Accepted Manuscript

Women's knowledge of cervical cancer and uptake of Pap smear testing and the
factors influencing it in a Nigerian tertiary hospital

Adeyemi A. Okunowo, Ebunoluwa S. Daramola, Adaiah P. Soibi-Harry, Ezenwankwo

Francis, Jubril O. Kuku, Kehinde S. Okunade, Rose I. Anorlu

PII: S2311-3006(17)30149-0
DOI: 10.1016/j.jcrpr.2018.02.001
Reference: JCRPR 85

To appear in: Journal of Cancer Research and Practice

Received Date: 26 November 2017

Revised Date: 10 February 2018
Accepted Date: 21 February 2018

Please cite this article as: Okunowo AA, Daramola ES, Soibi-Harry AP, Francis E, Kuku JO, Okunade
KS, Anorlu RI, Women's knowledge of cervical cancer and uptake of Pap smear testing and the factors
influencing it in a Nigerian tertiary hospital, Journal of Cancer Research and Practice (2018), doi:
10.1016/j.jcrpr.2018.02.001.

This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to
our customers we are providing this early version of the manuscript. The manuscript will undergo
copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please
note that during the production process errors may be discovered which could affect the content, and all
legal disclaimers that apply to the journal pertain.
 ACCEPTED MANUSCRIPT

Manuscript type:

Original research

PT
Title of the article:

RI
Women’s knowledge of cervical cancer and uptake of Pap smear testing and the factors

SC
influencing it in a Nigerian Tertiary Hospital.

U
AN
List of Authors:
M

1. OKUNOWO Adeyemi A.1

2. DARAMOLA Ebunoluwa S.2

D

3. SOIBI-HARRY Adaiah P. 2
TE

4. EZENWANKWO Francis2

5. KUKU Jubril O.2

EP

6. OKUNADE Kehinde S.1

C

7. ANORLU Rose I.1

AC

Department and institutional affiliation of all authors:

1
Department of Obstetrics & Gynecology, College of Medicine, University of Lagos /

Lagos University Teaching Hospital, PMB 12003, Lagos, Nigeria

1
 ACCEPTED MANUSCRIPT

2
Department of Obstetrics & Gynecology, Lagos University Teaching Hospital, PMB

12003, Lagos, Nigeria

PT
Corresponding Author:

RI
Name : OKUNOWO Adeyemi A.

Address: Department of Obstetrics & Gynecology, College of Medicine, University of

SC
Lagos / Lagos University Teaching Hospital (LUTH), PMB 12003, Lagos, Nigeria.

Phone number: +234 803 561 1000

U
AN
E-mail address: yemiokunowo@gmail.com
M

Acknowledgement:
D

The authors would like to thank all those that contributed to the study
TE
EP

Running title:
C

Knowledge of cervical cancer and uptake of Pap smear testing

AC

2
 ACCEPTED MANUSCRIPT

PT
RI
U SC
AN
M
D
TE
EP
C
AC

3
 ACCEPTED MANUSCRIPT

ABSTRACT

Background:

Both the incidence and burden of cervical cancer have been drastically reduced in the developed

PT
world, due to the practice of regular cervical cancer screening with Pap smear. Unfortunately, the

disease is still the most common gynaecological cancer, and the second leading cause of female

RI
cancer mortality in Nigeria, with up to 80% of women with cervical cancer ultimately

SC
succumbing to the disease.

Objective:

U
AN
We examined the knowledge of cervical cancer and uptake of Pap smear screening among

women attending obstetric and gynaecological outpatient clinics at the Lagos University
M

Teaching Hospital in Lagos, Nigeria, and the factors that affect it.
D

Methods:
TE

The study was a descriptive cross-sectional study derived from a cohort of 225 pregnant and

non-pregnant women using a structured questionnaire to assess their knowledge of cervical

EP

cancer, uptake of Pap smear and factors that affect them. Data was analyzed using the Statistical

Package for Social Sciences (SPSS) version 20.0.

C
AC

Results:

The knowledge of women in this study regarding symptoms and risk factors of cervical cancer

was very poor (40.0% and 15.6%, respectively), despite a 78.5% awareness rate. Likewise, the

uptake of Pap smear was very low (22.9%), with an awareness rate of 55.1%. The major reasons

for having a Pap smear were recommendation from doctors/nurses (89.4%) and fear of
 ACCEPTED MANUSCRIPT

developing cervical cancer (23.4%), while the reasons for not having a Pap smear were lack of

awareness (53.8%) and non-recommendation of the test by doctors/nurses (31.0%). Prior

counselling by doctors/nurses and knowing someone with cervical cancer significantly increased

the knowledge of cervical cancer and the uptake of Pap smear, while high level of education was

PT
significantly associated only with increased knowledge of cervical cancer and awareness of Pap

RI
smear, but not its uptake.

SC
Conclusion:

Our study indicates that when healthcare providers supply regular health education and

U
recommendation of Pap smear test, this will increase the knowledge of cervical cancer and its
AN
screening, and reduce the burden of the disease.
M

KEY WORDS
D
TE

Knowledge of cervical cancer; Risk factors for cervical cancer; Symptoms of cervical cancer;

Uptake of Pap smear; Nigeria

C EP
AC
 ACCEPTED MANUSCRIPT

1. INTRODUCTION

Cervical cancer is a highly preventable and curable disease when detected and treated early in its

precancerous stage. Medical science has provided effective evidence-based interventions for the

PT
prevention, early detection and treatment of the disease. As a result, no woman should be in the

position to suffer or die from cervical cancer and its complications. Unfortunately, this is not the

RI
reality. Cervical cancer has remained a common disease as noted by the larger worldwide cancer

SC
statistics. In 2012, cervical cancer was the 4th most common cancer seen among women

worldwide. While it was the 2nd commonest female cancer in developing countries after breast

U
cancer, cervical cancer was uncommon in developed nations, where it was not even rated among
AN
the top 10 female cancers.1

Developing nations contribute the largest portion of the global burden of cervical cancer. Among
M

the 527,624 new cases of cervical cancer diagnosed worldwide in 2012, more than 80%
D

(444,546) of cases were diagnosed in less developed nations, with 14,089 new cases reported in
TE

Nigeria. Approximately 90% of the 265,672 cervical cancer deaths worldwide occurred in less

developed countries, with 16,546 and 8240 occurring in the West Africa region and Nigeria,
EP

respectively.1,2 It is the 2nd leading cause of female cancer mortality in Nigeria,1,2 .with up to

80% of women dying of the disease.3 Together with breast cancer, they accounted for more than
C

50% of all female cancers and about two-thirds of cancer deaths in women4,5
AC

Regular cervical cancer screening with Papanicolaou (Pap) smear testing has remained an

effective public health intervention in the prevention and subsequent reduction of the incidence,

morbidity and mortality of cervical cancer disease.6-8 Though the modalities of screening could

either be organized mass screening program or opportunistic screening, it has been demonstrated
 ACCEPTED MANUSCRIPT

that only organized mass screening of the populace that targets all women at risk is known to be

effective.9 Over the past 40 years, this population – based method of screening has drastically

reduced the incidence and mortality of cervical cancer by as much as 65% in the developed

world.10,11 Unfortunately, opportunistic screening is what is commonly practiced in the less

PT
developed nations such as Nigeria, which is due to the ineffectiveness of its health system.12-14

RI
This method is less effective because it principally targets a small proportion of women who

have the opportunity to come in contact with health care providers either in a health facility or in

SC
the community. 9,12,15,16 Worse still, this opportunistic screening is not widely available; where

they are available, the service is grossly underutilized.13,14 Some studies have reported very low

U
levels of uptake of Pap smear even in areas where the screening test are available. 8,13,17-19 Studies
AN
have also shown a wide variation between cervical cancer awareness, knowledge of the disease

and uptake of cervical cancer screening such as Pap smear screening test.7,8,20-22 Approximately
M

50-90% of women who develop or die as a result of cervical cancer have never been screened.12
D

Even more troubling is the fact that a significant proportion of these women were not even aware
TE

of the Pap smear screening test.8,22,23

Several factors have been shown to influence the uptake of Pap smear. Young age, high level of
EP

education and knowledge of risk factors have been shown to increase the willingness and uptake
C

of Pap smear test.24 On the other hand, low respondent perception of the risk of developing
AC

cervical cancer, lack of knowledge about symptoms of the disease and the benefits of Pap smear,

and unfamiliarity with the location of its screening sites have been identified to be barriers to the

uptake of Pap smear.25,26 The health care providers also have roles to play in improving the

knowledge of cervical cancer, awareness of Pap smear and its uptake in our environment. It has
 ACCEPTED MANUSCRIPT

been shown that respondents have identified non – recommendation of Pap smear test as a major

reason for not doing the test.27

This study was conducted to assess women’s knowledge of the symptoms and risk factors of

PT
cervical cancer, the extent of their uptake of Pap smear and to determine the factors that

influence it. The outcome of this study will be useful in making recommendations intended to

RI
create an effective cervical cancer hospital screening program, and in Nigeria as a whole.

U SC
AN
M
D
TE
C EP
AC
 ACCEPTED MANUSCRIPT

2.0 MATERIALS AND METHODS

2.1 Study design and study site

The study was an observational descriptive cross-sectional study conducted among women

PT
attending antenatal and gynaecological out-patient clinics at the Lagos University Teaching

Hospital (LUTH), between March 1 and March 30, 2016. LUTH is one of largest federal tertiary

RI
hospitals in Nigeria, with a 761-bed capacity, and is located in Lagos, part of the south-western

SC
portion of Nigeria. It is the main referral hospital for all government and private hospitals in

Lagos state and its environs. Two antenatal and two gynaecological outpatient clinics were

U
selected by ballot method among the four existing antenatal and gynaecological outpatient
AN
clinics, respectively. The antenatal clinics run in the morning between the hours of 8am - 1pm

from Monday to Friday, excluding Wednesday, while the gynaecological out-patient clinics run
M

in the afternoon from 2 – 6 pm on week days, excluding Friday.

D

2.2 Study participants and Sample size determination

TE

All women attending the selected outpatient clinics who provided informed consent and were 18

years of age or older were recruited for the study. Critically ill patients and patients who did not
EP

give informed consent were excluded from the study.

C

The minimum sample size was calculated using the formula n = Z2 p (1-p) / d2 28 with an absolute
AC

error margin of 5% (d = 0.05), type 1 error of 5% (Z = 1.96), and the proportion of women who

were aware of cervical cancer and had done Pap smear (p) of 8.5%.7 The calculated sample size

was 120 and after adjusting for a non – response rate of 20%, the final calculated minimum

sample size was 144.

 ACCEPTED MANUSCRIPT

2.3 Data collection

All consecutive patients attending the selected clinics who met the inclusion criteria were

PT
recruited for the study. The survey tool was a structured questionnaire which was self-

administered to all the participants. Those participants who were unable to read or write had their

RI
questionnaires administered by a trained interviewer. All questionnaires were retrieved

SC
immediately after completion.

The questionnaire was designed to elicit information about the respondents’ socio-demographic

U
characteristics, awareness about cervical cancer, aetiology of cervical cancer, knowledge of
AN
symptoms and risk factors of cervical cancer, and the awareness, knowledge and uptake of Pap
M

smear. Information on the reasons for doing and not doing Pap smear and willingness to do a Pap

smear test were also elicited. History of previous counseling by a doctor/nurse about Pap smear
D

and knowledge of someone with cervical cancer were also elicited to determine its effect on a
TE

respondent’s knowledge of the disease, awareness and uptake of Pap smear. Those socio-

demographic characteristics elicited were age, highest educational status attained, occupation,
EP

marital status, religion and ethnicity. The symptoms of cervical cancer that were assessed in the

study were bleeding after sexual intercourse (post-coital bleeding), abnormal vaginal bleeding
C

(bleeding unrelated to sexual intercourse), offensive vaginal discharge, lower abdominal pain
AC

and weight loss. The risk factors examined in the study included infection with human papilloma

virus, having multiple sexual partners, early age at sexual intercourse, early marriage, early age

at childbirth and having partner who has multiple sexual partners. Other risk factors included
 ACCEPTED MANUSCRIPT

smoking, HIV infection, use of birth control pills, giving birth to several children, reduced body

immunity and having a sexually transmitted infection.

Adopting a similar scoring system used in assessing cervical cancer knowledge,29 each correctly

PT
identified symptom or risk factor was assigned a score of 1, and a score of zero was assigned to

an incorrect or “I don’t know” response. The total attainable score for cervical cancer symptoms

RI
was 5, while the total obtainable score for cervical cancer risk factors was 12. Respondents with

SC
an average score of ≥ 3 were categorized as having good knowledge of cervical cancer

symptoms, while respondents with score < 3 were categorized as having poor knowledge.

U
Similarly, women with an average score of > 6 were categorized as having good knowledge of
AN
cervical cancer risk factors, while women with score ≤ 6 were adjudged to have poor knowledge.

2.4 Data analysis

M

Data was analyzed using the Statistical Package for Social Sciences (SPSS) version 20.0, IBM
D

Corp. Armonk, NY, USA. Variables were expressed using frequency tables. Categorical
TE

variables were compared using the Pearson Chi-square test or Fisher’s exact test as appropriate,

while continuous variables were compared using the Student's t - test. A p value of < 0.05 was
EP

considered to be significant.
C
AC
 ACCEPTED MANUSCRIPT

3.0 RESULTS

Out of 225 questionnaires distributed, 205 (91.1%) were correctly filled and analyzed. Of that

number, 111 respondents (49.3%) were pregnant women, while 104 (50.7%) were non- pregnant

PT
women. There were no significant differences in the socio – demographic characteristics

between the pregnant women and the non – pregnant women (p<0.05). The mean age of the

RI
respondents was 35.9 ± 9.5 years (range 20 – 74 years), while the median parity was 1 (range 0 -

SC
8). A majority of the respondents were married (79.0%), Christians (85.4%) and had a tertiary

level of education (75.6%) (Table 1). Though a majority (78.5%) of the study participants were

U
aware of cervical cancer, only 22.4% (46) of the respondents were aware that human papilloma
AN
virus (HPV) is the implicating agent in the aetiology of cervical cancer. Likewise, only 40.0%

(82) and 15.6% (32) of the respondents had good knowledge of the symptoms and risk factors of
M

cervical cancer, respectively, even though more respondents had better knowledge of symptoms

of cervical cancer than risk factors (Table 2). The most frequently identified symptoms of
D

cervical cancer were abnormal vaginal bleeding (43.4%), post-coital bleeding (39.5%) and lower
TE

abdominal pain (39.0%); however, having multiple sexual partners (37.6%), sexually transmitted

infections (34.6%) and having partner who has multiple sexual partners (34.2%) were the
EP

frequently identified risk factors (Table 3). Overall, 83.9% (172) of the respondents were not
C

aware of the vaccine used for preventing cervical cancer. The most common sources of
AC

knowledge were radio/television (30.4%) and doctors/nurses (24.8%), while the least common

sources of knowledge were religious bodies (2.5%) and friends and relatives (5.6%).

Also, 41.5% (85) of the respondents believed that cervical cancer is a common cancer in women,

but only 16.6% (34) believed that they are at risk of having the disease. Though more than half

of the study participants, 55.1% (113) were aware of Pap smear, less than a third of them, 31.7%
 ACCEPTED MANUSCRIPT

(65) had knowledge of the purpose of Pap smear. Unsurprisingly, less than a quarter of the

respondents, 22.9% (47) had ever had a Pap smear. However, a majority of these smears, 85.1%

(40) were done within the last 3 years.

PT
Tables 4 and 5 showed the reasons respondents gave for doing and not doing Pap smear,

respectively. Recommendation from doctors/nurses (89.4%) and the fear of developing cervical

RI
cancer (23.4%) were the most common reasons respondents gave for doing a Pap smear test. On

SC
the other hand, lack of awareness of Pap smear (53.8%) and non - recommendation of the test by

doctors/nurses (31.0%) were the main reasons for not doing a Pap smear test. However, 67.1%

U
(106) of the respondents who had never done Pap smear were now willing to do the test.
AN
Tertiary level of education was the only socio–demographic characteristic that was significantly

associated with both good knowledge of symptoms and risk factors of cervical cancer among
M

respondents (p = 0.005 and 0.009 respectively). Prior counseling by doctor/ nurse, and knowing
D

someone with cervical cancer was also significantly associated with good knowledge of
TE

symptoms and risk factors of cervical cancer (p = < 0.001, 0.001 and 0.004, 0.001, respectively)

(Table 6).
EP

Though a tertiary level of education was observed to significantly increase the awareness of Pap

smear among the respondents (p = 0.003), it did not have any positive impact on their uptake of
C

Pap smear (p = 0.751). Other socio–demographic factors did not significantly affect the
AC

awareness and uptake of Pap smear (p > 0.05). However, prior counseling by doctor/ nurse and

knowing someone with cervical cancer were observed to be significantly associated with

increased awareness of Pap smear (p < 0.001 and < 0.001, respectively), and uptake of Pap

smear (p = 0.003, 0.002, respectively) (Table 7). There was no association observed between
 ACCEPTED MANUSCRIPT

pregnancy status and respondents’ level of knowledge of the symptoms and risk factors of

cervical cancer (p value > 0.05, respectively). Their level of awareness and uptake of Pap smear

was also not significantly influenced by their pregnancy status (p value > 0.05, respectively).

PT
RI
U SC
AN
M
D
TE
C EP
AC
 ACCEPTED MANUSCRIPT

4.0 DISCUSSION

The level of awareness of cervical cancer was high among women in our study, ultimately

reaching approximately 80%. This was not the case in a similar study conducted in Lagos and at

PT
another tertiary hospital in the same geopolitical zone, where only 37.2%7 and 37.3%22 of the

women were aware of cervical cancer, respectively. Similarly, low levels of awareness were

RI
observed among women in other studies in Nigeria.7,30-33 The high level of awareness in our

SC
study was probably due to the fact that a majority of the study participants were educated, with

75.6% having tertiary education. This could have also partly accounted for why more than half

U
(55.1%) of our study participants were aware of Pap smear, compared to lower levels of
AN
awareness ranging from 4.8 to 19.5% observed in other studies conducted in other regions in the

same geographical zone.22,26,34 A similar low level of Pap smear awareness was observed in
M

Ghana (2.3%)25 and Kenya (32%).35 However, a relatively high level of awareness was observed

in studies among health workers,36,37 which was probably due to the nature of their jobs that
D

affords them better knowledge of Pap smear.

TE

A majority of the respondents in our study had poor knowledge of cervical cancer, with only
EP

40.0% and 15.6% of the respondents having good knowledge of the symptoms and risk factors of

cervical cancer, respectively. Similarly, only 31.7% of the study participants knew what Pap
C

smear is used for compared with awareness rate of 55.1%. This shows that there is a wide gap
AC

between awareness and knowledge, and that awareness does not necessarily translate to

knowledge. More effort needs to be applied to improve the education of women about the

disease condition, its recognition and prevention. This low level of knowledge is also seen in

many studies across different states in Nigeria. More than 95% of women were unable to identify

at least 1 risk factor or symptom of cervical cancer in a study in Ogun state,30 while 85% of
 ACCEPTED MANUSCRIPT

women in the ancient city of Ibadan had very poor knowledge about the disease and its

screening.38 In a neighbouring West African country, Ghana, 93.6% of the women had no

knowledge about the risk factors of cervical cancer.25 This was contrary to findings in developed

country like London, where 76.2% of women were aware of the risk factors of cervical cancer.39

PT
The commonest sources of knowledge about cervical cancer in our study were from

RI
radio/television followed by the doctors/nurses, which were findings similar to those of another

study.7

SC
Less than a quarter of the study participants (22.9%) had ever done a Pap smear. This statistic

U
was not unexpected due to the poor knowledge about the disease among Nigerian women, and
AN
the importance of Pap smear in the prevention of cervical cancer. The uptake of Pap smear and

cervical screening in our environment remains very low, as several studies had reported
M

embarrassingly low uptake levels. In one study, 3.2% of women had done Pap smear within the

last five years,22 while only 8.5% of women who were aware of cervical cancer had done the test
D

in another Nigerian study.7 Similarly, another study showed that only 3.9% of women ever had
TE

cervical screening done.34 Even among female health worker where a high uptake of Pap smear

is expected due to their high level of awareness and knowledge of the disease and its prevention,
EP

the uptake of Pap smear remained very low. This ranged from 0.3 - 23.3% in several studies
C

done in Nigeria8,13,17-19,36. A similar low level of uptake is seen in other African countries among
AC

the general female populace33,40 and female health workers.26,41 It is therefore not surprising that

cervical cancer is still the leading gynaecological cancer in our environment, in terms of its

prevalence, morbidity and mortality.

Recommendation from doctors/nurses (89.4%) and fear of developing cervical cancer (23.4%)

were the main reasons respondents gave for doing a Pap smear test, while the lack of awareness
 ACCEPTED MANUSCRIPT

about Pap smear (53.8%) and the non–recommendation of the test by Doctors/ Nurses (31.0%)

were the commonest reasons for poor uptake of Pap smear in our study. In other Nigerian

studies, lack of awareness about Pap smear (95.5%)30 and non-recommendation of the test

(52.3% in the study group and 63.6% in the control group)42 were the major reasons for not

PT
doing a Pap smear test. Similarly, the main barrier to the uptake of Pap smear in Kuwait and Iran

RI
was non-recommendation of the test by physicians in 48.4%27 and 52.2%43 of cases,

respectively. These findings suggest that health workers, especially doctors/nurses, have a

SC
critical role to play in reducing the burden of cervical cancer disease in our environment. In the

absence of an established cervical screening program, the importance of regular health education

U
and counseling of women about cervical cancer, its prevention and screening tests by
AN
doctors/nurses in the health facility or in the community cannot be understated. This is because

these categories of health workers have more contact with the women in the health facility, and
M

also because these patients have a high regard for the opinion of health workers and their advice
D

regarding health matters. Better health education will improve women’s knowledge about the
TE

disease and enhance the uptake of cervical screening. These knowledgeable women will in turn

promote the knowledge and uptake of the screening test among their peers, friends and relatives
EP

as seen in our study, where knowing someone who had done a Pap smear accounted for the 3rd

most stated reason (12.8%) for respondent’s uptake of Pap smear.

C
AC

The level of education was the only socio-demographic factor that was significantly associated

with increased knowledge of cervical cancer disease in our study. Having a tertiary level of

education was a significant factor associated with good knowledge of the symptoms and risk

factors of cervical cancer among the study participants. Likewise, women who had prior
 ACCEPTED MANUSCRIPT

counseling by doctors/nurses about cervical cancer and women who knew someone with cervical

cancer had significantly better knowledge of the symptoms and risk factors of cervical cancer.

Concerning Pap smear, a high level of education was significantly associated with increased

PT
awareness of Pap smear but not its uptake among respondents, whereas prior counseling by

doctors/nurses about cervical cancer and knowing someone who has cervical cancer significantly

RI
increased both the awareness of Pap smear and the uptake of Pap smear test. In other studies, the

SC
participants’ level of education did not significantly influence the uptake of cervical cancer

screening in one study,33 while it significantly predicted uptake of cervical cancer screening in

U
another study.24 Though education is a vital tool in health promotion, it may not be the sole
AN
determinant of the health practices of individuals which are usually multifactorial in nature.

Several studies have identified physician recommendation as a major determinant and predictor
M

of the uptake of cancer screening tests, irrespective of the barriers.44-47 It was therefore not

surprising that women in our study, most of whom had tertiary education, identified
D

“recommendation by doctor/nurse” and “non-recommendation by doctor/nurse” as major reasons

TE

for doing and not doing Pap smear, respectively.

C EP
AC
 ACCEPTED MANUSCRIPT

5.0 CONCLUSION

The knowledge of cervical cancer and the uptake of Pap smear screening are abysmally low

among the women in our study. Though a high level of formal education and literacy level are

PT
associated with increased awareness and knowledge of the disease, it had no influence on the

uptake of Pap smear. Regular health education of women and recommendation of Pap smear

RI
screening by clinicians and other health care providers will go a long way to improve the uptake

SC
of Pap smear, and ultimately reduce the incidence and burden of the disease.

U
AN
M
D
TE
C EP
AC
 ACCEPTED MANUSCRIPT

6.0 FINANCIAL SUPPORT AND SPONSORSHIP:

Nil

PT
RI
U SC
AN
M
D
TE
C EP
AC
 ACCEPTED MANUSCRIPT

7.0 CONFLICT OF INTEREST:

The authors state that they have no conflicts of interest.

PT
RI
U SC
AN
M
D
TE
C EP
AC
 ACCEPTED MANUSCRIPT

8.0 REFERENCES

1. Ferlay J, Soerjomataram I, Ervik M, Dikshit R, Eser S, Mathers C, et al. GLOBOCAN

2012 v1.2, Cancer Incidence and Mortality Worldwide: IARC Cancer Base No. 11

PT
[Internet]. Lyon, France: International Agency for Research on Cancer; 2013. Available

from: http://globocan.iarc.fr.

RI
2. Bruni L, Barrionuevo-Rosas L, Albero G, Serrano B, Mena M, Gómez D, et al. ICO

SC
Information Centre on HPV and Cancer (HPV Information Centre). Human

Papillomavirus and Related Diseases in Africa. Summary Report 27 July 2017. [Data

U
Accessed on 27/07/17].
AN
3. Airede LR, Onakewhor JUE, Aziken ME, Ande ABA, Aligbe JU. Carcinoma of the

uterine cervix in Nigerian women: the need to adopt a national prevention strategy. Sahel
M

Med J. 2008; 2(1): 1 – 11.

4. Jedy-Agba E, Curado MP, Ogunbiyi O, et al. Cancer incidence in Nigeria: a report from
D

population-based cancer registries. Cancer Epidemiol. 2012; 36: 271–278.

TE

5. Awodele O, Adeyomoye AA, Awodele DF, Fayankinnu VB, Dolapo DC. Cancer
EP

distribution pattern in south-western Nigeria. Tanzan J Health Res. 2011; 13: 125–131.

6. Peirson L, Fitzpatrick-Lewis D, Ciliska D, Warren R. Screening for cervical cancer: a

C

systematic review and meta-analysis. Syst Rev. 2013; 2:35. doi:10.1186/2046-4053-2-35.

AC

7. Wright KO, Aiyedehin O, Akinyinka MR, Ilozumba O. Cervical cancer: Community

perception and preventive practices in an urban neighborhood of Lagos (Nigeria) ISRN

Prev Med. 2014; article ID 950534 9pgs.

8. Bakari M, Takai IU, Bukar M. Awareness and utilization of Papanicoloau smear among

health care workers in Maiduguri, Nigeria. Niger J Basic Clin Sci. 2015; 12: 34-38.
 ACCEPTED MANUSCRIPT

9. Gustafsson L, Sparen P, Gustafsson M, Wilander E, Bergstrdm R, Adami HO. Efficiency

of organised and opportunistic cytological screening for cancer in situ of the cervix.

British J Cancer. 1995; 72: 498-505.

10. Horan T. Women’s health. Screening in time saves lives. Nurs Comm. 2007;8:25-26.

PT
11. American cancer society. Global cancer facts & figures, 3rd Edition. Atlanta: American

RI
cancer society; 2015.

12. Owoeye IOG, Ibrahim IA. Knowledge and attitude towards cervical cancer screening

SC
among female students and staff in a tertiary institution in the Niger Delta. Int J Med

Biomed Res. 2013; 2(1): 48-56.

U
13. Udigwe GO. Knowledge, attitude and practice of cervical cancer screening (Pap smear)
AN
among female Nurses in Nnewi, south eastern Nigeria. Niger J Clin Pract. 2006; 9(1): 40

– 43.
M

14. Onah HE, Ozugwu FO, Eze JM. Cervical cancer screening. A survey of current practice
D

among Nigerian Gynaecologist. Trop J Obstet Gynaecol 2001; 18(2): 78 – 81.

TE

15. Ngoma T. World Health Organization cancer priorities in developing countries. Ann.

Oncol. 2006: 17 (Suppl. 8), viii9—viii14.

EP

16. Anorlu RI, Ribiu KA, Abudu OO, Ola ER. Cervical cancer screening practices among

general practitioners in Lagos, Nigeria. J Obstet Gynaecol 2007; 27(2): 181 – 14.
C

17. Bukar M, Takai IU, Audu BM. Determinants of utilization of Papanicolaou’s smear
AC

among outpatient clinic attendees in North‑eastern Nigeria. Afr J Med Med Sci.

2012;41:183-189.
 ACCEPTED MANUSCRIPT

18. Oyebode TA, Sagay SA, Ekwempu CC, Daru PH. The possible role of the gynaecologist

in the poor awareness and non‑utilization of the pap smear among female health

workers. Trop J Obstet Gynaecol. 2006; 23(Suppl 1):S20.

19. Aboyeji PA, Ijaiya MA, Jimoh AA. Knowledge, attitude and practice of cervical smear as

PT
a screening procedure for cervical cancer in Ilorin, Nigeria. Trop J Obstet Gynaecol.

RI
2004;21:114-117.

20. Bukar M, Audu BM. Women’s attitude towards cervical cancer screening in North

SC
Eastern Nigeria. Nig Med Pract. 2011; 60: 13-18.

21. Parkin DM, Bray F, Ferlay J, Pisani P. Global cancer statistics, 2002. Cancer J Clin.

2005; 55: 74-108.

U
AN
22. Ajenifuja KO, Adepiti CA. Knowledge of cervical cancer and utilization of Pap smear

among patients in a tertiary centre in south west Nigeria. Ibom Med J. 2008; 3(2): 56–60.
M

23. Wright KO, Faseru B, Kuyinu YA, Faduyile FA. Awareness and uptake of the Pap smear
D

among market women in Lagos, Nigeria. J Public Health Afr. 2011;2:e14.

TE

24. Leung SSK, Leung I. Cervical cancer screening: knowledge, health perception and

attendance rate among Hong Kong Chinese women. Int J Women's Health. 2010; 2: 221-
EP

228.

25. Charan J, Biswas T. How to Calculate Sample Size for Different Study Designs in
C

Medical Research? Indian J Psychol Med. 2013; 35(2): 121-126. doi:10.4103/0253-

AC

7176.116232.

26. Abiodun OA, Fatungase OK, Olu-Abiodun OO, Idowu-Ajiboye BA, Awosile JO. An

assessment of women’s awareness and knowledge about cervical cancer and screening
 ACCEPTED MANUSCRIPT

and the barriers to cervical screening in Ogun State, Nigeria. IOSR-JDMS. 2013; 10(3):

52 – 58.

27. Al Sairafi M, Mohamed FA. Knowledge, Attitudes, and Practice Related to Cervical

Cancer Screening among Kuwaiti Women. Med Princ Pract. 2009;18:35–42 doi:

PT
10.1159/000163044.

RI
28. Nnodu O, Erinosho L, Jamda M, Olaniyi O, Adelaiye R, Lawson L. et al. Knowledge and

attitudes towards cervical cancer and human papilloma virus: a Nigerian pilot study. Afr J

SC
Reprod Health. 2010; 14(1):95-108.

29. Dhendup T, Tshering P. Cervical cancer knowledge and screening behaviors among

U
female university graduates of year 2012 attending national graduate orientation program,
AN
Bhutan. BMC Women's Health. 2014; 14: 44. doi:10.1186/1472-6874-14-44.

30. Feyi-Waboso PA, Kamanu C, Aluka C. Awareness and risk factors for cervical cancer
M

among Women in Aba, south-eastern Nigeria. Trop J Obstet Gynaecol. 2005; 22(1):25-
D

26.
TE

31. Amosu AM, Degun AM, Babalola AO, Thomas MA. Level of specific knowledge,

awareness, perception and screening behavior regarding carcinoma of the cervix among
EP

rural women in Iwo local government area, Osun state, Nigeria. Ann Biol Res. 2011;

2(2): 206 – 221.

C

32. Abiodun OA, Fatungase OK, Olu-Abiodun OO. Knowledge, perception and predictors of
AC

uptake of cervical screening among rural Nigerian women. J Public Health Epidermiol.

2014; 6(3): 119 – 124.

 ACCEPTED MANUSCRIPT

33. Ebu NI, Mupepi SC, Siakwa MP, Sampselle CM. Knowledge, practice, and barriers

toward cervical cancer screening in Elmina, Southern Ghana. Int J Womens Health.

2015:7 31–39.

34. Gichangi P, Estambale B, Bwayo J. Knowledge and practice about cervical cancer and

PT
Pap smear among patients at Kenyatta National Hospital, Nairobi. Int J Gynecol Cancer.

RI
2003; 13: 827 – 833.

35. Awodele O, Adeyomoye AAA, Awodele DF, Awodele IO, Dolapo DC. A Study on

SC
Cervical Cancer Screening Amongst Nurses in Lagos University Teaching Hospital,

Lagos, Nigeria. J. Cancer Educ. 2011; 26(3):497–504 doi: 10.1007/s13187-010-0187-6.

U
36. Bakari M, Takai IU, Bukar M. Awareness and utilization of Papanicoloau smear among
AN
health care workers in Maiduguri, Nigeria. Niger J Basic Clin Sci. 2015;12:34-38.

37. Ogun GO, Bejide R. Cervical cancer in Nigeria, still a dismal story: the poor state of
M

cervical cytology screening, factors responsible for continuous high incidence of cervical
D

cancer and hope for improvement. UICC World Cancer Congress, Washington DC, USA
TE

2006.

38. Yu CKH, Rymer J. Women’s attitudes to and awareness of smear testing and cervical
EP

cancer. Br J Family Planning. 1998; 23: 127-133.

39. Adanu RM, Seffah JD, Duda R, Darko R, Hill A, Anarfi J. Clinic visits and cervical
C

cancer screening in Accra. Ghana Med J. 2010; 44 (2): 59–63.

AC

40. Mutyaba T, Mmiro FA, Weiderpass E. Knowledge, attitudes and practices on cervical

cancer screening among the medical workers of Mulago Hospital, Uganda. BMC Med

Educ. 2006; 6:13.

 ACCEPTED MANUSCRIPT

41. Urasa M, Darj E. Knowledge of cervical cancer and screening practices of nurses at a

regional hospital in Tanzania. Afr Health Sci. 2011; 11(1): 48 – 57.

42. Adamu AN, Abiola AO, Ibrahim M. The effect of health education on the knowledge,

attitude, and uptake of free Pap smear among female teachers in Birnin-Kebbi, North-

PT
Western Nigeria. Niger J Clin Pract. 2012;15:326-32.

RI
43. Rezaie-Chamani S, Mohammad-Alizadeh-Charandabi S, Kamalifard M. Knowledge,

Attitudes and Practice about Pap Smear among Women Reffering to A Public Hospital. J

SC
Family Reprod Health. 2012; 4(6): 177 – 182.

44. Smith RA, Cokkinides V, Brawley OW. Cancer screening in the United States, 2009: A

U
review of current American Cancer Society guidelines and issues in cancer screening. CA
AN
Cancer J Clin. 2009; 59: 27–41. doi:10.3322/caac.20008.

45. Bessler P, Aung M, Jolly P. Factors Affecting Uptake Of Cervical Cancer Screening
M

Among Clinic Attendees In Trelawny, Jamaica. Cancer Control. 2007; 14: 396-404.
D

46. Levy BT, Nordin T, Sinift S, Rosenbaum M, James PA. Why hasn't this patient been
TE

screened for colon cancer? An Iowa Research Network study. J Am Board Fam

Med. 2007; 20: 458–468.

EP

47. Sohl SJ, Moyer A. Tailored interventions to promote mammography screening: a meta-

analytic review. Prev Med. 2007; 45: 252–261.

C
AC
 ACCEPTED MANUSCRIPT

TABLES

Table 1: Socio-demographic characteristics of respondents

N= 205
Variable Frequency Percentage
Age (as at last birthday)

PT
≤ 20 years 2 1.0%
21 – 30 years 62 30.2%
31 – 40 years 95 46.4%

RI
41 – 50 years 32 15.6%
51 – 60 years 9 4.4%

SC
≥ 61 years 5 2.4%
Total 205 100.0%
Occupation
Skilled 22 10.7%

U
Semi-skilled 170 82.9%
AN
Unskilled 3 1.5%
Unemployed 10 4.9%
Total 205 100.0%
Educational Status
M

No formal education 1 0.5%

Primary education 2 1.0%
D

Secondary education 47 22.9%

Tertiary education 155 75.6%
TE

Total 205 100.00%

Ethnicity/Tribe
Yoruba 102 49.8%
EP

Igbo 77 37.6%
Hausa 2 1.0%
Others 24 11.6%
C

Total 205 100.00%

Marital status
AC

Single 26 12.7%
Married 162 79.0%
Separated 6 3.0%
Divorced 3 1.5%
Widow 8 3.8%
Total 205 100.00%
Religion
Christianity 175 85.4%

1
 ACCEPTED MANUSCRIPT

Muslim 30 14.6%
Total 205 100.0%
Parity
0 80 39.0%
1 38 18.5%
2 38 18.5%

PT
3 22 10.8%
4 12 5.9%
≥5 15 7.3%
Total 205 100.0%

RI
U SC
AN
M
D
TE
CEP
AC

2
 ACCEPTED MANUSCRIPT

Table 2: Knowledge of cervical cancer among the respondents

Variable Category of knowledge

PT
Good Poor Total

RI
n = 205

SC
Knowledge of symptoms of 82(40.0%) 123(60.0%) 205 (100.00%)
cervical cancer

Knowledge of risk factors of 32(15.6%) 173(84.4%) 205 (100.00%)

U
cervical cancer
AN
M
D
TE
C EP
AC

3
 ACCEPTED MANUSCRIPT

Table 3: Identified symptoms and risk factors of cervical cancer.

N = 205

Symptoms Frequency Percentage

PT
Post – coital bleeding 81 39.5%
Abnormal vaginal bleeding 89 43.4%
Offensive vaginal discharge 77 37.6%

RI
Weight loss 64 31.2%
Lower abdominal pain 80 39.0%

SC
Risk factors Frequency Percentage

HPV infection 84 24.9%

U
Early marriage 38 18.5%
AN
Multiple sexual partners 77 37.6%
Early age at sexual intercourse 55 26.8%
Early age at birth 22 10.7%
Having partners who have multiple sexual partners 70 34.2%
M

Smoking 30 14.6%
HIV infection 42 20.5%
D

Use of birth control pills 24 11.7%

Having plenty children (multiparity) 19 9.3%
TE

Reduced body immunity 45 22.0%

Sexually transmitted infections 71 34.6%
Multiple responses observed
C EP
AC

4
 ACCEPTED MANUSCRIPT

Table 4: Respondent’s main reasons for doing Pap smear.

N = 47

Reasons Frequency Percentage

PT
Recommendation by Doctors / Nurses 42 89.4%
Advice from friends / relatives 4 8.5%
Advice from the media 6 12.8%

RI
Because I know someone who had done the test 6 12.8%
Because I know I am at risk of having the disease 5 10.6%

SC
Because I know someone who has cervical cancer 5 10.6%
Fear of developing cervical cancer 11 23.4%
Because it is affordable 3 6.4%

U
Because my husband encouraged me to do itAN 5 10.6%
M
D
TE
C EP
AC

5
 ACCEPTED MANUSCRIPT

Table 5: Respondent’s main reasons for not doing Pap smear.

N = 158

Reasons Frequency Percentage

PT
Because I am not aware of it 85 53.8%
Because I don’t know where to do the test 25 15.8%
Because my Doctor did not advise me to do it 49 31.0%

RI
Because I couldn’t afford it 8 5.1%
Because the method of doing the test is embarrassing 7 4.4%

SC
Because my husband discouraged me from doing it 1 0.6%
Fear of being diagnosed with cervical cancer 7 4.4%
Because I don’t know much about the test 37 23.4%

U
Because I believe I can’t have cervical cancer 29 18.4%
Because the test is painful 1 0.6%
AN
Because of lack of time due to busy schedule 2 1.3%
M
D
TE
C EP
AC

6
 ACCEPTED MANUSCRIPT

Table 6: Factors associated with respondents’ knowledge of cervical cancer.

N = 205

PT
Variable
Knowledge of risk factors of cervical
Knowledge of symptoms of
cancer
cervical cancer

RI
SC
n (%) X2 P value n (%) X2 P value

U
Good Poor Good Poor
Age (years)
AN
≤ 20 0(0.0) 2(1.6) 6.90⃰ 0.735 0(0.0) 2(1.2) 4.08⃰ 0.538
21 – 30 22(26.8) 40(32.5) 9(28.1) 53(30.6)
31 – 40 41(50.0) 54(43.9) 16(50.0) 79(45.7)
M

41 – 50 13(15.9) 19(15.4) 7(21.9) 25(14.5)

51 – 60 4(4.9) 5(4.1) 0(0.0) 9(5.2)
≥ 61 2(2.4) 3(2.4) 0(0.0) 5(2.9)
D

Total 82(100.0) 123(100.0) 32(100.0) 173(100.0)

Educational
TE

Status
None 1(1.2) 0(0.0) 18.46⃰ 0.005 0(0.0) 1(0.6) 4.72⃰ 0.009
Primary 1(1.2) 1(0.8) 0(0.0) 2(1.2)
EP

Secondary 8(9.8) 39(31.7) 3(9.4) 44(25.4)

Tertiary 72(87.8) 83(67.5) 29(90.6) 126(72.8)
Total 82(100.0) 123(100.0) 32(100.0) 173(100.0)
C

Marital
status 5.98⃰ 0.649 7.41⃰ 0.116
AC

Single 6(7.3) 20(16.3) 1(3.1) 25(14.5)

Married 70(85.4) 92(74.8) 31(96.9) 131(75.7)
Separated 2(2.4) 2(1.6) 0(0.0) 6(3.5)
Divorced 1(1.2) 4(3.2) 0(0.0) 3(1.7)
Widow 3(3.7) 5(4.1) 0(0.0) 8(4.6)
Total 82(100.0) 123(100.0) 32(100.0) 173(100.0)

7
 ACCEPTED MANUSCRIPT

Religion
Christianity 69(84.1) 106(86.2) 1.06 0.588 26(81.2) 149(86.1) 0.51 0.473
Muslim 13(15.9) 17(13.8) 6(18.8) 24(13.9)
82(100.0) 123(100.0) 32(100.0) 173(100.0)
Total
Prior
counseling by

PT
Doctor /
Nurse
Yes 49(59.8) 31(25.2) 26.61 <0.001 21(65.6) 59(34.1) 13.90 0.001
No 33(40.2) 92(74.8) 11(34.4)

RI
114(65.9)
Total 82(100.0) 123(100.0) 32(100.0) 173(100.0)
Knowing

SC
someone with
cervical
cancer
Yes

U
No 18(22.0) 6(4.9) 15.56 0.004 10(31.3) 14(8.1) 15.06 0.001
Total 64(78.0) 117(95.1) 22(68.7) 159(91.9)
AN
82(100.0) 123(100.0) 32(100.0) 173(100.0)

⃰ Fisher exact chi square

M
D
TE
C EP
AC

8
 ACCEPTED MANUSCRIPT

Table 7: Factors associated with respondents’ awareness and uptake of Pap smear.

N = 205

PT
Variable
Uptake of Pap smear
Awareness of Pap smear

RI
SC
n (%) X2 P value n (%) X2 P value

U
Yes No Yes No
Age (years)
AN
≤ 20 0(0.0) 2(2.2) 5.93⃰ 0.313 0(0.0) 2(1.3) 8.10⃰ 0.151
21 – 30 36(31.9) 26(28.3) 10(21.3) 52(32.9)
31 – 40 55(48.7) 40(43.5) 22(46.8) 73(46.2)
M

41 – 50 17(15.0) 15(16.3) 12(25.5) 20(12.6)

51 – 60 4(3.5) 5(5.4) 3(6.4) 6(3.8)
≥ 61 1(0.9) 4(4.3) 0(0.0) 5(3.2)
D

Total 113(100.0) 92(100.0) 47(100.0) 158(100.0)

Educational
TE

Status
None 0(0.0) 1(1.1) 13.68⃰ 0.003 0(0.0) 1(0.6) 1.21⃰ 0.751
Primary 2(1.8) 0(0.0) 1(2.1) 1(0.6)
EP

Secondary 16(14.2) 31(33.7) 10(21.3) 37(23.5)

Tertiary 95(84.1) 60(65.2) 36(76.6) 119(75.3)
Total 113(100.0) 92(100.0) 47(100.0) 158(100.0)
C

Marital
status
AC

Single 14(12.4) 12(13.0) 5.53⃰ 0.237 2(4.3) 24(15.2) 4.27⃰ 0.371

Married 91(80.5) 71(77.2) 40(85.1) 122(77.2)
Separated 5(4.4) 1(1.1) 2(4.3) 4(2.5)
Divorced 1(0.9) 2(2.2) 1(2.1) 2(1.3)
Widow 2(1.8) 6(6.5) 2(4.3) 6(3.8)
Total 113(100.0) 92(100.0) 47(100.0) 158(100.0)

9
 ACCEPTED MANUSCRIPT

Religion
Christianity 99(87.6) 76(82.6) 1.02 0.314 44(93.6) 131(82.9) 3.32⃰ 0.068
Muslim 14(12.4) 16(17.4) 3(6.4) 27(17.1)
113(100.0) 92(100.0) 47(100.0) 158(100.0)
Total
Prior
discussion

PT
with Doctor /
Nurse
Yes 74(65.5) 6(6.5) 74.39 <0.001 38(80.9) 42(26.6) 46.90 <0.001
No 39(34.5) 86(93.5) 9(19.1)

RI
116(73.4)
Total 113(100.0) 92(100.0) 47(100.0) 158(100.0)
Knowing

SC
someone with
cervical
cancer
Yes

U
No 16(14.2) 8(8.7) 13.67 0.003 12(25.5) 12(7.6) 15.23 0.002
Total 97(85.8) 84(91.3) 35(74.5) 146(92.4)
AN
113(100.0) 92(100.0) 47(100.0) 158(100.0)

⃰ Fisher exact chi square

M
D
TE
C EP
AC

10