, Jeffrey Cheah School of Medicine and Health Sciences, Monash University Malaysia, Subang Jaya, Malaysia
4
Department of Surgery, Faculty of Medicine, University Malaya Cancer Research Institute, University of Malaya, Kuala Lumpur, Malaysia
Corresponding Author:
Désirée Schliemann, PhD
Centre for Public Health
Queen’s University Belfast
Institute of Clinical Science, Block B
Royal Victoria Hospital
Belfast, BT12 6BA
United Kingdom
Phone: 44 02890245133
Email: [email protected]
Abstract
Background: Cancer screening provision in resource-constrained settings tends to be opportunistic, and uptake tends to be low,
leading to delayed presentation and treatment and poor survival.
Objective: The aim of this study was to identify, review, map, and summarize findings from different types of literature reviews
on the use of mobile health (mHealth) technologies to improve the uptake of cancer screening.
Methods: The review methodology was guided by the PRISMA-ScR (Preferred Reporting Items for Systematic Reviews and
Meta-Analyses extension for Scoping Reviews). Ovid MEDLINE, PyscINFO, and Embase were searched from inception to May
2021. The eligible criteria included reviews that focused on studies of interventions that used mobile phone devices to promote
and deliver cancer screening and described the effectiveness or implementation of mHealth intervention outcomes. Key data
fields such as study aims, types of cancer, mHealth formats, and outcomes were extracted, and the data were analyzed to address
the objective of the review.
Results: Our initial search identified 1981 titles, of which 12 (0.61%) reviews met the inclusion criteria (systematic reviews:
n=6, 50%; scoping reviews: n=4, 33%; rapid reviews: n=1, 8%; narrative reviews: n=1, 8%). Most (57/67, 85%) of the interventions
targeted breast and cervical cancer awareness and screening uptake. The most commonly used mHealth technologies for increasing
cancer screening uptake were SMS text messages and telephone calls. Overall, mHealth interventions increased knowledge about
screening and had high acceptance among participants. The likelihood of achieving improved uptake-related outcomes increased
when interventions used >1 mode of communication (telephone reminders, physical invitation letters, and educational pamphlets)
together with mHealth.
Conclusions: mHealth interventions increase cancer screening uptake, although multiple modes used in combination seem to
be more effective.
(J Med Internet Res 2022;24(8):e36316) doi: 10.2196/36316
KEYWORDS
mobile health; mHealth; cancer screening; scoping review of reviews; cancer; cancer detection; oncology; digital health; scoping
review; review; mobile phone
https://www.jmir.org/2022/8/e36316 J Med Internet Res 2022 | vol. 24 | iss. 8 | e36316 | p. 1

(page number not for citation purposes)
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different types of reviews. However, it is unknown whether

Introduction similar findings are observed across the reviews.
Background Objectives
Globally, cancer is the second leading cause of death; it This scoping review aimed to map and summarize findings from
accounted for approximately 9.6 million deaths in 2018 [1]. systematic, scoping, narrative, and rapid reviews on the use of
Cancer incidence and mortality are predicted to increase to 30.2 mHealth in cancer screening, as well as other screening-related
million cases and 16.3 million deaths by 2040, respectively, outcomes such as attitudes toward screening and knowledge
because of aging populations and the adoption of unhealthy and awareness of screening. We also included implementation
lifestyles [2]. Delay between symptom onset and treatment leads considerations for successful mHealth interventions in
to poorer cancer survival [3]. Screening increases the chance improving cancer screening uptake and screening-related
of early detection and treatment and, ultimately, survival. In outcomes.
many high-income countries, population-based cancer screening
is available for four common cancers and has contributed to Methods
reduced breast cancer [4], cervical cancer [5], prostate cancer
[6], and colorectal cancer [7] mortality. However, cancer Overview
screening in the majority of low- and middle-income countries This scoping review of reviews was conducted based on the
(LMICs) is opportunistic, and uptake is low compared with framework of Arksey and O’Malley [23] and using the
cancer screening in high-income countries, leading to delayed PRISMA-ScR (Preferred Reporting Items for Systematic
presentation, treatment, and survival [8]; for example, the uptake Reviews and Meta-Analyses extension for Scoping Reviews)
of mammogram screening was 12% to 31% in Brazil [9] and guidelines [24]. The protocol of this review has not been
7% to 25% in Malaysia [10] compared with 66% in Germany preregistered. As the use of mHealth in relation to cancer
[11] and 75% in Spain [12]. Low uptake of cancer screening screening is a relatively nascent field of study, a scoping review
might indicate poor awareness and knowledge of cancer and is useful in mapping the published literature comprehensively
cancer screening among the public; for example, Asian Pacific and systematically. The review was guided by the following
populations with the lowest uptake of colorectal cancer 5-step framework: (1) identifying the research question; (2)
screening, such as India, Malaysia, Indonesia, Pakistan, and identifying relevant studies; (3) study selection; (4) charting the
Brunei, had correspondingly low levels of awareness and data; and (5) collating, summarizing, and reporting the results.
knowledge of colorectal cancer symptoms, risk factors, and
screening tests [13]. Poor knowledge about, and negative Search Strategy
perceptions toward, mammogram screening are major barriers We first searched Ovid MEDLINE, PyscINFO, and Embase for
to mammogram screening uptake in Malaysia [10]. relevant literature on February 1, 2021, using two categories of
Digital health care, that is, the use of digital technologies for key terms: mHealth and early detection of cancer. We then
health, is now commonly used in public health care as well as refined the search on May 17, 2021. The key terms were based
primary health care [14]. According to the World Health on Medical Subject Headings indexing as well as free-text terms.
Organization Global Observatory for eHealth, mobile health We combined key terms from the same category with OR and
(mHealth) is defined as “medical and public health practice between categories with AND. The search strategy was
supported by the use of mobile devices” such as mobile phones, developed in Ovid MEDLINE (Multimedia Appendix 1) and
smartphones, and tablet computers [15]. Worldwide, there are adapted for the other databases. We also hand searched the
approximately 5.3 billion unique mobile phone users, reference lists of selected reviews for relevant reviews. All
representing 67.1% of the total population, and smartphones searches were exported into EndNote (Clarivate), and duplicates
account for approximately 75% of the mobile phones in use were removed.
[16]. The high penetration rate of mobile phones allows timely Inclusion Criteria
data collection as well as transmission and analysis of the data.
Papers were included if they satisfied all of the following
Thus, mHealth holds great potential for improving health
criteria: (1) a review of any type, (2) the reviewed interventions
outcomes because of its mobility, instantaneous access, and
related to cancer screening (for any cancer type) that were
ease of use. Some of the common mHealth apps offer patient
conducted on mobile devices such as mobile phones and tablet
education and behavior change communication, data collection
computers, (3) described the effectiveness and implementation
and reporting, population health registries and vital event
of mHealth interventions on outcomes related to cancer
tracking, and electronic health records, as well as provider
screening, (4) included adults aged ≥18 years from the general
training and education [17]. mHealth interventions have a
population, and (5) published in English in peer-reviewed
positive impact on clinical outcomes, adherence to treatment
journals from inception up to May 2021. We excluded reviews
and care, health behavior changes, disease management, and
that did not specify the use of mobile technologies but instead
primary care attendance rates with regard to various diseases
reported modes of delivery such as web-based and
[18]. mHealth has also been used in cancer self-care and
computer-delivered programs and videos.
self-management among cancer survivors to improve sleep and
quality of life; reduce fatigue, stress, and pain; and promote
health behaviors such as weight loss [19-22]. The role of
mHealth in promoting cancer screening has been explored in

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Selection of Reviews WMKH independently for inclusion, with discrepancies resolved

We selected the relevant reviews using a 3-stage process: (1) through discussion with DS, MMT, and WMKH; and (3) MMT
MMT and WMKH conducted the initial screening of titles and and WMKH extracted relevant data. The screening process is
abstracts to determine eligibility for inclusion; (2) WMKH provided in the PRISMA (Preferred Reporting Items for
retrieved full texts, which were screened by DS, MMT, and Systematic Reviews and Meta-Analyses) flowchart (Figure 1).
Figure 1. PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses) flowchart.
selected reviews. For reviews that included studies that focused

Data Extraction and Charting on mHealth and studies that did not, we only extracted
The following data were extracted by MMT and WMKH from information specifically reported on the studies that included
each selected review into an Excel (Microsoft Corporation) mHealth. Information related to the quality of the reviews was
spreadsheet: not assessed.
• Review identifiers (author, year, country, type of review,
number of studies, time range, intervention duration, and Results
follow-up duration)
•
Literature Search
Study aim
• Types of cancer mentioned in the relevant studies in the Our initial search identified 2083 citations, resulting in 1981
review (95.1%) unique citations after removal of duplicates (Figure 1).
• Types of mHealth mentioned in the relevant studies in the The titles and abstracts were assessed based on the inclusion
review criteria, and of the 1981 unique citations, 24 (1.21%) were
• Details of intervention procedures included for full-text screening. Of these 24 reviews, 12 (50%)
• Outcome measures (awareness, knowledge, or attitude; were excluded after the full-text screen: 5 (42%) did not include
screening uptake; and implementation-related outcomes) cancer screening-related outcomes, 6 (50%) did not include
• Key stakeholders in delivering the mHealth intervention, mHealth components, and 1 (8%) included children as their
if any target population. Hence, of the 24 reviews included for full-text
screening, 12 (50%) were included in this scoping review. Table
If the aforementioned data were not reported in the selected 1 summarizes the characteristics of the included reviews.
reviews, we referred to the individual studies included in the

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Table 1. Characteristics of included reviews.

Study Type of Aim Time frame Total number of Type of mHealthb in relevant Key stakeholders delivering
review of search studies; number of mHealth interventions
studiesa
strategy relevant studiesa by
cancer type
Bhochhib- Scoping To identify studies January 1, 12; cervical cancer • Telephone appointment • Telephone appointment
hoya et al review that examined 2009, to (n=12, 3 of which (n=1) by midwife (n=1)
[25], 2020 mHealth programs September, were qualitative • Telephone reminder with • Telephone counseling
that focused on in- 28, 2019 studies) tailored counseling ver- and reminders by re-
creasing cervical sus telephone reminder search staff (n=1)
cancer screening with print materials • Invitation telephone call
among women to (n=1) by clinical secretaries
determine if these • SMS text message re- (n=1)
interventions im- minders (n=3) • Telephone caller unspec-
proved adherence to • 15 behavior change ified (n=1)
screening and what messages with transporta-
factors (barriers and tion e-voucher versus
facilitators) were SMS text messages of
most influential location and hours of the
among participants closest screening clinic
(n=1)
• Automated SMS text
messages or telephone
call reminders (n=1)
• Automated SMS text
messages versus tele-
phone call re-
minders+manual tele-
phone call+face-to-face
interview (n=1)
• 3 sequential SMS text
message reminders, fol-
lowed by 3 telephone
call attempts (n=1)
Uy et al Systemat- To assess the effect January 9; breast (n=5), cervi- • SMS text message re- • None
[26], 2017 ic review of SMS text messag- 2000 to Jan- cal (n=1), and col- minder (n=5)
ing interventions on uary 2017 orectal (n=3) cancers • SMS text message re-
increasing patient minder plus letter (n=4)
adherence to screen-
ing for breast, cervi-
cal, colorectal, and
lung cancers
Zhang et al Systemat- To qualitatively syn- Up to Octo- 8 (1 cross-sectional • Invitation letter with • Motivational interview
[27], 2020 ic review thesize published ar- ber 10, 2019 study); cervical can- pamphlet, followed by through telephone call
ticles reporting the cer (n=7) telephone reminder by nurses (n=1)
impact of mHealth (n=1) • Telephone caller unspec-
on cervical cancer • Educational SMS text ified (n=1)
screening–related messages (n=2)
health behaviors • Educational SMS text
message versus SMS
text message reminder
(n=1)
• Educational SMS text
messages with transporta-
tion e-voucher versus
SMS text messages of
location and hours of the
closest screening clinic
(n=1)
• Motivational interview
over the telephone (n=1)
• Training through SMS
text message, electronic
posters, infographics,
podcasts, and video tuto-
rial (n=1)

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studiesa
cancer type
Halake and Scoping To establish the ex- 1990 to 2014 15; breast cancer • SMS text message invita- • Not described
Ogoncho review tent and nature of (n=2) tion and cancer screen-
[28], 2017 the published and ing information (n=1)
gray literature on the • Smartphone app to facil-
use of mHealth- itate BSEd (n=1)
based technologies
for cancer preven-
tion, detection, and
management in
LMICsc
Choi et al Systemat- To investigate recent January 1, 18; skin cancer • Educational SMS text • Not described
[29], 2018 ic review research trends relat- 2007, to De- (n=1) message about skin self-
ed to the use of mo- cember 31, examination (n=1)
bile technology in 2017
the prevention and
management of skin
cancer, focusing on
how such technolo-
gy is evaluated and
what impact it has in
each phase across
the cancer continu-
um
Houghton et Systemat- To determine how Up to Febru- 69; breast cancer • Mammopad, a decision • Mobile apps paired with
al [30], 2019 ic review mobile apps are be- ary 7, 2019 (n=4) aid mobile app on iPad community health navi-
ing used for breast Mini (n=1) gators (n=2)
cancer prevention • Mobile app to assist
among women navigator (n=1)
across the cancer • mMammogram mobile
control continuum app for SMS text mes-
sage (n=1)
• Mobile app for BSE
(n=1)
Plackett et al Scoping To map the evidence 2004 to June 23; breast (n=4) and • Facebook (n=3) • Not described
[31], 2020 review for social media in- 2019 cervical (n=1) can- • Snapchat (n=1)
terventions to im- cers
prove cancer screen-
ing and early diagno-
sis, including behav-
ior change, and how
the interventions fa-
cilitate behavior
change
Musa et al Systemat- To review the evi- Up to Au- 28; cervical cancer • Telephone counseling • Telephone caller unspec-
[32], 2017 ic review dence of the effec- gust 2016 (n=5) (n=1) ified (n=3)
and meta- tiveness of provider • SMS text message or • Telephone counseling by
analysis recommendations telephone reminder health educator (n=1)
for cervical cancer (n=1) • Telemarketing company
screening on screen- • Email, telephone, or (n=1)
ing rates in women multimodal (let-
at risk for cervical ter+email+telephone)
cancer screening reminder and
invitation and education
flyer (n=1)
• Telephone reminder
(n=1)
• Invitation letter and infor-
mation pamphlet, fol-
lowed by telephone re-
minder with counseling
(n=1)

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studiesa
cancer type
Duffy et al Rapid re- To review the cur- Time frame 68; breast (n=9), • Automated telephone • Colorectal cancer
[33], 2017 view rent evidence on ef- not specified cervical (n=5), col- and SMS text message screening navigator
fects of interventions orectal (n=2), and reminders or telephone (n=1)
to improve cancer stomach (n=1) can- outreach (n=1) • Bilingual advocate at a
screening participa- cers • Telephone reminder or community organization
tion, focusing in par- motivational telephone with experience in tele-
ticular on effects in call (n=1) phone outreach (n=1)
underserved popula- • Telephone call to con- • Local women recruited
tions firm receipt of invitation by Community Links, a
letter, followed by tele- community charity (n=1)
phone reminder (n=1) • Female scheduler and
• Telephone reminders female counselors (n=1)
(n=8) • Female research assis-
• SMS text message re- tants (n=1)
minder (n=3) • Telephone counselors
• Tailored telephone (n=2)
counseling (n=2) • Trained GPe receptionist
• Telephone appointment (n=1)
(n=1) • Volunteers (n=1)
• Researcher (n=1)
• Research nurse (n=1)
• Telemarketing company
(n=1)
• Telephone caller unspec-
ified (n=2)
Lott et al Scoping To map the literature Up to 2019 19; cervical cancer • SMS text message re- • Telephone counselors
[34], 2020 review on interventions to (n=3) minders (n=1) (n=1)
increase uptake of • Telephone follow-up and
cervical screening in counseling (n=1)
sub-Saharan Africa • Email (n=1)
and identify opportu-
nities for future inter-
vention development
and research
Déglise et al Narrative To describe the Up to May 17; breast cancer • SMS text message re- • Not described
[35], 2012 review characteristics and 2011 (n=1) minder
outcomes of SMS
text messaging inter-
ventions for disease
prevention in LMICs
and provide recom-
mendations for fu-
ture work
Peiris et al Systemat- To critically ap- Up to May 48; breast cancer • SMS text message re- • Not described
[36], 2014 ic review praise the role of 2014 (n=1) minder
mHealth in improv-
ing health care quali-
ty for NCDsf in
LMICs
a
Relevant studies are studies that met the inclusion criteria for this review; for example, some reviews included diseases other than cancer. We only
reported results from the studies evaluating cancer-related interventions.
b
mHealth: mobile health.
c
LMICs: low- and middle-income countries.
d
BSE: breast self-examination.
e
GP: general practitioner.
f
NCD: noncommunicable disease.

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Characteristics of Reviews included studies that were conducted mainly in high-income

The included reviews (n=12) were published between 2012 and Western countries [25,26,29-33], whereas 42% (5/12) focused
2020 (Table 1). Of the 12 reviews, 6 (50%) were systematic on LMICs [27,28,34-36], of which 20% (1/5) focused solely
reviews [26,27,29,30,32,36], of which 1 (17%) also included a on sub-Saharan Africa [34]. In total, 33% (4/12) of the reviews
meta-analysis [32]; 4 (33%) were scoping reviews [25,28,31,34]; focused on cervical cancer [25,27,32,34]; 8% (1/12) focused
1 (8%) was a rapid review [33]; and 1 (8%) was a narrative on skin cancer [29]; 8% (1/12) focused on breast cancer [30];
review [35]. The 12 reviews reported different outcomes of the 8% (1/12) examined breast, cervical, lung, and colorectal cancers
studies that were relevant to this review of reviews (Table 2): [26]; 25% (3/12) included any type of cancer [28,31,33]; and 2
5 (42%) reported solely the effectiveness of mHealth reviews focused on disease prevention in general [35,36]. In
interventions on cancer screening [26,29,32-34]; 4 (33%) terms of interventions, 42% (5/12) of the reviews included
reported outcomes in relation to cancer screening, change in interventions of various types of mHealth technologies
cancer knowledge, and attitudes to screening [25,27,30,31]; 2 [25,27-29,36], 2 (33%) focused solely on SMS text messages
(17%) reported outcomes in relation to breast self-examination [26,35], 1 (17%) focused on social media interventions [31], 1
(BSE) practice [35,36]; and 1 reported outcomes in relation to (17%) was specifically about mobile apps [30], and 25% (3/12)
BSE and cancer screening [28]. Most (7/12, 58%) of the reviews included any type of communication (mHealth, face-to-face,
and other media) [32-34].

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Table 2. Summary of screening-related outcomes extracted from each review.

Study Outcomes
Screening outcomes Screening awareness-, knowledge-, Implementation-related outcomes and
and attitude-related outcomes measures
Bhochhibhoya et al • Screening uptake: n=5/6a (9.1%-17.9% • Knowledge improvement: n=2/2 • Advantages: convenient, time effec-
[25], 2020 increase between intervention group • Attitude about screening: n=1/2 tive, ease of use, and able to receive
versus control group; 9.3% increase after • Perceived behavior control: notification
the intervention compared with before)b n=0/1 • Concerns: confidentiality of SMS
• Screening follow-up adherence: n=0/1 • Perceived barriers about screen- text messages, loss of the mobile
• Effective methods: stepwise approach ing: n=0/1 phones, clarity of the language
(automated telephone calls and SMS text • Belief about screening: n=1/1 used, and receiving negative results
messages, followed by manual telephone • Screening intention: n=0/2 through SMS text message
call and face-to-face interview), SMS • Effective methods: health-specif- • Barriers: inconvenient for older
text messages only, telephone call only, ic and spiritually based SMS text participants, lack of texting profi-
telephone appointment by midwives, messages and personally tailored ciency, difficulty in texting, and
telephone reminders combined with texts with statistical facts apprehension that SMS text mes-
other methods such as tailored counsel- sages might not be clearly under-
ing, and SMS text message with trans- stood
portation e-voucher • Enabling factors: contact prefer-
ences, cell phone ownership, and
portability of same number
• Enhancing factors: message content
(reminder and informative) and
short and simple messaging formats
Uy et al [26], 2017 • Screening uptake: n=5/9 (1.2%-9.9% —c —

absolute increase)
• Effective methods: SMS text message
reminder+letter and single SMS text
message reminder
Zhang et al [27], • Screening uptake: n=3/5 (12.9%-50.9% • Knowledge improvement: n=1/2 • Interest in receiving screening test
2020 increase) • Perceived benefits of Pape test: results through SMS text message:
• Screening follow-up: n=1/1 (91.8%- n=1/1 n=0/1
93.5%; ORd 1.37-1.40) • Reduced barriers to undergoing • Interest in receiving screening test
• Effective methods: SMS text message Pap smear: n=1/1 results using nonprivate telephone:
with transportation e-voucher, invitation • Attitude about screening: n=0/1 n=1/1 (OR 0.31, 95% CI 0.18-0.51)
letter with telephone reminder, re- • Effective methods: a combina- • Interest in receiving appointment
minders sent through letter, registered tion of SMS text message, elec- reminders through SMS text mes-
letter, SMS text message or telephone tronic posters, infographics, sage: n=1/1 (OR 14.19, 95% CI
call, and telephone reminders or educa- podcasts, and video tutorials 1.72-117.13)
tional telephone call • Interest in receiving appointment
reminders using nonprivate tele-
phone: n=0/1
Halake and Ogoncho • Screening uptake: n=1/1 (30.7% and — —

[28], 2017 31.6% increase)
• BSEf practice: n=1/1
• Effective method: BSE smartphone app
Choi et al [29], 2018 • Screening uptake: n=1/1 (27% absolute — —

increase in skin self-examination)
• Effective method: educational SMS text
messages with reminders

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Study Outcomes
Houghton et al [30], • Screening uptake: n=3/3 • Knowledge improvement: n=2/2 • Intervention satisfaction (mMammo-
2019 • Effective methods: community health (33% increase) gram): n=1/1
workers (trained or untrained in patient • Reduced decisional conflict: • Effectiveness satisfaction (mMam-
navigation) equipped with smartphone n=1/1 mogram): n=1/1
app plus standard risk counselling and • Self-efficacy: n=1/1
mMammogram (SMS text messages • Screening intention: n=0/1
plus health navigator) • Screening readiness: n=1/1
• Effective methods: smartphone
app plus standard risk counsel-
ing, mMammogram (SMS text
messages plus health navigator),
and smartphone app decision aid
(Mammopad)
Plackett et al [31], • Screening uptake: n=1/1 (12.9% in- • Knowledge improvement: n=2/2 • Using Facebook is acceptable for
2020 crease) • Screening intention: n=1/1 (82% delivering breast cancer screening
• Effective method: breast cancer screen- increase) information: n=1/1
ing service Facebook page • Effective methods: Facebook or
face-to-face discussions for 2
weeks after 50-minute classroom
cervical cancer prevention edu-
cation lecture (female high
school students), receiving
breast cancer awareness informa-
tion through Snapchat, and tai-
lored SMS text message mam-
mography campaign on Face-
book during Breast Cancer
Awareness Month
Musa et al [32], • Screening uptake: n=5/6 (7.8%-31.1% — —

2017 absolute increase)
• Reduced screening median time: n=1/1
• Effective methods: direct invitation
mail+brochure+telephone counseling
by health educators; telephone reminder
with educational information and multi-
modal intervention; invitation letter and
information pamphlet, followed by
telephone reminder with counseling;
telephone reminder with educational in-
formation; and multimodal intervention
Duffy et al [33], • Screening uptake: n=13/16 (5%-45% — —

2017 absolute increase)
• n=3/3, SMS text reminder studies;
n=11/13, telephone reminder studies
Lott et al [34], 2020 • Screening uptake: n=2/3 (8.6% differ- — —

ence in screening uptake between con-
trol and intervention groups; 51% in-
crease after the intervention)
• Effective methods: SMS text message
about cervical cancer and context-specif-
ic barriers to screening (and SMS text
message plus e-voucher for transporta-
tion) and enhanced patient-centered
counseling with patient follow-up by
telephone (with or without escort to
cervical cancer screening)
Déglise et al [35], • BSE practice: n=1/1 — —

2012 • Effective method: SMS text message
reminder to conduct BSE

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Study Outcomes
Peiris et al [36], • BSE practice: n=1/1 — —
2014 • Effective method: SMS text message
reminder to conduct BSE
a
Number of studies that reported a positive outcome out of the total number of studies that included the particular outcome.
b
Percentage of change or odds ratios are included if available.
c
Not available (ie, not reported).
d
OR: odds ratio.
e
Pap: Papanicolaou.
f
BSE: breast self-examination.
with an abnormal clinical breast examination (CBE). A

Types of mHealth Interventions BSE-facilitating smartphone app included BSE date reminders
SMS text messages were the most commonly used mHealth and a reminder to encourage mother and daughter to practice
technology and were used in 46% (31/67) of the interventions. BSE together [39].
They were mainly delivered as reminders of cancer screening
appointments, alone or in combination with telephone reminders, Other mHealth platforms that were less frequently used were
physical invitation letters, and educational pamphlets. emails and social media. Emails were used to deliver screening
Educational SMS text messages, sent as a one-off or in a series invitations, reminders, web-based educational flyers, and cancer-
over days or weeks, were also widely used. Their contents and health-related information. Social media platforms such as
included information about cancer risk factors, benefits of Facebook and Snapchat were used as intervention modes to
screening, location and operating hours of screening clinics, provide information about breast and cervical cancers and
spiritually based health messages, and facts about cancer (eg, screening, promote mammogram screening, and schedule breast
incidence, mortality, and screening rates). Educational SMS screening appointments, as well as a platform for discussions
text messages were used alone or in combination with an about cervical cancer after a lecture [31].
e-voucher (to subsidize the cost of transportation to and from Almost all (11/12, 92%) reviews described mHealth
the screening facility) [37]. interventions that included 1 or 2 mHealth technologies. There
Text messages were most commonly sent as SMS text messages. was only 1 intervention that used a combination of >2 types of
In later studies, they were also sent through IP-based messaging mHealth technologies: a training in cervical cancer through
services such as Telegram and Snapchat and mobile apps SMS text message, electronic posters, infographics, podcasts,
specifically designed for the interventions. In almost all (10/12, and video tutorials [40].
83%) reviews, the delivery of SMS text messages was one-way, Key Stakeholders in mHealth Interventions
8% (1/12) of the reviews reported an intervention that included
Of the 12 reviews, 5 (42%) included telephone call interventions
a specifically designed mobile app (mMammogram) that
that were delivered by a broad range of personnel [25,27,32-34].
featured personally tailored messages [38], and 8% (1/12) used
Telephone reminders or telephone calls to make or confirm
social media for communication [31].
screening appointments were delivered by bilingual advocates
Telephone calls were used in 40% (27/67) of the interventions from a community organization, local women recruited from a
mostly as cancer screening invitations and reminders and to community charity, research assistants, general practitioner
arrange screening appointments. Telephone reminders, receptionist, volunteers, research nurses, midwives at antenatal
automated or live, were used alone or with SMS text message health clinics, clinical secretaries, and telemarketers.
reminders, screening invitation letters, and pamphlets.
Among the important personnel in mHealth interventions were
Participants were contacted through telephone to confirm the
telephone counselors who called the participants to inquire about
receipt of a screening invitation letter. Motivational interviews
their screening intention and ascertain whether they had received
were conducted over the telephone to increase participants’
the invitation letters, provided information about screening,
readiness to attend screening [27]. Knowledge about cancer was
addressed current or potential barriers to screening uptake
provided and barriers to screening addressed through telephone
through motivational interviews and applied a counseling
counseling [25,33,34].
approach to increase motivation for behavior change, or assisted
A few breast cancer mobile apps were specifically designed for with appointment scheduling. Telephone counseling was
interventions. Mammopad, for example, is a decision aid, a tool delivered by nurses or hospital-based health counselors.
that helps women to decide to participate in mammogram
Health navigator services were mentioned in 8% (1/12) of the
screening, that ran on the iPad Mini [30]. Another app was
reviews [30]. Health navigators used mobile apps to facilitate
designed to assist community health workers (CHWs) in
interviews, report data, show motivational videos, and offer
interviewing participants, reporting data, showing a motivational
screening appointments. Health navigators or CHWs guided
video, and offering a mammogram appointment for women

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participants in navigating cancer screening information, provided such as showing a motivational video and offering an
transportation and interpretation services, addressed technical appointment, detected 3 times more women with abnormal
problems related to mobile app use, and reminded participants CBEs than CHWs without smartphone support (3.1% without
to complete cancer screening. navigation training and 3.2% with navigation training vs 1%
without smartphone) [30,43]. CHWs who used mobile apps and
Cancer Screening Uptake were trained in navigation had the highest percentage of
All (12/12, 100%) reviews included in this review reported participants with an abnormal CBE who attended further clinical
mainly improved cancer screening uptake or self-examination assessment compared with those who used mobile apps only or
practice (for breast or skin cancer; Table 2). The increase in without smartphone support. In a study in the United States,
screening between the intervention and control groups (from participants who failed to complete a fecal occult blood test
relevant studies) ranged from 1.2% to 50.9%. were much more likely to complete a second fecal occult blood
Overall, the reviews concluded that interventions that included test than those in usual care if they had been contacted through
>1 communication mode seemed more effective than those that telephone call by colorectal screening navigators (82.2% vs
included a single telephone call or SMS text message reminder. 37.3% among those who received standard care; P<.001)
A 3-step sequential approach (an automated reminder telephone [33,44].
call and SMS text message, followed by manual telephone calls There were a number (46/67, 69%) of studies that used only 1
and face-to-face interviews) conducted at Portuguese primary mode of mHealth communication, and the findings related to
health care units resulted in 51% of the women in the screening uptake after the intervention compared with before
intervention group attending cervical cancer screening compared the intervention were mixed; for example, in an email
with 34% of the women in the control group who received only intervention study, whether an email message was loss-framed
written invitation letters [25,41]. In another study, women in (focused on risk), gain-framed (focused on health and well-being
northern Tanzania who received transportation e-vouchers to improvement), or neutrally framed (provided only facts) had
cover return transportation to the nearest screening facility as no effect on cervical cancer screening uptake [34,45]. An
well as a series of 15 behavior change messages delivered exception was a study conducted in western Sweden where there
through SMS text message were more likely to attend cervical was telephone contact through midwives to offer an appointment
cancer screening (uptake: 18%; OR 4.7, 95% CI 2.9-7.4) for a Pap test, which increased the uptake of Pap tests compared
compared with those who received only the same SMS text with the usual annual invitations without telephone contact
message (uptake: 12.9%; OR 3.0, 95% CI 1.5-6.2) and those (uptake at 3-month follow-up: 13% vs 3.9%; risk ratio 3.37,
who received 3 SMS text messages with the location and hours 95% CI 2.83-4.01) [25,46]. Another exception was the use of
of the nearest screening clinic (uptake: 4.3%) [27,34,37]. Facebook to share breast cancer information and schedule breast
Participants from Iran who received a Health Belief screening appointments, which increased breast cancer screening
Model–based training in cervical cancer through SMS text attendance by an average of 12.9% [31,47].
messages, electronic posters, infographics, podcasts, and a video
tutorial were more likely to complete a Papanicolaou (Pap) test A brief invitation SMS text message was as effective as a
(47.9%) than the participants in the control group (5.8%) detailed informative SMS text message: there was no significant
[27,40]. difference in screening uptake between Lebanese women who
received an SMS text message mammogram invitation and those
A once-a-month SMS text message reminder over 6 months who received the same SMS text message and an additional
combined with a BSE training through a lecture, video, and informative SMS text message about the benefits of
demonstration of the technique on a breast model led to a 32% mammogram screening [28,48].
increase in BSE practice [35,36,42]. An Android operating
system–based smartphone app that included a BSE date alarm, Screening Awareness, Knowledge, Intention, and
a reminder to encourage mother and daughter to practice BSE Attitude
together, a mother motivation function that allows the user to Of the 12 reviews, 4 (33%) [25,27,30,31] included studies
call her mother using a notification function to practice BSE specifically on knowledge, awareness, intention, or attitude in
together, and educational videos increased the percentage of relation to cervical cancer screening (2/4, 50%), breast cancer
Korean women practicing BSE from 62.2% to 71.1% [39]. screening (1/4, 25%), or both (1/4, 25%), and almost all of the
Of the 12 reviews, 1 (8%) included interventions that individual interventions (7/8, 88%) reported improvements in
incorporated navigation to health services [30], which was found knowledge, whereas few studies reported an improvement in
to be effective in increasing screening uptake. All (3/3, 100%) screening intention (1/4, 25%; Table 2). Interventions that were
of the interventions that included health navigation services successful in increasing screening uptake were also successful
were effective in increasing screening uptake. Korean American in increasing knowledge and awareness about screening for
immigrant women who received a series of 8 to 21 SMS text both cervical and breast cancer.
messages about breast cancer through a specially designed The CervixCheck intervention was designed for African
mobile app (mMammogram) and were provided with health American women and consisted of a series of 22 health-specific,
navigation services had a significantly higher percentage of spiritually based, cervical cancer–related SMS text messages
completed mammograms after 6 months than women who (eg, on the importance of keeping the body healthy and attending
received printed brochures only (75% vs 30%; P<.001) [30,38]. screening) that were sent over 16 days. It resulted in a significant
CHWs in Bangladesh who used mobile apps to facilitate CBE, increase in knowledge about cervical cancer and the Pap test
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(mean difference=0.619; P=.001) [25,49]. A 1-week personally loss of mobile phones, clarity of the language used, and
tailored SMS text message intervention significantly increased receiving negative results through SMS text messages.
Korean American women’s knowledge of cervical cancer Participants were interested in receiving SMS text message
screening guidelines (mean difference=0.31-0.71; P=.006) reminders for appointments; however, there was reluctance to
[25,50]. Participants who went through the Health Belief receive screening results through SMS text messages in case
Model–based cervical cancer training scored significantly higher someone else accessed their mobile phones and saw the results
in perceived benefits of a Pap test and lower in barriers to (OR 0.31, 95% CI 0.18-0.51), although they reported no issue
obtaining a Pap test, in addition to a higher uptake of Pap tests with making an appointment.
[27,40]. Female high school students who participated in
The barriers to using mHealth in reaching out to people to
Facebook or face-to-face discussions for 2 weeks after a
encourage cancer screening included inconvenience for older
50-minute classroom cervical cancer prevention education
participants, lack of texting proficiency, difficulty in texting,
lecture that included knowledge about Pap testing increased
and apprehension that SMS text messages might not be clearly
their knowledge about cervical cancer compared with those in
understood [56]. Including a reminder and keeping the SMS
the control group (β=2.942; P<.001) [31,51]. Compared with
text messages informative, short, and simple was suggested to
a telephone reminder and invitation intervention, an educational
increase screening uptake [57].
telephone call that provided a brief explanation on cervical
cancer, its risks, and colpocytological examination increased
knowledge about colpocytological examination but not attitude
Discussion
toward it [27,52]. Principal Findings
Korean women who used the mMammogram app and were This scoping review of reviews suggests that mHealth
provided with health navigation services had increased interventions can be effective in increasing cancer screening
knowledge of breast cancer screening compared with the control uptake and practice, as well as improving other screening-related
group (group difference=mean 16.93, SD 4.77; P=.001) [30,38]. outcomes such as knowledge and awareness about screening.
Users of Mammopad, a decision aid for mammogram screening, The results are consistent across different types of reviews. The
reduced decisional conflict and increased self-efficacy in relation most commonly used mHealth technologies used were SMS
to mammography, although there was no significant change in text messages and telephone calls. Interventions that included
screening intention [30,53]. Saudi Arabian women who received >1 mode of communication, such as telephone calls and SMS
breast cancer awareness information through Snapchat had text message reminders combined or together with invitation
better breast cancer awareness and knowledge, including letters, health education, or navigation services, seemed to be
knowledge about breast cancer screening (P=.01), than those more effective than interventions that included only 1 mode of
in the control group who did not receive any awareness communication. A few (4/12, 33.3%) of the reviews reported
information [31,54]. Among women who were surveyed in the implementation measures, and 75% (3/4) suggested that mHealth
tailored SMS text message mammography campaign on interventions were well accepted by participants.
Facebook during Breast Cancer Awareness Month, 82%
intended to get a mammography in the next year [31,55]. The effectiveness of interventions that used >1 mode of
communication has been demonstrated in cancer screening
Implementation Outcomes and Measures uptake in LMICs [58]; for example, in Malaysia, mass media
Of the 12 reviews, 4 (33%) [25,27,30,31] included studies that campaigns that used different channels of health promotion
examined outcomes related to the implementation of mHealth successfully increased symptom awareness of breast cancer [59]
in cancer screening uptake interventions (Table 2). Of these 4 and colorectal cancer [60].
reviews, 3 (75%) reported a high acceptance of such A very effective intervention was a combination of educational
interventions [25,30,31]. In a 1-week personally tailored SMS SMS text messages and e-vouchers to subsidize the
text message intervention, 83% of the participants expressed transportation to attend screening [37], which is especially
satisfaction with the intervention, and 97% reported that they relevant in rural areas in LMICs. In many LMICs, public
would recommend the program to their friends [25,50]. In the transport and e-hailing services are mainly available in cities,
CervixCheck intervention, 83% of the participants reported and the majority of health care facilities that offer cancer
being either “satisfied” or “very satisfied,” and 85% found the screening are located in town areas; for example, in Malaysia,
SMS text messages either “useful” or “very useful” [25,49]. travel distance to the nearest mammogram screening facility
The mMammogram intervention participants were satisfied ranged between 2 km and 340 km with a median of 22 (IQR
with the intervention (P=.003) and agreed that it was effective 12-42) km [61]. Longer travel distance to cancer services is
(P<.001) [30,38]. In a tailored SMS text message mammography associated with lower likelihood of cancer screening uptake
campaign on Facebook during Breast Cancer Awareness Month, [62] and presentation of more advanced stages of breast cancer
25% of the women surveyed agreed that they used Facebook [63] and colorectal cancer [64]. Interventions that increase
to find breast cancer screening information, and 43% agreed knowledge might not translate into higher screening uptake if
with seeing more mammogram information on Facebook underlying structural barriers to screening, such as lack of
[31,55]. transportation, are not addressed [25,27]. The use of e-vouchers
Some of the concerns of the participants regarding mHealth has been described as a form of an “enablement” intervention
interventions included confidentiality of SMS text messages,

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that reduces “barriers to increase capability or opportunity” coverage at all [70]. The rural-urban gap is especially prominent
[65]. in LMICs, where urban access to a mobile broadband network
is 2.3 times as high as rural access [70]. In LMICs, women’s
Approximately half (31/67, 46%) of the interventions included
mobile phone ownership and internet use is significantly lower
in the reviews included SMS text messaging, which uses a
than that of men’s, and the gap ranges from 50% in South Asia
cellular network and is preinstalled on every mobile phone,
and 20% in sub-Saharan Africa to 12% in the Middle East and
unlike internet-based instant messaging apps. Almost 100% of
North Africa [71].
SMS text messages are read, and 90% of them are read within
30 minutes of receipt compared with emails (approximately The gap in mobile phone ownership and internet use has
18% are read) [66], which might explain the ineffectiveness of important public health implications. mHealth interventions to
emails in improving cancer screening uptake and related increase cancer screening uptake might be less effective in rural
outcomes. Worldwide, IP-based chat apps are gaining areas, where screening uptake is already low [72]. Many (57/67,
popularity: WhatsApp, Facebook Messenger, and WeChat have 85%) of the mHealth interventions targeted cervical and breast
2 billion users, 1.3 billion users, and 1.2 billion users, cancers, the 2 most common cancers among women. Thus, the
respectively [67]. Chat apps, especially those with high open rural-urban gap in mobile access means that women from rural
rates, such as SMS text messaging [68], enable more efficient areas are at a greater risk of inequitable access to information
communication by allowing users to send longer messages; and interventions on cancer screening.
share pictures, videos, or audio messages; and chat in real time.
Given the rapid development of mHealth technologies, there is
However, because SMS text messaging is operator-based, it is
a need for researchers to incorporate them effectively into
more useful in rural areas where there is poor mobile internet
interventions. However, the speed of research does not advance
coverage. In addition, SMS text messaging is simple to use and
at the speed of mobile technology, and researchers have little
does not require additional apps, which might be more user
control over app development [30]. Most smartphone apps
friendly for those who are less tech savvy; for example, older
address tertiary cancer prevention [30], such as support for
adults.
patients with cancer in health information management [73],
In addition to SMS text messaging and chat apps, social medication adherence [74], weight management [75], and mental
networking sites, with their large numbers of users, hold great health improvement among cancer survivors [76], and there is
potential in mHealth interventions. As of July 2021, popular a lack of smartphone apps for secondary cancer prevention.
social networking sites such as Facebook and Instagram had Many of the apps developed for research are not available for
2.85 billion users and 1.39 billion users, respectively, and the download and have not been widely adopted after the studies
numbers are increasing rapidly [67]. However, in the only were concluded.
review that examined social media solely [31], the studies
mHealth holds great potential to reach out to many people in
included were mostly about low-level engagement (number of
low-cost settings, and it is also safe in times of the COVID-19
impressions, reach, likes, comments, and sharing of tweets and
pandemic where social contact has to be minimized. However,
posts), and the review highlighted the lack of studies (1/4, 25%)
it might not be acceptable to pass on personal information
that examined high-level engagement with social media
through certain mHealth technology; for example, there were
interventions, such as uptake of screening [31]. This is likely
participants who mentioned that although it was acceptable to
because of the difficulty in linking screening uptake and social
receive SMS text message reminders about their screening
media data because social media posts are not designed for such
appointment, they would not want to be informed about their
analysis. The fast pace of social media means that social media
screening results through SMS text messages. The gap could
contents could be outdated quickly or get inundated by other
be filled by CHWs, who could act as the link between mHealth
information, which reduces their reach to the target population
technologies and participants by informing the latter personally
and long-term sustainability. Running multiple campaigns on
through telephone calls of their screening results. A recent
multiple social media platforms also means that it is difficult
review found that CHWs play a critical role, particularly during
to pinpoint which campaign or platform has the greatest impact
pandemics, in community engagement [77]. CHWs are usually
on behavior change. In addition, there are age differences in
members from the same communities as the intervention
social media use; many individuals in the targeted age groups
participants and are knowledgeable about the resources available
for cancer screening might not be reached through social media.
within the communities. They may be able to reach out to
In a survey of American adults, >80% of those aged 18 to 49
vulnerable populations and encourage uptake of cancer screening
years and 73% of those aged 50 to 64 years used social media
[78] and mobile technologies [79]. However, despite proven
sites, whereas only 49% of those aged ≥65 years reported so
effectiveness of CHWs in cancer screening and early diagnosis
[69].
interventions [80], there were very few (1/12, 8%) reviews that
mHealth interventions will only work if there is access to mobile included interventions that combined mHealth and CHWs.
phones and mobile internet. Globally, although the penetration
of mobile phones and mobile internet is high, there is an unequal
Limitations
access to mobile technology and internet between urban and Given the heterogeneity of reporting and differences in the
rural areas and between sexes. All urban areas are covered by details reported in each review, it was challenging to summarize
a mobile broadband network; however, in some LMICs, 19% the evidence from the reviews concisely. In addition, some
of the rural population are covered by only a second generation reviews did not exclusively examine mHealth and cancer
network, and 17% of the rural population have no mobile screening; they included other types of interventions and
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preventive measures. Furthermore, unlike in a systematic review, conducted. In addition, engagement with different social media
the quality of the selected articles was not assessed. apps varies among age groups. Other incentives such as transport
vouchers may be included when interventions are conducted
Future Research and Recommendations among those with poor access to screening facilities. Facilitators
Future interventions should consider combining at least two to improving access to, and engagement with, mHealth among
modes of mHealth communication, for example, SMS text older adults have been described, including support from the
messages and telephone calls, and screening interventions are government and family, addressing digital problems in deprived
likely to achieve better attendance when participants receive at areas, and increasing accessibility to mobile phones or tablet
least one reminder. In addition, future interventions should computers [81]. CHWs and navigation services may be provided
consider incorporating instant messaging apps such as along with mobile technologies to support participants’ needs,
WhatsApp, Facebook Messenger, and WeChat, in addition to promote and facilitate the use of mHealth, and pass on
SMS text messaging, because the number of users is increasing information such as screening results.
exponentially, and more educational information using videos,
audio messages, or graphics could be shared. Social media Conclusions
platforms, especially Facebook, should be incorporated for mHealth interventions have the potential to increase cancer
health promotion, sharing of educational information, and screening uptake and other cancer screening–related outcomes
appointment making. When social media platforms are used, such as knowledge about screening and intention to screen.
there is a need to take into account their popularity and Combining >1 mode of communication may have a better impact
acceptability within the country where the interventions are on cancer screening uptake.
Acknowledgments
This work was supported by the UK Research and Innovation Medical Research Council (537084059) and the Newton Fund
Impact Scheme 2020-2021 (MIGHT/CEO/NUOF/4-2020 (06) for the study “Improving early detection and diagnosis of breast
cancer among multi-ethnic rural communities in Malaysia – the implementation of the community education and navigation
programme (CENP).” MD and DS were also supported by the UK Research and Innovation Medical Research Council and Global
Challenges Research Fund (MR/S014349/1) during the conduct and write-up of this study.
Authors' Contributions
DS and MMT developed the review protocol, MMT and WMKH conducted the screening independently, DS and MMT wrote
the manuscript, and TTS and MD planned the study and led in revising the manuscript. DS, WMKH, DM, and NAT revised the
manuscript. All authors provided feedback and helped shape the research, analysis, and manuscript. DS and MMT contributed
to the study equally and are joint first authors of the manuscript. TTS and MD contributed equally to the study and are joint last
authors of this manuscript.
Conflicts of Interest
None declared.
Multimedia Appendix 1
Search strategy.
[DOCX File , 19 KB-Multimedia Appendix 1]
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Abbreviations
BSE: breast self-examination
CBE: clinical breast examination
CHW: community health worker
LMICs: low- and middle-income countries
mHealth: mobile health
Pap: Papanicolaou
PRISMA: Preferred Reporting Items for Systematic Reviews and Meta-Analyses
PRISMA-ScR: Preferred Reporting Items for Systematic Reviews and Meta-Analyses extension for Scoping
Reviews
Edited by A Mavragani; submitted 13.01.22; peer-reviewed by A Spini, HL Tam; comments to author 07.03.22; revised version received
14.06.22; accepted 16.06.22; published 15.08.22
Please cite as:
Schliemann D, Tan MM, Hoe WMK, Mohan D, Taib NA, Donnelly M, Su TT
mHealth Interventions to Improve Cancer Screening and Early Detection: Scoping Review of Reviews
J Med Internet Res 2022;24(8):e36316
URL: https://www.jmir.org/2022/8/e36316
doi: 10.2196/36316
PMID:
©Désirée Schliemann, Min Min Tan, Wilfred Mok Kok Hoe, Devi Mohan, Nur Aishah Taib, Michael Donnelly, Tin Tin Su.
Originally published in the Journal of Medical Internet Research (https://www.jmir.org), 15.08.2022. This is an open-access

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article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/),
which permits unrestricted use, distribution, and reproduction in any medium, provided the original work, first published in the
Journal of Medical Internet Research, is properly cited. The complete bibliographic information, a link to the original publication
on https://www.jmir.org/, as well as this copyright and license information must be included.

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JOURNAL OF MEDICAL INTERNET RESEARCH Schliemann et al

mHealth Interventions to Improve Cancer Screening and Early

(J Med Internet Res 2022;24(8):e36316) doi: 10.2196/36316

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different types of reviews. However, it is unknown whether

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Selection of Reviews WMKH independently for inclusion, with discrepancies resolved

selected reviews. For reviews that included studies that focused

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Table 1. Characteristics of included reviews.

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Characteristics of Reviews included studies that were conducted mainly in high-income

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Table 2. Summary of screening-related outcomes extracted from each review.

Uy et al [26], 2017 • Screening uptake: n=5/9 (1.2%-9.9% —c —

Halake and Ogoncho • Screening uptake: n=1/1 (30.7% and — —

Choi et al [29], 2018 • Screening uptake: n=1/1 (27% absolute — —

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Musa et al [32], • Screening uptake: n=5/6 (7.8%-31.1% — —

Duffy et al [33], • Screening uptake: n=13/16 (5%-45% — —

Lott et al [34], 2020 • Screening uptake: n=2/3 (8.6% differ- — —

Déglise et al [35], • BSE practice: n=1/1 — —

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with an abnormal clinical breast examination (CBE). A

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