Oketch et al.

BMC Women's Health (2019) 19:75

https://doi.org/10.1186/s12905-019-0778-2

RESEARCH ARTICLE Open Access

Perspectives of women participating in a

cervical cancer screening campaign with
community-based HPV self-sampling in
rural western Kenya: a qualitative study
Sandra Y. Oketch1* , Zachary Kwena1, Yujung Choi2, Konyin Adewumi2, Michelle Moghadassi3,
Elizabeth A. Bukusi1,4,5,6 and Megan J. Huchko2,7

Abstract
Background: Despite cervical cancer being preventable with effective screening programs, it is the most common
cancer and the leading cause of cancer-related death among women in many countries in Africa. Screening
involving pelvic examination may not be feasible or acceptable in limited-resource settings. We sought to evaluate
women’s perspectives on human papillomavirus (HPV) self-sampling as part of a larger trial on cervical cancer
prevention implementation strategies in rural western Kenya.
Methods: We invited 120 women participating in a cluster randomized trial of cervical cancer screening
implementation strategies in Migori County, Kenya for in-depth interviews. We explored reasons for testing,
experience with and ability to complete HPV self-sampling, importance of clinician involvement during screening,
factors and people contributing to screening decision-making, and ways to encourage other women to come for
screening. We used validated theoretical frameworks to analyze the qualitative data.
Results: Women reported having positive experiences with the HPV self-sampling strategy. The factors facilitating
uptake included knowledge and beliefs such as prior awareness of HPV, personal perception of cervical cancer risk,
desire for improved health outcomes, and peer and partner encouragement. Logistical and screening facilitators
included confidence in the ability to complete HPV self-sampling strategy, proximity to screening sites and feelings
of privacy and comfort conducting the HPV self- sampling. The barriers to screening included fear of need for a
pelvic exam, fear of disease and death associated with cervical cancer. We classified these findings as capabilities,
opportunities and motivations for health behavior using the COM-B framework.
Conclusions: Overall, HPV self-sampling was an acceptable cervical cancer screening strategy that seemed to meet
the needs of the women in this community. These findings will further inform aspects of implementation, including
outreach messaging, health education, screening sites and emphasis on availability and effectiveness of
preventative treatment for women who screen positive.
Keywords: HPV self-sampling, Cervical cancer screening, COM-B, Theoretical domains framework, LMIC

* Correspondence: [email protected]
1
Center for Microbiology Research, Kenya Medical Research Institute, P. O.
Box 54840 00200, Mbagathi Road, Nairobi, Kenya
Full list of author information is available at the end of the article

© The Author(s). 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0
International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and
reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to
the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver
(http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
Oketch et al. BMC Women's Health (2019) 19:75 Page 2 of 10

Background frameworks (TDF) mapped to the capacity (C), oppor-

Cervical cancer deaths worldwide were estimated at 275, tunity (O) and motivation (M) to bring about behavior
000 annually and over 530,000 new cases diagnosed [1]. (B) change (COM-B) [21, 22].
This is despite the fact that cervical cancer is prevent-
able with effective screening and treatment of pre- Methods
invasive lesions [2]. The incidence of cervical cancer is Design
highest in low- and middle-income countries (LMICs) This qualitative study was conducted as part of a larger
where about 80% of new cases [3] and 85% of deaths cluster-randomized trial comparing two implementation
occur [4]. It is the most common cancer affecting strategies for community-based HPV testing carried out
women and the leading cause of cancer deaths in many between January and September 2016 in Migori County,
countries in Africa [5, 6]. In Kenya, cervical cancer is the Kenya (Clinicaltrials.gov, NCT02124252) [23]. We
leading female cancer and cause of cancer-related deaths sought to determine women’s perspectives on acceptabil-
for women with an incidence of 20.5 per 100,000 women ity of and experiences with an HPV self-sampling strat-
[5]. New cases and mortality are expected to rise by 75% egy through in-depth interviews (IDIs) with a purposive
by 2025 in the absence of substantial scale interventions sample of 120 women participating in the community
for screening and early treatment [7]. driven cervical cancer prevention program.
While high quality, accessible and acceptable screening
programs are necessary to prevent cervical cancer [8], Parent study description and settings
trained human resources, functional referral and labora- Migori County is located in Western Kenya, with some
tory facilities, and lack of transport and tracking systems areas bordering Lake Victoria. This area has one of
make cytology-based screening strategies unfeasible in the highest HIV prevalence rates in the region
most LMICs [2]. Women in LMICs have a low screening (15.1%) [24, 25]. The parent study enrolled women
rate with only 3.5% of women aged between 25 to 64 aged 25 to 65 years living within selected communities
years screened in any 3-year period [5]. High-risk human within Migori County, and offered HPV-based self-
papillomavirus (HPV) is the primary cause of almost all screening in health facilities or through community
cervical cancer [7]. Testing for HPV is a simple, low- health campaigns between January to September 2016
cost technology that has been shown to reduce the [23]. The main outcomes and study design are
cervical cancer incidence and related mortality when presented elsewhere [26]. Relevant to this study,
directly coupled with outpatient cryotherapy treatment Community Health Volunteers (CHVs) explained the
for women testing HPV positive [2, 9, 10]. The World self-sampling procedure during outreach and
Health Organization (WHO) recommends a simplified mobilization activities in public, group settings and
HPV screen & treat as a strategy for cervical cancer through door-to-door mobilization. More detailed
control in LMICs [11]. To increase screening coverage, messages were provided immediately prior to screen-
HPV testing has been offered to women via self- ing through a group educational module in both
collection, removing the need for a pelvic exam, clinic health facility and community settings. Posters with
setting and a trained provider [12–17]. diagrams and instructions for self-collection were dis-
Although the strategy of HPV self- sampling would ad- played in private rooms at campaign sites and health
dress many logistical barriers, the ultimate success of facilities where the self-sampling took place.
this strategy depends upon its acceptability among Specimens were collected using careHPV™ (Qiagen,
women in the target population. Studies have confirmed Gaithersburg, MD) in a private area and returned to
a high acceptability to HPV self-sampling in different the CHVs, who periodically transported them to the
settings [15, 18, 19]. Though other studies have com- laboratory in the Migori County Referral Hospital for
pared HPV collection through clinician versus self- processing. Participants received their results in
sampling [18] only a few studies have provided self- approximately two weeks via their choice of text
sampling in community settings [15, 19] thus, the need message, phone call, or home visit.
to investigate whether this strategy would be an accept-
able form of screening. This has not been studied in Sample size and sampling framework
rural western Kenya, a low-resource setting with limited For this qualitative study, we used purposive sampling
access to health facilities and multiple barriers to pelvic and asked CHVs to identify participants who would be
exams that could be avoided in a community based self- willing to share their experiences with screening. We
sampling strategy [20]. We sought to examine women’s determined that a sample size of 10 interviews per com-
perspective and experience with HPV self-sampling munity would provide enough information and variation
using two frameworks that merges internal, interper- in data within the target population [27]. We therefore
sonal and systems factors, of the theoretical domain recruited participants until we reached ten participants
Oketch et al. BMC Women's Health (2019) 19:75 Page 3 of 10

from each of the twelve study communities. The face-to- influence of beliefs and behaviors to inform of this and
face interviews were conducted by trained qualitative in- future implementation strategy.
terviewers after women underwent the self-sampling at
either the community health campaign or health facility. Results
The questions from the IDI guide were developed from The TDF allowed for the identification of the facilita-
literature review and had both multiple choice and open- tors to screening which included awareness and
ended sections. Quantitative measures included questions acceptability of HPV self-sampling, personal percep-
on socio-demographic attributes and acceptability of HPV tion of cervical cancer risk, confidence in the ability
self-sampling. They were followed by open-ended to complete HPV self-sampling, peer and partner
questions that explored reasons for testing, self-sampling encouragement, privacy and comfort conducting the
experience, importance of clinician involvement during HPV self-sampling, proximity to screening sites,
screening, the factors and people contributing to screen- improved health outcomes and desire to know HPV
ing decision, and what can be done to encourage other status. The identified barriers to screening were:
women in the community to come for screening. The social stigma associated with cervical cancer, a
guide was developed in English, translated to the local lan- number of fears were reflected which included fear of
guages (Luo and Kiswahili), and then back-translated into pelvic exam and fear of disease and death. These
English to ensure accuracy. IDIs lasted approximately 20– domains were mapped to the behavior change
30 min and were audio-recorded into an MP3 file and constructs of capability, opportunity and motivation
then transcribed and translated. All translations were read (Table 1).
again along with the audio by a member of the study team The mean age of the 120 women interviewed was 36.1
to confirm accuracy. years, (SD = 9.55). Over half (59.4%) the women
interviewed had up to a primary school education. Over
three quarters (78%) were married with a median of 4
Data analysis (IQR 3–5) children, and 16% of women had undergone
We utilized a theoretical thematic analysis approach to prior screening (Table 2).
identify themes during the coding process [28]. A code-
book was developed based on a thorough review of five Capability
sample IDI transcripts. Using NVivo10 [29], a group of Themes related to capability nested within the TDF
five members of the research team coded the transcripts domains of knowledge and skills and included awareness
independently, with each transcript coded by two mem- and acceptability of HPV self-sampling and participant’s
bers producing coding reports for joint review. Coding confidence in their ability to complete HPV self-
reports were discussed in a series of meetings to refine sampling strategy. There were all seen to influence their
the codebook and guide the analysis and the themes decision to be screened.
considered in relation to the domains in the TDF and
then mapped onto the segments of COM-B framework. Awareness and acceptability of HPV self-sampling
Theoretical Domains Framework is used to identify The majority of women mentioned both their own
the facilitators and barriers and influences on behavior volition and an awareness of self-sampling availability in
in application of specific evidence based behaviors and screening decision making. One married woman with no
can be used in qualitative studies to understand imple- prior screening stated “It was my own decision when I
mentation and provide insight to an intervention and its heard about it I saw it wise to go for it”. Most women
mechanism of change [21, 30–32]. The TDF domains thought that the self-sampling would be widely accepted
have been shown to have influence on the behaviors by the community “because they are afraid of the metal
across all levels of health implementation and uptake insertion procedure. They will go for this”. Some women
[21, 30]. The sources of behavior, COM-B, has been used had anxiety about the procedure, seen in the following
to understand behavior change interventions and it cate- quotes: “Those who haven’t gone for the test feel that the
gorizes behavior in terms of the three key determinants procedure can lead into a scratch …: ” and that “… .some
of capability, opportunity and motivation [33] . The TDF women told me that they are scared of having to use the
has been validated for use in the COM-B, behavior care brush”. Others felt that the privacy allowed with
change wheel and the two frameworks are used together self-sampling afforded them agency.
to inform intervention and describe behavior change in
implementation and behavior change research [21, 22]. “They will [get screened] because the test is not painful
The combination of these two frameworks guided our and it is not difficult. If you go to the testing room, you
analysis in an attempt to ensure an understanding of are all alone just like in your own room, so you are
women’s perspective on HPV self-sampling to assess the just free”. (Married woman with no prior screening)
Oketch et al. BMC Women's Health (2019) 19:75 Page 4 of 10

Table 1 Key findings from women’s perspective on HPV sampling mapped onto the TDF and COM-B frameworks
COM-B TDF Domain TDF Domain Description Key Findings
Component
Capability Knowledge An awareness of the existence of something Awareness and acceptability of HPV self-
sampling
Skills An ability or proficiency acquired through Confidence in their ability to complete HPV
practice self-sampling strategy
Role of clinicians in HPV sample collection
Opportunity Social Influences Those interpersonal processes that can Peer and partner encouragement
cause an individual to change their Social stigma associated with cervical cancer
thoughts, feelings, or behaviors
Environmental Context and Any circumstance of a person’s situation or Proximity to cervical cancer screening sites
Resources environment that discourages or Fear of pelvic screening
encourages the development of skills and
abilities, independence, social competence,
and adaptive behavior
Motivation Social Role and Identity A coherent set of behaviors and displayed Feeling of privacy and comfort conducting
personal qualities of an individual in a social the HPV self-sampling
or work setting
Beliefs about Capabilities Acceptance of the truth, reality, or validity Personal perception of cervical cancer risk
about an ability, talent, or facility that a Screening will improve health outcomes
person can put to constructive use
Beliefs about Consequences Acceptance of the truth, reality, or validity Fear of disease and death
about outcomes of a behavior in a given
situation
Note: Description data from Cane et al. [23]

Confidence in the HPV self-sampling strategy the new type of testing was easy to undertake with no
When asked whether women would be able to complete difficulties”.
the testing, we had almost uniform responses of confi-
dence. Some of the facilitators to screening completion Role of clinicians in HPV sample collection
included “… ..the procedure does not take time”, “because Despite women’s confidence in and preference for a self-
it is private and one performs the test by herself” and “… collection without a pelvic exam, there were diverse

Table 2 Socio-demographic characteristics and reproductive history of participants (n = 117)

Socio-demographic Characteristics n (%) Reproductive History Characteristics n (%)
Age Mean (SD) 36.08 (9.55) Number of children (IQR) 4 (3,5)
Education Level Family planning use (n = 80)
Primary 77 (55.8) Yes 36 (45.0)
Secondary 28 (24.0) No 44 (55.0)
College and beyond 8 (6.8)
None 4 (3.4)
Occupation Previous cervical cancer screening (n = 80)
Agriculture and fishing 42 (35.9) Yes 16 (20.0)
Sales and services 32 (27.3) No 64 (80.0)
Professional/Technical/Managerial 16 (13.7) Previous cervical cancer screening type
Skilled and unskilled manual 11 (9.4) Pap smear 6 (37.5)
Housewife/None 16 (13.7) VIA/VILI 10 (62.5)
Relationship Status Previous cervical cancer screening result
Married/Partnered 91 (77.8) Negative 15 (93.8)
Widowed/Divorced 24 (20.5) Positive 1 (6.2)
Single 2 (1.7)
Note: Missing quantitative data for 3 participants
Oketch et al. BMC Women's Health (2019) 19:75 Page 5 of 10

opinions on the need for clinician presence. The women ….” . There were also feelings that general belief that
who expressed a desire for clinicians felt their role would cervical cancer is a life threatening disease was a major
be to provide any additional information about screening hindrances to testing. Women suggested education and
and results, and be available for treatment after a HPV counseling as a measure to counter the stigma and
positive screen test. We did not find any women who create positive attitudes towards screening.
preferred clinicians to provide screening via pelvic exam.
“They will not accept because they feel that cancer is a
“In relation to the new self-test kits that have emerged, deadly disease. So I feel that they should be counseled
it isn’t a must that the health care provider to be next and taught about this disease in such a way that they
to you … ”. (Unmarried woman with no prior would feel free to do the cervical cancer test”.
screening) (Unmarried woman with prior screening using
VIA/VILI)
“I would wish for the clinician to be there so that after
getting tested and I end up being positive the doctor is
able to … [perform the] treatment already but not Proximity to cervical cancer screening sites
that I look for money and go to Migori”. (Married A majority of women reported that long distance travel
woman, with no prior screening) may be a barrier due to high travel costs and travel time
away from home and chores. Some suggested that HPV
screening was a better option when offered “at the com-
Opportunity munity site, because you may even lack fare when screen-
Themes related to opportunity nested within the TDF ing is taken to a far place.” This same sentiment was
domain of social influences included peer and partner expressed about treatment sites and availability.
encouragement, social stigma associated with cervical
cancer. The environmental resources and context “It depends on how I am that way because, if it were
domains were mapped and the ideas about proximity to near I would perform my responsibilities and later go
screening sites and fear of pelvic screening as influencing for treatment but if it is far transport will be an issue,
behavior and attitude to screening uptake. so it’s better if it were near because I will be able to go
for the treatment and later perform my duties”.
Peer and partner encouragement (Unmarried woman with no prior screening)
Women cited peer and partner encouragement as influ-
ential in their decision making process, which shows the Many of the communities are located considerable dis-
significance of these support systems to screening. A tances (average 24 km) from the health facilities and
number of women recounted how their peers shared most of these facilities lack the screening and treatment
their self-sampling experience which encouraged them resources needed. The inadequacy of the resources and
to get screened. Common sentiments included “those proximity to screening services intensifies the lack of
who have screened encourage those who have not by screening and under screening. The majority of women
telling them the benefits of screening …” and “I was appreciated the fact that the HPV screening services
encouraged by those of us who have been through the were brought closer to them through community out-
process”. Other women mentioned the role their male reach and in the nearby health centers which facilitated
spouses played which included encouragement and their ability to access HPV self-sampling.“Maybe if it
support to get screened. [HPV screening] could have been far I wouldn’t have
gone and so the fact that it [HPV screening] was closer
“I had been talking with my husband about it [HPV is what made me make the decision to come”.
self-testing] and … … My husband could encourage me (Married woman with no prior screening)
that cancer is a deadly disease and that I should go
for early screening so that I can be able to be
screened”. (Married woman with no prior screening) Fear of pelvic screening
Fear of cervical cancer screening was reflected when
women mentioned that they would feel pain from the
Social stigma associated with cervical cancer pelvic exam procedure which acted as a possible barrier
There was an indication of stigma where some women to screening. There was also the feeling of embarrass-
feared being associated with having the disease. ment if male providers offered screening through a pel-
“Generally people fear others seeing them going for vic exam. All of these factors from the women’s previous
screening because they might think one has the disease screening experiences made them hesitant to go for
Oketch et al. BMC Women's Health (2019) 19:75 Page 6 of 10

screening again, and therefore making the HPV self- necessary prevention mechanisms in recognition of their
sampling approach an attractive opportunity. increased susceptibility to complications.

“The fact that I get to do the test on my own and I “I wanted to know my [HPV] status so that if at all I
don’t have to expose myself to a male doctor {laughs} test positive I can be helped before it progresses
the way it was before.” (Married woman with no prior secondly, me knowing my [HPV] status, will be good in
screening) a way that I would be able to start on early treatment,
even if I don’t have I will be able to know and that is
“ … .I used to hear that those who were being tested why I decided to come for the test”. (Married woman
were experiencing pain because there was something with prior screening using Pap smear)
that was being inserted inside them, it was great pain,
and this scared me from going for the test, so when “First and foremost I am HIV positive so my immune
you introduced the new type of testing, I made a system is low, and so it forces me to always come and
decision to come for it”. (Married woman with no do the test”. (Married woman with prior screening
prior screening) using Pap smear)

Motivation Screening will improve health outcomes

Themes related to motivation nested within the TDF Women reported that their reason for HPV self-
domain of social identity included the feelings of privacy sampling was to improve their health outcome by taking
and comfort conducting the HPV self-sampling. The beliefs necessary steps based on the test result where those who
about capabilities domains identified included personal per- screen positive for HPV are able to seek early treatment
ception of cervical cancer risk and improved health out- as a preventive measure. Some women stated the role
comes. The theme of fear of disease and death was mapped the education played in their understanding of screening
onto the domain of beliefs about consequences. in improving their health outcome as illustrated by this
quote “I made the decision because I was taught that if
it [HPV] gets [into] and stays in the uterus, it turns to
Feeling of privacy and comfort conducting the HPV self- full-blown cancer and it shortens one’s life, and if de-
sampling tected early you can still find help”. As such, indicating
Most women reiterated that self-sampling eliminated the that education and awareness of the cervical cancer pre-
embarrassment and fear they had from pelvic exam by a vention initiated and influenced their personal decision
clinician and reported having a positive experience to screen.
conducting the self-sampling compared to previous
testing with a pelvic exam. “Because it is private and one “I heard of the benefits of doing the [HPV] screening to
performs the test by herself”, “… … and the procedure prevent it, because prevention is better than cure.”
does not take time”. (Married woman with no prior screening)

“What I didn’t like is that initially there was a way “The reason why we do HPV testing is to make one
through which cancer was being screened [with a aware of their status in relation to HPV, such that if
pelvic exam] … that I didn’t like so I was scared. I felt they are found to be positive then they would know
that these doctors are from the community and maybe how to get treatment in good time when it’s not yet too
I would meet up with them at a later time in the late”. (Unmarried woman with prior screening using
village and so this was a burden, but with the self-test VIA/VILI)
kit I felt it was good because I could test myself”.
(Unmarried woman with no prior screening) One woman expressed a desire to test for HPV to avoid
complications that would interfere with childbearing. This
acted as a motivator to seek cervical cancer screening:
Personal perception of cervical cancer risk
Most of the women were aware of the fact that they “What contributed to my decision to get screened was I
were susceptible to cervical cancer and that early HPV wanted to know whether I was HPV positive or
screening would prevent disease progression. “I wanted negative, according to my age I still need to have
to know my status, I might be having cancer yet I don’t children, so if you keep silent about it without knowing
know, so I wanted to know so that I seek treatment”. For what is going on, it is good if you know earlier”.
some HIV-positive women, they wanted to employ any (Married woman with no prior screening)
Oketch et al. BMC Women's Health (2019) 19:75 Page 7 of 10

Fear of disease and death self-sampling approach provides the opportunity to

Some women mentioned fear of disease and death if eliminate some of these barriers and improve on screen-
they do not get early screening, so this encouraged ing uptake. Health system factors such as access and
women to get screened to know their HPV test results proximity to care were also identified as barriers to con-
so as to be able to seek treatment in time as late ventional screening, as they have also acted for other
detection and failure to seek treatment was associated prevention programs as has been found in other studies
with death. [37, 38, 40–43]. Important facets of environmental con-
text and resources include the need to increase commu-
“I have seen cervical cancer kill those who did not nity outreach, provide access to screening and treatment
want to go to the hospital for screening. That is why services in central locations and ensure privacy for
when I heard about it, I decided to go for the screening women undergoing counseling and testing.
so that in case I am HPV positive, I find help”. We also identified some areas of stigma around HPV
(Unmarried woman with no prior screening) and cervical cancer. While this was not a frequent find-
ing, it concurs with other studies which have also found
“You know some fear. One might say, I will go there that having pre cancer or cervical cancer has been
and be found to have the virus … . That is what scares stigmatized with women fearing being “talked” about or
a lot of people. They really do not know what they are facing discrimination [37, 39]. Our results support the
going to screen for. They wait until they get worse that need for improved community education and stigma re-
is when they go”. (Married woman with prior duction to ensure high uptake of screening and support
screening using VIA/VILI) for women who screen positive. We found that peer and
partner encouragement, mapped to the social influences
domain, were common and an important motivator for
Discussion screening. The social support systems of peer and part-
Innovative cervical cancer screening strategies are an es- ner support is important in successful implementation
sential part of the prevention cascade that will ultimately of health prevention programs [40] consequently, ensure
reduce the global disparity in cervical cancer incidence. high cervical screening participation and attendance.
Effective implementation of cervical cancer prevention The motivation construct illustrated the women’s be-
services requires reaching women at the community havior to screening under the beliefs about capabilities
level with programs that are acceptable, inexpensive, domain whereby the perception of one’s susceptibility to
easy to use, and sustainable. HPV self-sampling may cervical cancer does affect screening behavior and for
bridge the gap for women in underserved areas as it has women who expressed personal susceptibility to cervical
the potential to increase screening availability in more cancer believed it was necessary to have HPV self- test
remote areas, by using a less invasive procedure. We done and vice versa to those who expressed lack of per-
found that women in rural western Kenya had positive sonal susceptibility [44–46]. As has been previously doc-
expectations of and personal experiences with HPV self- umented, knowledge and perception play a key role in
sampling, which compared favorably to prior experience influencing screening behavior [47–51]. The domain on
with or beliefs about pelvic exams which is consistent to belief about consequences also reflected the women’s
other studies done in Africa and Asia [18, 19, 33–35]. motivation construct that highlight barriers to HPV
Also, HPV self-sampling has been found to improve screening which include the fear of disease and death
screening uptake [36]. Acceptability of this method sug- which has been identified in other studies [18, 52]. To
gests an opportunity to increase attendance and screen- address the issue of fear of potentially learning that one
ing through community based programs in LMICs. has cancer, a rigorous screening awareness campaign is
Using the TDF to map drivers of behavior change needed to empower the women and address the fears of
(COM-B), we found that environmental context and re- screening and an understanding to personal perception
sources were the most widely cited, followed by social of cervical cancer risk.
influences, both under the opportunity construct. This study is limited by the inclusion of data only from
Women reported that cervical cancer screening using an women who had already self-sampled for HPV. As such,
exam-based method elicited a number of barriers that we do not have the perspectives of those who did not
were not part of HPV self-screening. The findings on participate, a population who may be the most difficult
pelvic exam as a barrier to screening is consistent with to reach and may better articulate the barriers to self-
other studies done in Africa and Asia [18, 19, 33–35] sampling. We also sampled a population with a high
which showed concerns around speculum use, HIV prevalence and a strong response to the epidemic,
embarrassment, and reluctance to have a male provider which may consequently have been exposed to prior re-
perform the exam [37–39]. Consequently, employing the search studies and health interventions that may have
Oketch et al. BMC Women's Health (2019) 19:75 Page 8 of 10

influenced their health beliefs and behaviors. These Authors’ contributions

may impact their response towards the HPV self- SYO wrote the initial manuscript draft, participated in the conceptualization
of the study and design, data collection, analysis and interpretation,
sampling uptake and thus may also not be manuscript writing. ZK participated in the conceptualization of the study and
generalizable to other rural populations without such design, manuscript writing. KA and YC participated in the data analysis,
a robust response to HIV. These limitations notwith- manuscript review. MM participated in the conceptualization of the study
and design, manuscript writing. EAB participated in the conceptualization of
standing, our results inform of women’s experiences the study and design, manuscript writing and gave the overall scientific
and insights to HPV self- sampling approaches to this guidance and leadership. MJH participated in the conceptualization of the
settings. Also, due to the study’s cluster randomized study and design, manuscript writing and gave the overall scientific
guidance and leadership. All authors reviewed and approved the manuscript.
design, it provides a representative sample and the
participants were potentially comfortable due to the Funding
fact that the interviews were conducted in their native Research reported in this publication was solely supported by National
Cancer Institute of the National Institutes of Health under award number
languages. This study’s use of behavior change theory R01CA188248. The content is solely the responsibility of the authors and
provides a novel aspect of understanding women’s does not necessarily represent the official views of the National Institutes
perspectives and experiences that influences their of Health.
The funders had no role in the study design, data collection and analysis,
screening behavior. interpretation of data, writing the manuscript or decision to publish.

Availability of data and materials

Conclusion The data sets used and/or analysed during the current study are available
from the corresponding author upon reasonable request.
A combination of the TDF and COM-B allowed for
identification of the women’s facilitators and barriers Ethics approval and consent to participate
to screening which in turn described potential drivers The study was approved by the Kenya Medical Research Institute (KEMRI)
Scientific and Ethical Review Committee (Protocol No. 2918), the University
of behavior change in the relation to screening with
of California, San Francisco Committee for Human Research, and the Duke
self-collected HPV. The health systems in low income University Institutional Review Board. All participants gave written informed
regions have limited financial and human resources consent before participation in the study.
therefore prevention of cervical cancer remains an
Consent for publication
unmet priority. Thus, acceptability of self-sampling in There is no identifiable participant data.
the community setting is encouraging as these can
ensure focus on treatment efforts for those who Competing interests
The authors declare that they have no competing interests.
screen positive. Increased community awareness and
emphasis that screening would not involve a pelvic Author details
1
exam, can be done in privacy, and would still involve Center for Microbiology Research, Kenya Medical Research Institute, P. O.
Box 54840 00200, Mbagathi Road, Nairobi, Kenya. 2Duke Global Health
provider counseling and may encourage even broader Institute, Box 90519, 310 Trent Drive, Durham, NC 27710, USA. 3Department
participation in organized screening campaigns. of Obstetrics and Gynecology, University of California San Francisco, 550 16th
Cervical cancer screening access in terms of distance Street, 3749, San Francisco, CA 94158, USA. 4Department of Obstetrics and
Gynecology, University of Nairobi, P. O. Box 54840 00200, Nairobi, Kenya.
and convenience provide opportunities to increase 5
Department of Obstetrics and Gynecology, Aga Khan University, P. O. Box
screening uptake. Future research efforts should focus 30270 00100, Third Avenue, Limuru Rd, Nairobi, Kenya. 6Departments of
on the self-sampling delivery and infrastructure Obstetrics and Gynecology, University of Washington, P. O. Box 356460,
Seattle, WA 98195, USA. 7Department of Obstetrics and Gynecology, Duke
strengthening. University, Box 90519, 310 Trent Drive, Durham, NC 27710, USA.

Received: 1 November 2018 Accepted: 5 June 2019

Abbreviations
CHVs: Community Health Volunteers; COM- B: Capability, Opportunity and References
Motivation in Behavior; HIV: Human Immunodeficiency Virus; HPV: Human 1. de Sanjosé S, Serrano B, Castellsagué X, Brotons M, Muñoz J, Bruni L, Bosch
papilloma Virus; IDI: In depth interview; LMICs: Low and Middle Income FX. Human papillomavirus (HPV) and related cancers in the global Alliance
Countries; TDF: Theoretical Domain Framework; VIA: Visual inspection with for vaccines and immunization (GAVI) countries: a WHO/ICO HPV
acetic acid; VILI: Visual inspection with lugols iodine solution; WHO: World information Centre report. Vaccine. 2012;30(Suppl 4):D1–83.
Health Organization 2. Denny L, Kuhn L, De Souza M, Pollack AE, Dupree W, Wright TC. Screen-
and-treat approaches for cervical cancer prevention in low-resource settings: a
randomized controlled trial. J Am Med Assoc. 2005;294(17):2173–81.
Acknowledgements 3. Sherris J, Herdman C, Elias C. Beyond our Borders: cervical cancer in the
We are grateful to the women who participated in this study and gave their developing world. West J Med. 2001;175(4):231.
invaluable time. We thank the National Institutes for Health, National Cancer 4. Ferlay J, Shin H-R, Bray F, Foreman D, Mathers C, Parkin DM. GLOBOCAN
Institute for the funding support. We are grateful to the Director KEMRI and 2008 v1.2, Cancer Incidence and Mortality Worldwide: IARC Cancer Base
Director CMR. We appreciate the Migori County Ministry of Health. We No. 10. 2010. http://globocan.iarc.
acknowledge the study team for their important contributions towards this 5. Bruni L, Albero G, Serrano B, Mena M, Gómez D et al. ICO/IARC information
research. We thank Purba Chatterjee and Irene Okumu from the UCSF/ Centre on HPV and Cancer (HPV information Centre). Human papillomavirus
FACES Evaluation unit program for their guidance, manuscript reviews and and related diseases in Kenya. Summary Report. 2018. www.hpvcentre.net.
suggestions. We thank Dr. Janet Turan for her reviews and suggestions. Accessed 16 May 2019.
Oketch et al. BMC Women's Health (2019) 19:75 Page 9 of 10

6. World Health Organization (WHO). Comprehensive cervical Cancer control: a 28. Braun V, Clarke V. Using thematic analysis in psychology. Qual Res Psychol.
guide to essential practice. 2nd Edi. 2014. 2006.
7. Ministry of Public Health and Ministry of Medical Services. 29. QSR International. NVivo qualitative data analysis software | QSR
Government of Kenya. National Guidelines for prevention and international Pty ltd. version 10. 2012. https://www.qsrinternational.com/
Management of Cervical, breast and prostate Cancers. 2012. nvivo/home.
8. Sankaranarayanan R. Cancer survival in Africa, Asia, the Caribbean and 30. Atkins L, Francis J, Islam R, O’Connor D, Patey A, Ivers N, et al. A guide to
Central America. Introduction IARC Scientific Publications. 2011:1–5. using the theoretical domains framework of behaviour change to
9. lin QY, Sellors JW, Eder PS, ping BY, Lim JM, hui ZF, et al. A new investigate implementation problems. Implement Sci. 2017;12(1):77.
HPV-DNA test for cervical-cancer screening in developing regions: a 31. Phillips CJ, Marshal AP, Chaves NJ, Jankelowitz SK, Lin IB, Loy CT, et al.
cross-sectional study of clinical accuracy in rural China. Lancet Oncol. Experiences of using the theoretical domains framework across diverse
2008;9:929–36. clinical environments: a qualitative study. J Multidiscip Healthc. 2015;8:139.
10. Sankaranarayanan R, Nene BM, Shastri SS, Jayant K, Muwonge R, 32. Michie S, Seers K, Chandler J, Hawkes CA, Crichton N, Allen C, et al. Making
Budukh AM, et al. HPV screening for cervical Cancer in rural India. N psychological theory useful for implementing evidence based practice: a
Engl J Med. 2009. consensus approach. BMJ Qual Saf. 2005;14:26–33.
11. World Health Organization. WHO guidelines for screening and treatment of 33. Gottschlich A, Rivera-Andrade A, Grajeda E, Alvarez C, Mendoza Montano C,
precancerous lesions for cervical cancer prevention: WHO Press; 2013. Meza R. Acceptability of human papillomavirus self-sampling for cervical
12. Agurto I, Arrossi S, White S, Coffey P, Dzuba I, Bingham A, et al. Involving Cancer screening in an indigenous Community in Guatemala. Journal
the community in cervical cancer prevention programs. Int J Gynecol Global Oncol. 2017;3:444–54.
Obstet. 2005;89:S38–45. 34. Senkomago V, Saraiya M. Examining acceptability of self-collection for
13. Arrossi S, Thouyaret L, Herrero R, Campanera A, Magdaleno A, Cuberli M, et human papillomavirus testing among women and healthcare providers
al. Eff ect of self-collection of HPV DNA offered by community health with a broader lens. J Women’s Health. 2017;26. https://doi.org/10.1089/jwh.
workers at home visits on uptake of screening for cervical cancer (the EMA 2017.6384.
study): a population-based cluster-randomised trial. Lancet Glob Health. 35. Oranratanaphan S, Termrungruanglert W, Khemapech N. Acceptability of
2015;3:e85–94. self-sampling HPV testing among Thai women for cervical Cancer screening.
14. Sewali B, Okuyemi KS, Askhir A, Belinson J, Vogel RI, Joseph A, et al. Cervical Asian Pac J Cancer Prev. 2014;15:7437–41. https://doi.org/10.7314/APJCP.
cancer screening with clinic-based pap test versus home HPV test among 2014.15.17.7437.
Somali immigrant women in Minnesota: a pilot randomized controlled trial. 36. Sarai Racey C, Withrow DR, Gesink D. Self-collected HPV testing improves
Cancer Med. 2015;4:620–31. participation in cervical Cancer screening: a systematic review and meta-
15. Crosby RA, Hagensee ME, Vanderpool R, Nelson N, Parrish A, Collins T. analysis. Canadian J Public Health. 2013;104:e159–66.
Community-based screening for cervical cancer: A feasibility study of rural 37. Buchanan Lunsford N, Ragan K, Lee Smith J, Saraiya M, Aketch M.
Appalachian women. Sexually Transmitted Dis. 2015;42:607. Environmental and psychosocial barriers to and benefits of cervical Cancer
16. Barbee L, Kobetz E, Menard J, Cook N, Blanco J, Barton B, et al. Assessing screening in Kenya. Oncologist. 2017;22:173–81. https://doi.org/10.1634/
the acceptability of self-sampling for HPV among haitian immigrant women: theoncologist.2016-0213.
CBPR in action. Cancer Causes Control. 2010;21:421–31. 38. Arrossi S, Ramos S, Straw C, Thouyaret L, Orellana L. HPV testing: a mixed-
17. De Alba I, Anton-Culver H, Hubbell FA, Ziogas A, Hess JR, Bracho A, et al. method approach to understand why women prefer self-collection in a
Self-sampling for human papillomavirus in a community setting: feasibility middle-income country. BMC Public Health. 2016;16:832.
in Hispanic women. Cancer Epidemiol Prevent Biomark. 2008;17:2163–8. 39. Lim JNW, Ojo AA. Barriers to utilisation of cervical cancer screening in sub
18. Bansil, Pooja and Wittet, Scott and Lim, Jeanette L and Winkler, Jennifer L Sahara Africa: a systematic review. European J Cancer Care. 2017;26:e12444.
and Paul, Proma and Jeronimo J. Acceptability of self-collection sampling 40. Zachary O, Turan J, Bukusi EA, Cohen CR, Gray GEMK. “You know you
for HPV-DNA testing in low-resource settings: a mixed methods approach. are sick, why do you carry a pregnancy again?” applying the socio-
BMC Public Health 2014;14:596. ecological model to understand barriers to PMTCT service utilization
19. Ogilvie GS, Mitchell S, Sekikubo M, Biryabarema C, Byamugisha J, Jeronimo in Western Kenya. J AIDS Clin Res. 2015;6.
J, et al. Results of a community-based cervical cancer screening pilot project 41. Tung W-C, Nguyen DHT, Tran D. Applying the transtheoretical model
using human papillomavirus self-sampling in Kampala, Uganda. Int J to cervical cancer screening in Vietnamese-American women. Int Nurs
Gynaecol Obstet. 2013;122:118–23. https://doi.org/10.1016/j.ijgo.2013.03.019. Rev. 2008;55:73–80.
20. Rosser JI, Hamisi S, Njoroge B, Huchko MJ. Barriers to cervical cancer 42. Daley E, Alio A, Anstey EH, Chandler R, Dyer K, Helmy H. Examining
screening in rural Kenya: perspectives from a provider survey. J Community barriers to cervical cancer screening and treatment in Florida through
Health. 2015;40:756–61. a socio-ecological lens. J Community Health. 2011;36:121–31.
21. Cane J, O’Connor D, Michie S. Validation of the theoretical domains 43. Kivuti-Bitok LW, Pokhariyal GP, Abdul R, McDonnell G. An exploration
framework for use in behaviour change and implementation research. of opportunities and challenges facing cervical cancer managers in
Implement Sci. 2012;7:37. Kenya. BMC Research Notes. 2013;6:136.
22. Michie S, van Stralen MM, West R. The behaviour change wheel: a new 44. Hill D, Gardner G, Rassaby J. Factors predisposing women to take precautions
method for characterising and designing behaviour change interventions. against breast and cervix Cancer. J Appl Soc Psychol. 1985;15:59–79.
Implement Sci. 2011;6:42. 45. Mutyaba T, Mmiro FA, Weiderpass E. Knowledge, attitudes and
23. Huchko MJ, Kahn JG, Smith JS, Hiatt RA, Cohen CR, Bukusi E. Study protocol practices on cervical cancer screening among the medical workers of
for a cluster-randomized trial to compare human papillomavirus based Mulago hospital, Uganda. BMC Med Educ. 2006;6:13.
cervical cancer screening in community-health campaigns versus health 46. Morema EN, Atieli HE, Onyango RO, Omondi JH, Ouma C. Determinants
facilities in western Kenya. BMC Cancer. 2017;17:826. of cervical screening services uptake among 18-49 year old women
24. National AIDS and STI Control Programme (NASCOP) K. Kenya AIDS seeking services at the Jaramogi Oginga Odinga teaching and referral
Indicator Survey 2012: Final Report. 2014. hospital, Kisumu, Kenya. BMC Health Serv Res. 2014;14:335.
25. Maina WK, Kim AA, Rutherford GW, Harper M, K’Oyugi BO, Sharif S, et al. 47. McMullin JM, De Alba I, Chávez LR, Hubbell FA. Influence of beliefs
Kenya AIDS indicator surveys 2007 and 2012: Implications for public health about cervical cancer etiology on pap smear use among Latina
policies for HIV prevention and treatment. Journal Acquired Immune immigrants.
Deficiency Syndromes (1999). 2014;66(Suppl1):S130. https://doi.org/10.1097/ Ethn Health. 2005;10:3–18.
QAI.0000000000000123. 48. Breitkopf CR, Pearson HC, Breitkopf DM. Poor knowledge regarding the pap
26. Huchko MJ, Ibrahim S, Blat C, Cohen CR, Smith JS, Hiatt RA, et al. Cervical test among low-income women undergoing routine screening.
cancer screening through human papillomavirus testing in community Perspectives on sexual and reproductive health, vol. 37; 2005. p. 78–84.
health campaigns versus health facilities in rural western Kenya. Int J 49. Jirojwong S, Thassri J, Skolnik M. Perception of illness and the use of health
Gynaecol Obstet. 2018;141(1):63–9. care givers among cervical cancer patients at Songkla Nagarind hospital. A
27. Boddy CR. Sample size for qualitative research. Qualitative Market Res. 2016; study in southern Thailand. Cancer Nurs. 1994;17:395–402 http://www.ncbi.
19(4):426–32. nlm.nih.gov/pubmed/7954387.
Oketch et al. BMC Women's Health (2019) 19:75 Page 10 of 10

50. Maaita M, Barakat M. Jordanian women’s attitudes towards cervical

screening and cervical cancer. J Obstet Gynaecol. 2002;22:421–2.
51. Rosser JI, Njoroge B, Huchko MJ. Changing knowledge, attitudes, and
behaviors regarding cervical cancer screening: the effects of an educational
intervention in rural Kenya. Patient Educ Couns. 2015;98:884–9.
52. Li M, Nyabigambo A, Navvuga P, Nuwamanya E, Nuwasiima A, Kaganda P,
et al. Acceptability of cervical cancer screening using visual inspection
among women attending a childhood immunization clinic in Uganda.
Papillomavirus Res. 2017;4:17–21.