Available via license: CC BY 4.0
Content may be subject to copyright.
Page 1/20
Factors inuencing cervical cancer re-screening in
sub-Saharan Africa: a cohort study
Sophie Evina Bolo ( Sophie.Evina@etu.unige.ch )
University of Geneva
Bruno Kenfack
Annex Regional Hospital of Dschang
Ania Wisniak
University Hospital of Geneva
Beat Stoll
University of Geneva
Alida Moukam
University of Geneva
Pierre Vassilakos
Geneva Foundation for Medical Education and Research
Gilles Tankeu
Global Research Agency
Virginie Yakam
Annex Regional Hospital of Dschang
Patrick Petignat
University Hospital of Geneva
Jessica Sormani
University Hospital of Geneva
Research Article
Keywords: screening, Human Papilloma Virus, cervical cancer, barriers, Sub-Saharan Africa
Posted Date: June 16th, 2023
DOI: https://doi.org/10.21203/rs.3.rs-3039725/v1
License: This work is licensed under a Creative Commons Attribution 4.0 International License.
Read Full License
Page 2/20
Abstract
Background
- Screening participation at recommended intervals is a crucial component of cervical cancer prevention
effectiveness. However, little is known regarding the rate of re-screening in a Sub-Saharan context. Our
aim was to estimate the re-screening rate of women in Cameroon after an initial Human Papilloma Virus -
based screening and to identify factors that inuence adherence.
Methods
- A cohort study was conducted in the Annex Regional Hospital of Dschang, where a primary screening
unit had been implemented in 2015. Participants enrolled in the present study were women who had been
screened more than 5 years before the date of inclusion and, for whom a re-screening test for cervical
cancer was due. Women who initially tested positive for human papilloma virus (n = 132) and, a random
sample of women who tested negative for human papilloma virus (n = 220) were enrolled in the present
study. Participants were invited to participate in a telephone survey conducted between October 2021 and
March 2022. The survey assessed participation to re-screening or not and reasons for participation or
non-participation. Sociodemographic factors were collected, and associations were evaluated using chi-
squared tests and logistic regression.
Results
- A total of 352 participants aged under 50 years (mean age 37.4 years) were contacted, and 203 (58.0%)
complete the survey. The proportion of women who complied with the screening recommendation was
34.0% (95% CI 27.5% − 40.5%). Age, marital status, education level, type of employment, and place of
residence were not associated with the rate of re-screening. Main reported barriers to re-screening were
lack of information (39.0%), forgetfulness (39.0%), and impression of being in good health (30.0%).
Women who remembered the recommended screening interval were 2 to 3 times more likely to undergo
re-screening (aOR (adjusted odds ratio) = 2.3 [1.2–4.4], p = 0.013). Human papilloma virus- positive status
at the initial screening was also associated with the re-screening((aOR) (95% CI): 3.4 (1.8–6.5).
Conclusion
- Following an initial Human Papilloma Virus-based screening campaign in the West Region of Cameroon,
one third of women adhered to re-screening within the recommended timeframe. Existing screening
strategies would benet from developing better information approaches to reinforce the importance of
repeated cervical cancer screening.
Page 3/20
Background
Cervical cancer is the fourth most common cancer among women worldwide, with over 600,000 new
cases in 2020 [1]. Nearly 90.0% of cervical cancer deaths occur in low-income countries, and the mortality
rate is 18 times higher in low- and middle-income countries than in high-income countries [2, 3]. It is the
leading cause of cancer death- related among women in sub-Saharan Africa, largely due to the lack of
screening [2, 3, 4]. In Cameroon, it is the second most common cancer among women, after breast cancer
[5, 6]. However, regular screening could reduce the risk of cervical cancer by 70.0% [7]. According to the
World Health Organization's (WHO) global strategy for the elimination of cervical cancer, 70.0% of the
target population should undergo screening using a high-performance test such as a Human
Papillomavirus (HPV) test [4, 8]. This remains a challenge in low-income countries that face many
obstacles that may hinder women's access to cervical cancer screening services. Screening and treatment
failures are related to diculties such as lack of awareness among the target population, nancial
diculties, and lack of adequate specialized health infrastructures [9, 10]. Long distances to travel to the
few health facilities that offer screening, prohibitive transportation costs, negative attitudes towards
patients, long waiting times, and lack of male support have been identied as major obstacles to
accessing existing screening services [11–16].
For HPV-based screening, the WHO recommends regular screening at ve-year intervals [8]. Adherence to
regular screening is necessary for a program to be effective and should be monitored through
longitudinal observation of screening participation. Only few studies have been conducted in low-
resource settings and available data evaluating one-year follow-up after HPV + testing support a low rate
of adherence to cervical cancer re-screening (26.0%) for recommended screening [17].
In Cameroon, only 5.0% of women aged between 30 to 49 years have undergone screening in the past ve
years [18]. In line with national guidelines recommending early and regular screening as well as treatment
of precancerous and cancerous lesions [19], the Annex Regional Hospital of Dschang, Cameroon, in
collaboration with the University Hospitals of Geneva, has established a cervical cancer screening unit
with free clinical services since 2015 [20]. The aim of cervical cancer screening is not only getting women
to initiate screening but also to encourage them to maintain regular use over time. To date, very little is
known about participation rate of re-screening as well as factors that may help or hinder women’s
participation to screening adherence over time. Yet, understanding determinants of re-screening appears
essential for developing interventions to encourage women to be re-screened. The aim of our study was
to determine the proportion of HPV-positive and HPV-negative women who attended cervical cancer re-
screening within the recommended timeframe and factors inuencing adherence and non-adherence to
re-screening.
Methods
Study site
Page 4/20
Our study was conducted in the West Region of Cameroon, in Dschang, a university town located 4 hours
from Douala and 5 hours from Yaoundé. It is a council situated in the Menoua division. Dschang has an
estimated population of around 176,940 inhabitants [21]. This is a follow-up study of a pilot study called
the "3T approach" based on primary screening for HPV, implemented with the support of the Cameroonian
Ministry of Health in 2015.
Study type and design
This retrospective cohort study included women screened as part of the 3T-Approach (test, triage, treat)
cervical cancer screening campaign organized at the Annex Regional Hospital of Dschang in
collaboration with the University Hospitals of Geneva in 2015. Approximately 1012 women aged between
30 to 49 were included if they understood the study procedures, and voluntarily agreed to participate by
signing an informed consent form. Women eligible for this study had to be under 44 years of age at the
time of initial screening. Exclusion criteria were pregnancy, previous total hysterectomy, and inability to
comply with the study protocol. Each included woman was primarily screened by an HPV test [22].
Women who tested negative for HPV received oral information from a qualied healthcare provider and a
document reminding them of their next screening appointment in 5 years. Women who tested positive for
HPV underwent a triage with visual inspection with acetic acid (VIA) and were treated free of charge if
needed. Women having a positive HPV test underwent a follow-up screening test following the same
procedure at 12 months, and, in case of negative results, received oral information from a qualied
healthcare provider reminding them of their next screening appointment in 5 years. Adherence to the 1-
year follow-up was of 80% [23]. For the present study, we considered for enrolment only women for whom
a re-screening test was due and non-adherence was dened as not receiving at least two consecutive
cervical cancer screening tests within a ve-year schedule.
Data collection
Sociodemographic data (age, education level, marital status, number of children, type of employment,
place of residence) of participants were collected from the archives of the 2015 cohort. Re-screening data
were collected over a 6-months period between October 2021 and March 2022. Participants were
contacted by phone and interviews were conducted in French and/or English by a Cameroonian
anthropologist (VY) and a physician (SE) based on a structured questionnaire developed by a team of
Cameroonian and Swiss physicians and anthropologists experienced in cervical cancer screening in
Cameroon. The questionnaires were pre-tested on 10 women and adapted accordingly. The nal
validated questionnaire was oriented along the following axes: (i) update of sociodemographic data and
medical history of participants, as well as cervical cancer screening status, (ii) reasons for participation in
re-screening, if any, (iii) reasons for non-participation in re-screening, (iv) experience of rst screening and
treatment, (v) support from the community, family or partner to attend screening, (vi) perception of
cervical cancer and screening. Likert scale questions were used for sections (iv) and (v) of the survey.
The participants who were not reachable during the rst call were called back at least two more times at
different times of the day and week. For those who remained unreachable, text messages containing
Page 5/20
information about the purpose of the call were sent. This method allowed us to maximize participation
rate. The data collected during the calls were recorded using a paper form and then entered into an
electronic database for analysis using Secutrial® software. At the end of the study, the accuracy of all
data was veried. Any inconsistencies were claried by recalling the participant.
Sample size
The study population consisted of 1012 women included in the 2015 cohort who were initially screened
and/or treated. Among these, 728 women were eligible for our study, of whom 132 (18.1%) were positive
for HPV. Assuming the proportion of women undergoing a new screening to be 20.0%, the inclusion of
246 women would have been necessary to obtain a precision of (+/- 5%) with a condence level of 95%.
However, considering a response rate to telephone questionnaires of 70.0%, based on our previous
experiences with this study design, a total sample size of approximately 350 women was required. To
achieve this sample size, we included all HPV-positive women (n = 132) and 220 randomly selected HPV-
negative women, for a total sample size of 352 women. Random selection of HPV-negative participants
was done using R statistical software [24].
Statistical analyses
The complete electronic dataset was analysed using SPSS 16 software [25]. Categorical variables were
expressed as proportions, and 95% condence intervals were estimated. Numeric variables were
expressed as means with standard deviations or medians with interquartile ranges, as appropriate.
Proportions between subgroups were compared using the Chi2 test or Fisher's exact test, depending on
the sample size, and means were compared using the t-test or Mann-Whitney test, depending on the
sample distribution. Associations between sociodemographic and clinical characteristics and cervical
cancer re-screening were evaluated by simple and multivariable logistic regression. All p-values less than
0.05 were considered statistically signicant.
Ethical considerations
This study is a continuation of the 3T-Approach 2015–2016 study approved by the Geneva Canton Ethics
Council, Switzerland (CCER, N°2017 − 0110, and ceR-amendment n°3) and the National Ethics Committee
for Human Health Research in Cameroon (N°2018/07/1083/CE/CNERSH/SP). Informed consent was
obtained orally by telephone from each participant before the survey began, and all data collection forms
were anonymized.
Results
Survey prole
A total of 203 female participants under 50 years old, including 88 (43.3%) positive for HPV and 115
(56.6%) negative, completed the questionnaire (participation rate of 58.0%). The average time between
initial screening and inclusion in the study was 6.5 years, with a standard deviation (SD) of 0.1. One
Page 6/20
hundred and forty-nine participants were unable to complete our questionnaire: 27 participants refused to
participate in the study, and 122 could not be reached (Fig.1).
Note
(n), number of patients, HPV: human papillomavirus.
FU: follow up
Sociodemographic characteristics of study participants
The mean age of participants was 37.4 years. Eighty-six percent were married or in a relationship, and
54.5% of participants had more than four children. Regarding education level, 57.6% had completed
secondary school, 21.7% university, 15.3% primary school, 2.9% apprenticeship, and 1.0% had not
completed any formal education. Seventy-ve percent of the participants lived in a semi-urban area. The
most common type of employment or profession was salaried (50.4%); 30.7% were self-employed, 15.8%
were housewives, and 2.9% were farmers ( Table1).
Clinical characteristics
Ninety-eight percent of the participants were non-smokers, and 84.7% had no known chronic diseases.
Less than one percent were HIV-positive, 50.7% were HIV-negative, and 48.3% had not been tested for HIV
for more than a year. Almost a third reported having a relative with cancer.
Page 7/20
Table 1
Socio-demographic and clinical characteristics of
participants
n (%)
Socio-demographic characteristics
Age (average) 37.4 (+/-3.9)
Marital status
Single/ Widow/ Widower 16 (7,8)
Divorced/separated 11 (5,4)
Married/coupled 175 (86,2)
I did not mean 1 (0,4)
Level of education
Primary 31 (15,2)
Learning/Secondary School 122 (60,1)
University 45 (22,1)
Not in school / Other 4 (1,9)
No response 1 (0,4)
Area of residence
Rural 19 (9,3)
Semi-urban 153 (75,)
Urban 31 (15,2)
Job/occupation* (if applicable)
Employee 102 (50,2)
Farmer/ Self-employed 60 (29,5)
Housewife/ Other 41 (20,2)
Number of children
≤ 4 92 (45,5)
> 4 110 (54,4)
Smoker* (*)
*:
Data updated during telephone calls in 2022
Page 8/20
n (%)
Socio-demographic characteristics
Age (average) 37.4 (+/-3.9)
Marital status
Yes 4 (1,9)
No 199 (98)
Clinical features* (1)
Chronic illness
Present 31 (15,2)
Not present 172 (84,7)
HPV status
HPV- 115 (56,6)
HPV positive 88 (43,3)
HIV infection
Yes 2 (0,9)
No 103 (50,7)
No screening for > 1 year 98 (48,2)
Parent with cancer
Yes 60 (29,5)
No 139 (68,7)
Prefer not to answer 3 (1,4)
Missing 1 (0,4)
*:
Data updated during telephone calls in 2022
Previous screening and/or treatment experience
Ninety-eight percent of the participants reported being satised with the health care providers at their
initial screening; among these, 97.5% reported being well-received, 81.3% were satised with the
information received, and 70.7% reported feeling treated with respect.
Screening practice
Page 9/20
Of the 203 women who completed the questionnaire, 34.0% had attended re-screening. Of those, 40.6%
did it at the recommended time (after at least 5 years), while 59.4% attended re-screening before the
recommended date. Forty-nine percent of re-screened women reported repeating screening because it was
free; 26.1% because they were advised to do so by their relatives, and 18.8% because they had symptoms
(pelvic pain, bleeding, etc.), 10.0% because it was the recommended date, 4.0% because they had been
recalled, and 14.5% for other reasons (out of concern, during a routine visit, during a health campaign, by
coincidence ).
Among those who attended re-screening, 79.7% had an HPV test, and 72.0% percent were re-screened at
the Dschang district hospital.
Obstacles to re-screening
Sixty-six participants did not undergo re-screening since their participation in the 2015 campaign.
Reported obstacles to rescreening included practical considerations, emotions related to screening,
perception of one’s own health, and other reasons. In terms of practical considerations, 23.0% of
participants stated that they did not repeat screening due to lack of time; 8.0% due to lack of money for
transportation; 14.0% due to lack of available screening facilities; and 12.0% due to the long distance
between their home and the hospital.
Regarding emotional reasons, 24.0% stated they did not repeat screening because they feared being
diagnosed with cervical cancer, 5.0% because they feared the screening procedure would be painful, and
2.0% because they were embarrassed to have their private parts examined. Additionally, 30.0% did not
undergo re-screening because they felt healthy, and 1.0% stated that their religious beliefs prevented them
from being re-screened.
Participants were also asked to report any other reason that had prevented them from undergoing re-
screening. In response to this question, 39.0% of participants said that lack of information was the
problem, and the same proportion stated that they had forgotten that they needed to be screened again.
Twenty-ve per cent of participants mentioned other reasons such as neglect (14.0%), insecurity (2.0%),
COVID-19 (1.0%), and others (8.0%).
For HPV-positive participants specically, the main obstacles to re-screening test were forgetfulness
(49.0%), lack of information (42.0%), anxiety about repeating the test (49.0%), the impression of being
healthy (43.0%), and lack of time (37.0%) ( Fig.2).
*Percentage of participants who answered 'agree' and 'strongly agree' to questions related to barriers to
CC re-screening
Support from partner, family, or community
Seventy-nine percent of participants reported receiving support from their spouse or partner; 69.0% from
their family and 57.0% from the community (Fig.3).
Page 10/20
Beliefs and perceptions of cervical cancer
More than 95.0% of participants believed that cervical cancer was a serious disease; 52.0% believed they
were at high risk of cervical cancer, and about the same proportion (51.0%) believed that screening could
prevent cervical cancer.
Approximately 15.0% of women trusted traditional medicine more than conventional medicine; and 82.0%
reported that cervical cancer should not be diagnosed and treated by traditional medicine (Fig.3).
Regarding knowledge of the recommended frequency of screening, 27.0% of participants stated that a
woman should undergo cervical cancer screening every 5 years, which was the recommended frequency
in our screening program. While 13.0% thought it should be done every 3 years and 28.0% every year,
31.0% said they did not know, and 1.0% believed it to be every 10 years.
Eighty-one percent of participants stated they would feel encouraged to undergo screening if it was
recommended by the government; 78.0% if it was recommended by community outreach workers, and
87.0% if recommended by religious gures.
Regarding the cost of screening, 77.0% of participants stated they could undergo screening if the cost
was between 5,000 and 10,000 FCFA (7.67 and 15.33 Euro), 38.0% if the cost was between 10,000 and
30,000 (15.33 and 46 Euro) and 32.0% between 30,000 and 50,000 FCFA (46 and 76,67 Euro).
Associations between re-screening and participant
characteristics
Associations between re-screening and family and medical history, as well as barriers to screening were
examined. Only HPV status at initial screening and knowledge of recommended screening frequency
were signicantly associated with adherence to re-screening (p = 0.001 and p = 0.03, respectively). After
adjusting for potential confounders, having a positive HPV status was associated with a 3 to 4 times
higher risk of being screened again, compared to non-infected women (aOR = 3.4 [1.8–6.5], p < 0.001).
Furthermore, women who remembered the recommended screening frequency were 2 to 3 times more
likely to undergo new testing than those who did not remember (aOR = 2.3 [1.2–4.4], p = 0.013).
None of the evaluated sociodemographic characteristics were signicantly associated with adherence to
re-screening ( Table2).
Page 11/20
Table 2
Factors associated with re-screening.
Test
repeated Test not
repeated cOR (95%
CI) p aOR
(95%
CI)
p
n (%) n (%)
Total 69 (34.0) 134 (66.0)
Age (Mean (SD))
37.4 (3.7) 37.2 (4.0)
0.625*
[30–35] years 16 (23.2) 41 (30.6) 1
[35–40] years 31 (44.9) 50 (37.3) 1.6 (0.8–
3.3) 0.214
[40–50] years 22 (31.9) 43 (32.1) 1.3 (0.6–
2.94) 0.492
Civil status
Married/coupled 58 (84,1) 117 (87,3) 0.8 (0.3–
1.7) 0,525
Single 11 (15,9) 17 (12,7) 1
Level of education
Primary + others 13 (19,1) 28 (20,9) 1
Secondary school 42 (61,8) 75 (56,0) 1.3 (0.6–
2.6) 0.628
University 13 (19,1) 31 (23,1) 0.9 (0.364–
2.34) 0.829
Area of residence
Rural 7 (10,1) 12 (9,0) 1
Semi-urban 52 (75,4) 101 (75,4) 0.9 (0.3–
2.4) 0.805
Urban 10 (14,5) 21 (15,7) 0.8 (0.2–
2.7) 0.740
Employment/profession
Housewife 16 (23,2) 29 (21,6) 1
Self-employed 18 (26,1) 36 (26,9) 0.9 (0.4–
2.1) 0.86
Employee 35 (50,7) 69 (51,5) 0.9 (0.4–
1.9) 0.75
Page 12/20
Test
repeated Test not
repeated cOR (95%
CI) p aOR
(95%
CI)
p
n (%) n (%)
Total 69 (34.0) 134 (66.0)
Chronic illness
No 59 (85,5) 113 (84,3) 1
Yes 10 (14,5) 21 (15,7) 0.9 (0.4–
2.1) 0.825
HPV status
HPV - 28 (40,6) 87 (64,9) 1 1
HPV + 41 (59,4) 47 (35,1) 2.7 (1.5–
4.9) 0.001 3,4 (1,8
− 6,5) <
0,001
Parent with cancer
No 45 (65,2) 94 (70,7) 1
Yes 24 (34,8) 39 (29,3) 1.3 (0.7–
2.4) 0.428
Frequency of screening
Knows 33 (47,8) 48 (35,8) 1.6 (0.9–
3.0) 0,108 2,3
(1,2–
4,4)
0,013
I don't know. 36 (52,2) 86 (64,2) 1 1
Partner support
Present 52 (75,4) 108 (80,6) 0.7 (0.4–
1.5) 0,391
Absent 17 (24,6) 26 (19,4) 1
Discussion
Among our cohort of women having undergone initial cervical cancer screening more than 5 years ago,
only one third (34.0%) of participants had attended re-screening at the time of inclusion in the follow-up
study. Although participants had been informed to repeat a screening test ve years later, our results
support that we have not achieved optimal levels of adherence to cervical cancer re-screening. This
nding is surprising in the context of a free of charge screening program and in a previously adherent
population [23]. To the best of our knowledge, no other studies have investigated re-screening rates
Page 13/20
following a negative cervical cancer screening test in low- and middle-income countries. However, in a
low-income population in Argentina, adherence of HPV-positive/cytology-negative women to follow-up
testing at 12–18 months was 26.0% [17]. Low re-screening rates could limit the long-term impact of
cervical cancer screening programs conducted in low-resource contexts (the target set by the WHO being
70.0% population coverage [4, 8]).
Having a previous positive HPV test was associated with adherence to re-screening (aOR:3.4 (1.8–6.5).
This may reect that women having a positive screening test may have a higher level of familiarity and
commitment to the cervical cancer screening process, as they previously had more procedures and
appointments than those with a negative HPV test. Several beliefs and perceptions of cervical cancer
were identied as potential reasons for adherence or lack thereof. More than half of the participants
believed they were at high risk for cervical cancer, and the same proportion believed in the preventive
nature of screening. It might be suggested that knowledge of the effectiveness of screening and
awareness of the risk of cervical cancer itself would increase women's willingness to be rescreened.
Regarding the obstacles to re-screening, overall, our study showed that the main reasons were lack of
information, forgetfulness, and a feeling of good health. Our study further showed that women who knew
the frequency of screening were 2 to 3 times more likely to undergo re-screening within the recommended
timeframe. Lack of information related to CC has also been highlighted in other studies conducted in
similar contexts [11, 26–29].
It would therefore be imperative for the Ministry of Health and screening programs to place special
emphasis on communication and dissemination of clear and appropriate information on best screening
practices, to develop better tailored information campaigns in specic settings to reach the target
population, both in public places (markets, streets, schools, universities, women's associations, etc.). And,
in hospitals, in departments such as gynaecology/obstetrics and paediatric vaccination, where cervical
cancer screening could be an additional service offered to women when they come for other care. In
addition, prescribing screening by health personnel is a factor that encourages women to undergo
screening, as shown by studies conducted in similar contexts [27, 30]. It would therefore be relevant to
involve health personnel in promotion of cervical cancer screening among women attending health care
facilities for other reasons. Communication and information strategies through contextually appropriate
reminders as SMS recall systems, such as the "call and recall" system that proved successful in the
United Kingdom in 1988, leading to a signicant drop in CC cases [31], could also be implemented to
increase screening rates according to recommendations. Among HPV-positive participants, anxiety
related to the idea of having cancer outweighed all other reasons, several other studies have found that
HPV + women with abnormal or normal cytology had higher short-term anxiety than those with normal
results [32, 33]. It would be very important to train caregivers to reassure HPV + patients.
More than half of our study population (57.0%) reported having community support when it came to
undergoing cervical cancer screening. This is an encouraging nding which is worthy of further
exploration for promotional activities in similar settings, as community support has been shown to act as
a facilitating factor for screening [30].
Page 14/20
No association between sociodemographic factors and CC rescreening were observed in our study
population. Other studies in Africa have shown that unemployed women were less likely to be screened
than employed women [34, 35]. This could be apprehended by the free screening during our study,
removing nancial barriers for our participants.
Cultural barriers did not seem to prevail in our population, given the high level of condence in
conventional medicine (82.0% reported that cervical cancer should not be diagnosed and managed by
traditional medicine) associated with a low percentage of participants (1.0%) who perceived their
religious beliefs as an obstacle to screening this high percentage is probably biased by the fact that this
is a population that has already been screened once. A large majority (86.0%) stated that they would
undergo screening if recommended by the government. Furthermore, most women (76.0%) stated that
they could afford screening for a fee ranging from 5,000 to 10,000 CFA francs (approximately 8–16
Euros). These ndings should be considered in the implementation of a national strategy for cervical
cancer prevention in Cameroon, with an emphasis on universal health coverage given the risk of
inequitable access to screening, as our study shows that nearly a quarter of women would not have
access to screening if it were to be paid for.
Limitations and strengths
To the best of our knowledge, we report for the rst time the re-screening rate in an HPV-based cervical
cancer in Sub-Saharan Africa. However, our study should be interpreted with some caveats. First, it is a
selected cohort of women who mainly lived in a semi-urban area and went to the local district hospital,
where screening and treatment for pre-cancerous cervical lesions were free, and transport was
reimbursed. These specics may have obscured nancial barriers to re-screening that may be prevalent in
other contexts. Second, adherence to re-screening may have been overestimated due to a participation
bias, considering the relatively low participation rate. In fact, the high number of unreachable women
resulting in a smaller sample size.
Conclusion
Only one-third of participants were re-screened within the recommended interval, and main reported
barriers to re-screening were lack of information, forgetfulness, and impression of being in good health.
Yet early and timely detection of precancerous lesions is crucial to prevent long-term morbidity and
mortality due to cervical cancer. Existing screening strategies would benet from developing new
approaches to inform women about the importance of regular cervical cancer screening to realize the full
benet of screening. Further studies should be conducted to assess strategies aiming to improve
adherence to re-screening.
Abbreviations
CC: cervical cancer
Page 15/20
ARHD: Annex Regional Hospital of Dschang
HPV: Human Papilloma Virus
HPV+: Human Papilloma Virus Positive
HPV-: Human Papilloma Virus Negative
VIA: Visual Inspection with Acetic Acid
WHO: World Health Organisation
Declarations
Statements
Ethical approval and consent to participate.
All methods were performed in accordance with the guidelines and regulations of the Declaration of
Helsinki. This study is a continuation of the 3T 2015-2016 study approved by the Geneva Canton Ethics
Council, Switzerland (CCER, N°2017-0110, and ceR-amendment n°3) and the National Ethics Committee
for Human Health Research in Cameroon (N°2018/07/1083/CE/CNERSH/SP).
Informed consent was obtained orally by telephone from each participant before the survey began, and
all data collection forms were anonymized.
Consent to publish –
Not applicable.
Availability of data and materials
The datasets used and/or analysed during this study are available from the corresponding author upon
reasonable request
.
Conict of Interest
The authors declare that they have no competing interests.
Funding
The study was funded by the Humanitarian Affairs Commission of the Geneva University Hospitals. The
funding sponsors played no role in the design and conduct of the study; collection, management,
analysis, and interpretation of the data; preparation, review, or approval of the manuscript; and decision to
submit the manuscript for publication.
Author Contributions
Page 16/20
SE: Writing- Original draft preparation; AW, PVand, PP: Conceptualization, Methodology; GT and SE: data
management and analysis; VY and SE: Investigation; BS and BK: Supervision; SE and, AW: Reviewing and
Editing; JS and AM: Project administration.
Acknowledgements
We thank the research team at the district hospital of Dschang-Cameroon and the University Hospitals of
Geneva-Switzerland, without whom this work would not have been possible.
References
1. Cancer today [Internet]. [cited 11 July 2022]. Available from: http://gco.iarc.fr/today/home.
2. Small W Jr, Bacon MA, Bajaj A, Chuang LT, Fisher BJ, Harkenrider MM et al. Cervical cancer: a global
health crisis. Cancer [Internet]. 2017 [cited October 7, 2021];123(13):2404-12. Available from:
https://onlinelibrary.wiley.com/doi/abs/10.1002/cncr.30667.
3. Arbyn M, Weiderpass E, Bruni L, de Sanjosé S, Saraiya M, Ferlay J, et al. 2018 estimates of cervical
cancer incidence and mortality: a global analysis. Lancet Glob Health. 2020 Feb;8(2):E191–203.
4. Levy J, Preux M, Kenfack B, Sormani J, Catarino R, Tincho E et al. Implementing the 3T-approach for
cervical cancer screening in Cameroon: Preliminary results on program performance. Cancer Med 5
August 2020;9.
5. Marie Tebeu P, Antaon JSS, Adjeba M, Pikop F, Fouogue JT, Ndom P. Knowledge, attitudes and
practices of health professionals on cervical cancer in Cameroon. Public Health. 2020;Vol.
32(5):489–496. Accessed September 27, 2021. https://www.cairn.info/revue-sante-publique-2020-5-
page-489.htm.
. IARC. (2020). Cameroon. Retrieved from The Global Cancer Observatory:
https://gco.iarc.fr/today/data/factsheets/populations/120-cameroonfact-sheets.pdf.
7. 7.Ronco G, Dillner J, Elfström KM, Tunesi S, Snijders PJ, Arbyn M et al. Ecacy of HPV-based
screening for prevention of invasive cervical cancer: follow-up of four European randomised
controlled trials. Lancet [Internet]. 2014;383(9916):524 – 32. Available at:
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5410654/.
. Human papillomavirus (HPV) and cervical cancer. Accessed on 12. October 2021.
https://www.who.int/news-room/fact-sheets/detail/human-papillomavirus-(HPV)-and-cervical-
cancer.
9. A comprehensive approach to cervical cancer prevention. and control: towards better health for
women and girls [Internet]. [cited 11 July 2022]. Available from: https://www.who.int/fr/publications-
detail/9789241505147.
10. World Health Organization. Cervical cancer control: essential practice guidelines [Internet]. World
Health Organization. ; 2017 [cited 2022 July 11]. 446 p. Available from:
https://apps.who.int/iris/handle/10665/254713.
Page 17/20
11. Chapola J, Lee F, Bula A, Mapanje C, Phiri B, Kamtuwange N et al. Barriers to follow-up after an
abnormal cervical cancer screening result and the role of male partners: a qualitative study. BMJ
Open. 2021.
12. Niyonsenga G, Gishoma D, Sego R, Goretti Uwayezu M, Nikuze B, Fitch M et al. Knowledge, utilization
and barriers to cervical cancer screening in district hospitals in Kigali, Rwanda. Canadian Oncology
Nursing Journal [Internet]. 2021 Jul 1 [cited 2022 Jul 11];31(3):275 – 84. Available from:
http://canadianoncologynursingjournal.com/index.php/conj/article/view/1184.
13. Datchoua Moukam AM, Embolo Owono MS, Kenfack B, Vassilakos P, Petignat P, Sormani J, et al.
Cervical cancer screening: awareness is not enough. Understanding barriers to screening among
women in western Cameroon - a qualitative study using focus groups. Reprod Health 9 July.
2021;18(1):147.
14. Bateman LB, Blakemore S, Koneru A, Mtesigwa T, McCree R, Lisovicz NF et al. Barriers and
facilitators to cervical cancer screening, diagnosis, follow-up care, and treatment: perspectives of
human immunodeciency virus-positive women and health professionals in Tanzania. The
Oncologist [Internet]. 2019 [cited July 11, 2022];24(1):69–75. Available from:
https://onlinelibrary.wiley.com/doi/abs/10.1634/theoncologist.2017-0444.
15. Roux AN, Kenfack B, Ndjalla A, Sormani J, Wisniak A, Tatrai K et al. Barriers to cervical cancer
prevention in rural Cameroon: a qualitative study on healthcare providers' perspective. BMJ Open
[Internet]. 2021 Jun 1 [cited 2022 Jul 11];11(6):e043637. Available from:
https://bmjopen.bmj.com/content/11/6/e043637.
1. Getachew S, Getachew E, Gizaw M, Ayele W, Addissie A, Kantelhardt EJ. Knowledge of and barriers to
cervical cancer screening among women in Addis Ababa, Ethiopia. PLoS ONE. 2019;14(5):e0216522.
17. Gago J, Paolino M, Arrossi S. Factors associated with low adherence to cervical cancer follow-up
retest among HPV+/ cytology negative women: a study in programmatic context in a low-income
population in Argentina. BMC Cancer [Internet]. 2019 Apr 23 [cited 2023 Apr 29];19(1):367. Available
from: https://doi.org/10.1186/s12885-019-5583-7.
1. Cervical cancer Cameroon. 2021 country prole [Internet]. [cited 2023 May 12]. Available from:
https://www.who.int/publications/m/item/cervical-cancer-cmr-country-prole-2021.
19. Cameroon Ministry of Public Health. National guidelines for the prevention and management of
cervical cancer. Yaoundé: Cameroon Ministry of Public Health; 2015.
20. Vassilakos P, Tebeu P, Halle-Ekane GE, Sando Z, Kenfack B, Baumann F, et al. Twenty years of
cervical cancer control in sub-Saharan Africa - Medical collaboration between Geneva and Yaoundé.
Swiss Medical Journal; 2019.
21. National Institute of Statistics (Cameroon). Annuaire statistique du Cameroun, 2021 edition.
Yaoundé: National Institute of Statistics; 2021.
22. Kunckler M, Schumacher F, Kenfack B, Catarino R, Viviano M, Tincho E, et al. Cervical cancer
screening in a low-resource setting: a pilot study of an HPV-based screening and treatment
approach. Cancer Med. 2017 Jul;6(7):1752–61.
Page 18/20
23. Viviano M, Tran PL, Kenfack B, Catarino R, Akaaboune M, Temogne L et al. Self- versus physician-
collected samples for the follow-up of human papillomavirus-positive women in sub-Saharan Africa.
International Journal of Women’s Health [Internet]. 2018 Dec 31 [cited 2023 Apr 29];10:187–94.
Available from: https://www.tandfonline.com/doi/abs/10.2147/IJWH.S154212.
24. R Core Team. (2020). R: A language and environment for statistical computing. R Foundation for
Statistical Computing, Vienna, Austria. URL: https://www.R-project.org/.
25. IBM Corp. Released 2016. IBM SPSS Statistics for Windows, Version 24.0. Armonk, NY: IBM Corp.
2. Maree JE, Moitse KA. Exploration of knowledge of cervical cancer and cervical cancer screening
amongst HIV-positive women. Curationis [Internet]. 2014 Feb 1 [cited 2022 Jul 11];37(1):e1-7.
Available from: http://www.curationis.org.za/index.php/curationis/article/view/1209.
27. Donatus L, Nina FK, Sama D, Nkfusai CN, Bede F, Shirinde J et al. Assessing the uptake of cervical
cancer screening among women aged 25–65 years in Kumbo West Health District, Cameroon. Pan
African Medical Journal [Internet]. 2019 [cited 2022 Jul 11]; Available from:
https://www.semanticscholar.org/paper/Assessing-the-uptake-of-cervical-cancer-screening-Donatus-
Nina/a88fe2ec573ee1dba54d7ae53fac4f5610a705ca.
2. Halle-Ekane G, Nembulefack D, Orock GE, Fon PN, Tazinya A, Tebeu P. Knowledge of Cervical Cancer
and Its Risk Factors, Attitudes and Practices towards Pap Smear Screening among Students in the
University of Buea, Cameroon. J Cancer Tumor Int. 2018.
29. Megersa BS, Bussmann H, Bärnighausen T, Muche AA, Alemu K, Deckert A. Community cervical
cancer screening: Barriers to successful home-based HPV self-sampling in Dabat district, North
Gondar, Ethiopia. A qualitative study. PLoS ONE. 2020;15(12):e0243036.
30. Darj E, Chalise P, Shakya S. Barriers and facilitators to cervical cancer screening in Nepal: a
qualitative study. Sex Reprod Healthc. 2019;20:20–6.
31. Quinn M, Babb P, Jones J, Allen E. PapersEffect of screening on incidence of and mortality from
cancer of cervix in England: evaluation based on routinely collected statistics. BMJ [Internet]. 1999
Apr 3 [cited 2023 May 12];318(7188):904. Available from:
https://www.bmj.com/content/318/7188/904.
32. Dodd RH, Mac O, Brotherton JML, Cvejic E, McCaffery KJ. Levels of anxiety and distress following
receipt of positive screening tests in Australia’s HPV-based cervical screening programme: a cross-
sectional survey. Sex Transm Infect. 2020 May;96(3):166–72.
33. McBride E, Tatar O, Rosberger Z, Rockliffe L, Marlow LAV, Moss-Morris R, et al. Emotional response to
testing positive for human papillomavirus at cervical cancer screening: a mixed method systematic
review with meta-analysis. Health Psychol Rev. 2021 Sep;15(3):395–429.
34. Ampofo AG, Adumatta AD, Owusu E, Awuviry-Newton K. A cross-sectional study of barriers to cervical
cancer screening uptake in Ghana: An application of the health belief model. PLoS ONE [Internet].
2020 Jan 1 [cited 2022 Jul 11];15(4):e0231459. Available from:
https://doi.org/10.1371/journal.pone.0231459.
Page 19/20
35. Gatumo M, Gacheri S, Sayed AR, Scheibe A. Women's knowledge and attitudes related to cervical
cancer and cervical cancer screening in Isiolo and Tharaka Nithi counties, Kenya: a cross-sectional
study. BMC Cancer. 2018 Jul;18(1):745.
Figures
Figure 1
Page 20/20
Participants ow chart.
Figure 2
Barriers to the cervical cancer re-screening visit (HPV + and – stratied)
Figure 3
Beliefs and perceptions of cervical cancer screening