|Year : 2018 | Volume
| Issue : 2 | Page : 90-97
Pap smear awareness, utilization, and pattern of cervical intraepithelial neoplasia among women attending a tertiary hospital in Northwestern Nigeria
Abdulrahman Shuaibu, Bukar Alhaji Grema, Godpower Chinedu Michael
Department of Family Medicine, Aminu Kano Teaching Hospital, Kano State, Nigeria
|Date of Web Publication||27-Nov-2018|
Dr. Abdulrahman Shuaibu
Department of Family Medicine, Aminu Kano Teaching Hospital Kano, P.M.B 3452, Kano State
Source of Support: None, Conflict of Interest: None
Background: Globally, cervical cancer affects approximately 528,000 women each year, with about 80% of them occurring in developing countries. Developed countries have successfully reduced the incidence of cervical cancer by 70% through organized cervical screening programs. Objective: The aim of the study is to assess the level of Pap smear awareness and utilization among adult females attending the general outpatient clinic of Aminu Kano Teaching Hospital, Northwestern Nigeria, in order to encourage early detection of premalignant cervical cancer. Methods: This was a descriptive cross-sectional study that assessed Pap smear awareness, utilization, and pattern of cervical intraepithelial neoplasia among 422 adult females in Kano, Northwestern Nigeria, using an interviewer-administered questionnaire. SPSS version 20 was used to analyze the data. The sociodemographic characteristics of participants, risk factors of cervical cancer, and awareness and utilization of Pap smears by participants were expressed in means and proportions. The Chi-square test was used to explore associations between categorical variables. Logistic regression was performed to identify the predictors of Pap smear awareness and its utilization among the study participants. P < 0.05 was considered statistically significant. Results: Of the 422 women who participated in the study, the majority (292, 69.2%) had never heard of Pap smear screening while 130 (30.8%) were aware of Pap smear. Similarly, 342 (81.0%) women who participated in the study had never undergone a Pap smear. Three hundred and eight (74%) had normal cytology results, 107 (25%) had inflammatory changes, 4 (0.8%) had low-grade squamous intraepithelial lesion, and 1 (0.2%) had high-grade squamous intraepithelial lesion. Having higher education and being employed were associated with Pap smear awareness while increasing age and educational level were associated with Pap smear utilization. Conclusion: This study revealed a low awareness and utilization of Pap smear screening in Northwestern Nigeria.
Keywords: Awareness, cervical intraepithelial neoplasia, Pap smear, utilization
|How to cite this article:|
Shuaibu A, Grema BA, Michael GC. Pap smear awareness, utilization, and pattern of cervical intraepithelial neoplasia among women attending a tertiary hospital in Northwestern Nigeria. Muller J Med Sci Res 2018;9:90-7
|How to cite this URL:|
Shuaibu A, Grema BA, Michael GC. Pap smear awareness, utilization, and pattern of cervical intraepithelial neoplasia among women attending a tertiary hospital in Northwestern Nigeria. Muller J Med Sci Res [serial online] 2018 [cited 2019 May 26];9:90-7. Available from: http://www.mjmsr.net/text.asp?2018/9/2/90/246171
| Introduction|| |
Cervical cancer is a malignant neoplasm of the cervix uteri, affecting approximately 528,000 women annually. Worldwide, estimates of the disease have revealed that 70% of such cases occur in developing countries, where the incidence of the disease is expected to rise from 444,546 to 588,922 cases between 2012 and 2025., Developed countries have successfully reduced the incidence of cervical cancer by 70% in the last 50 years, as cancer of the cervix is a preventable disease. The reduction in the incidence of the disease in developed countries was achieved by screening sexually active women with Pap smear More Details tests and visual inspection of the cervix with acetic acid.
Cervical cancer is the most common cancer among women in Northern Nigeria, accounting for 65.7% of all gynecological cancers. The current estimates indicate that 40.43 million women are at risk of developing cervical cancer in Nigeria. Each year, approximately 14,550 women are diagnosed with cervical cancer and 9,659 die from the disease in Nigeria. The deaths of women from cervical cancer have profound consequences on the well-being of their families, such as a decrease in school attendance and a decline in the nutritional status of their children. The factors that have contributed to the low uptake of Pap smear screening include lack of accessibility to such screening test due to few service delivery points and the time required to access such services. Currently, there is no organized and routine screening program for women of reproductive age in Nigeria and, therefore, women present late with advanced stages of the disease when treatment is of little or no benefit.
In developed countries, the incidence of cervical cancer has declined because of increased awareness and the presence of organized screening programs. This is not the case in Nigeria where there is no organized screening program to detect premalignant cervical lesions. The Northern part of Nigeria experiences the highest maternal mortality rates in the country; hence, attention is focused toward reducing obstetric deaths while morbidity and mortality associated with genital tract malignancies such as cervical cancer have been neglected. Assessment of Pap smear awareness and utilization among women is one of the first steps in this process.
Anecdotal evidence has shown that most women with cervical cancer present to our hospital late, which make cure impossible with only palliative care as a last resort. Despite the late presentation of the disease, no previous study has been conducted in the general outpatient clinic (GOPC) on Pap smear awareness in order to increase its utilization among females, which may ultimately lead to the detection of precancerous cervical lesions. Similarly, despite the recognized importance of regular Pap smears, most of the women who attend our clinic are either unaware of them or not convinced that they need them.
The Papanicolaou smear for cervical cytology fulfills most of the criteria for a screening test because it is cost-effective and acceptable to most patients. It can detect cervical intraepithelial neoplasia (CIN), resulting in decreased morbidity and mortality from invasive cervical cancer. Hence, this study is expected to reveal the factors associated with awareness and utilization of Pap smear tests and the pattern of CIN among adult females attending GOPC in order to help in the planning of future screening services.
| Subjects and Methods|| |
This study was carried out in the GOPC of our hospital. The hospital provides clinical care to Kano state residents and serves neighboring states as a referral center. The hospital has a capacity of 500 beds. The GOPC is a busy primary care center run by family physicians, residents in family medicine, and medical officers.
This study was a descriptive cross-sectional study among 422 women (18–65 years) attending GOPC between April 1 and June 30, 2015. This age range was arrived at because the age range of 25–64 represents the age at which cervical cancer changes are more prevalent. Similarly, the lower age range of 18 was chosen because anecdotal evidence has shown that women in the study environment get married at around this age; hence, they are sexually active.
From clinic records, an average of 840 adult females is seen at the GOPC; thus, the estimated sampling frame was 10,800, over a 12-week period. Using 50.9%, the proportion of respondents that had knowledge of cervical cancer reported by a study in Jos, Plateau state. The Fisher's formula for estimating sample size for descriptive studies was used to arrive at a sample size of 384. Ten percent of the sample size was added for possible poorly stained specimens to arrive at a total sample size of 422. Female patients who had hysterectomy, postcoital bleeding, and cancer of the cervix and those women who were pregnant were excluded from the study.
A systematic sampling method was used to select every 25th participant (10,800/422) until the sample size was reached. In the event the 25th patient being among those participants excluded from the study, the 24th patient was chosen. The first participant was selected by balloting.
An adapted pretested interviewer-administered questionnaire was administered to each participant after a written informed consent was obtained., The questionnaire assessed participants' sociodemographics, awareness of Pap smear, and risk factors for cervical cancer. Following questionnaire administration, Pap smear was collected by the investigator from each participant. Ethical approval was obtained from the aminu kano teaching hospital (AKTH) Research Ethics Committee.
Pap smear collection technique
The procedure was carried out in the presence of a female chaperon in a designated consulting room of the GOPC ensuring privacy and confidentiality. Before the procedure, patients were asked about their last menstrual period. This was because blood and cellular debris tend to obscure cells on the smear. They were also asked about a history of vaginal discharge and lower abdominal pain in order to exclude pelvic inflammatory disease (PID). Those women with PID and women whose last menstrual period (LMP) was less than a week were rescheduled for Pap smear collection.
A glass slide was labeled with the participant's initials and research number after a laboratory request form had been completed. In the lithotomy position, a single-use sterile Cusco's speculum was inserted gently through the vagina until the cervix was well exposed with the aid of a light source. The cervix was then inspected for ulcerations or masses. An Ayres spatula was inserted into the endocervical canal around the transformation zone and rotated several times through 360°. Afterward, the smear was spread evenly on a glass slide and quickly fixed in equal parts of 95% ethanol to prevent air-drying. The sample was taken to the histopathology laboratory of our hospital and stained using the Papanicolaou method by the cytotechnician.
The smeared slide was dipped in descending grades of alcohol (90%, 70%, to water) for 15 s each. The smear was deeped in Harris hematoxylin for 5 min and rinsed in tap water for 1 min. It was then dipped in blue in Scott's tap water for 30 s and rinsed in water. The smear was further dipped in 95% alcohol for 15 s and stained in orange green 6 for 1 min and rinsed in 95% alcohol for 15 s. The slide was then stained in Eosin Azure 50 for 1 min and rinsed in 95% and 100% alcohol for 15 s each. The smeared slides were cleared in xylene and mounted in a diphenyl xylene mountant. Two histopathologists read all the slides. They interpreted the results as follows:
The cytoplasm of superficial cells, intermediate cells, and parabasal cells were interpreted as pink, pale greenish, and deep greenish blue, respectively. The nuclei, red blood cells, and white blood cells were stained as dark blue, bright red, and pale blue, respectively.
Abnormal cervical cytology was classified using the Bethesda classification into normal, inflammatory, atypical squamous intraepithelial cells, low-grade squamous intraepithelial cells, and high-grade squamous intraepithelial cells.
Participants who had atypical squamous intraepithelial cells Atypical squamous intraepithelial cells (ACS), low-grade squamous intraepithelial lesions (LGSIL), and high-grade squamous intraepithelial lesions (HGSIL) were referred to the gynecologist for colposcopy and appropriately managed. Those patients who had cervicitis, inflammatory changes on Pap smear, or foul-smelling vaginal discharge were treated with oral antibiotics. In addition, those with cervicitis were advised to repeat Pap smear test in 6 months.
| Results|| |
Sociodemographic characteristics of the participants
Of the 422 women who participated in the study, 34 (8.1%) were from the rural areas while 388 (91.9%) were from the urban areas. Their mean age was 36 ± 10.1 years ranging from 18 to 65 years. The majority 226 (53.5%) were between the ages of 18 and 35 years while 175 (41.5%) and 21 (5.0%) were between the ages of 36–55 and 56–65 years, respectively. Most of the women 389 (92.2%) were Muslims while 33 (7.8%) were Christians. The majority (368, 87.2%) were married, 8 (1.9%) were single, 28 (6.6%) were divorced, and 18 (4.3%) were widowed. Most of the women (151, 35.8%) had tertiary level of education, while 126 (29.9%) and 77 (18.2%) had secondary and primary level of education, respectively. Most of the women (312, 73.9%) were unemployed while 60 (14.2%) and 40 (9.5%) were skilled and unskilled workers, respectively [Table 1].
Awareness of Pap smear, its utilization, and perceived hindrances to utilizing Pap smear screening among the participants
The majority (292, 69.2%) had never heard of Pap smear screening while 130 (30.8%) were aware of Pap smear [Table 2]. The majority (342, 81.0%) of women who participated in the study had never undergone a Pap smear while only 80 (19.0%) had experienced the test. Only 146 (34.6%) were aware of hospitals that conduct Pap smear screening while 276 (65.4%) were not aware of where it is carried out [Table 2].
|Table 2: Awareness of Pap smear, its utilization, and perceived hindrances to utilizing Pap smear screening among the participants|
Click here to view
The perceived reasons for poor uptake of Pap smear screening are presented in [Table 2]. Ignorance of screening test (117, 34.2%) and nonrecommendation (126, 36.9%) were the most common reasons cited by the women. Other reasons included the following: no reason 49 (14.3%), lack of time 28 (8.2%), afraid of the results 8 (2.3%), costly 6 (1.8%), it is for married women 7 (2.0%), and distance 1 (0.3%) [Table 2].
Pattern of cervical intraepithelial neoplasia
Cytology results were available for 420 women (99.5%), and two samples (0.5%) were poorly stained. Three hundred and eight (74%) had normal cytology results, 107 (25%) had inflammatory changes, 4 (0.8%) had LGSIL, and 1 (0.2%) had HGSIL [Figure 1].
|Figure 1: Bar graph shows the pattern of cervical intraepithelial neoplasia among the participants|
Click here to view
Relationship between sociodemographic characteristics of the participants and Pap smear awareness
The proportion of women with tertiary education who were aware of Pap smear was 79 (52.3%) while the proportion of women who had secondary education level and aware of Pap smear was 33 (26.2%) [Table 3]. The difference was statistically significant (χ2 = 57.66, P = 0.001). Similarly, the proportion of women who were either professional or skilled workers and aware of Pap smear was 10 (100%) and 32 (53.3%), respectively, while the proportion of those who were not employed and aware of Pap smear was 78 (25.0%). The difference in proportions was statistically significant (χ2 = 42.3, df = 3, P = 0.001). However, other sociodemographic characteristics such as age, religion, residence, and marital status were not associated with Pap smear awareness.
|Table 3: Relationship between the sociodemographic characteristics of the participants and Pap smear awareness|
Click here to view
Relationship between sociodemographic characteristics of the participants and Pap smear utilization
The proportion of women aged 36–55 years who had undergone a Pap smear screening was 46 (26.3%) while the number of women aged 18–35 years who had undergone a Pap smear was 28 (12.4%) [Table 4]. The difference in proportion was statistically significant (χ2 = 13.72, P = 0.001). This suggests that increasing age was associated with Pap smear uptake. Similarly, the proportion of women with tertiary level education who had undergone a Pap smear screening was 41 (27.2%) while the proportion of women with secondary level education who had undergone a Pap smear screening was 21 (16.7%). The difference was statistically significant (X = 12.16, P = 0.01). This suggests that there is a relationship between higher level of education and Pap smear uptake. Other sociodemographic variables such as religion, residence, marital status, and occupation were not associated with Pap smear utilization.
|Table 4: Relationship between the sociodemographic characteristics of the participants and Pap smear utilization|
Click here to view
Logistic regression on Pap smear awareness and utilization
Logistic regression of variables significantly associated with participants' Pap smear awareness showed that educational level and awareness of cervical cancer made statistical contribution to the model [Table 5]. Educational level had an odds ratio of 0.35, signifying that women who had below secondary level of education were 35% less likely to be aware of Pap smear screening (P = 0.001, 95% confidence interval [CI] = 0.19–0.67). Similarly, those women who were aware of cervical cancer were 65 times more likely to be aware of Pap smear screening (P = 0.001, 95% CI = 15.74–269.69).
Age group made a statistically significant contribution on Pap smear utilization. Age group had an odds ratio of 0.44. Those participants who had below secondary level of education were 44% less likely to utilize Pap smear screening (P = 0.03, 95% CI = 0.25–0.76). Similarly, those participants who were aware of cervical cancer were 20 times more likely to utilize Pap smear screening (P = 0.001, 95% CI = 6.36–68.21).
Relationship between risk factors for cervical cancer and abnormal cervical cytology
The proportion of women who were aged 56–65 years and had normal cervical cytology was 19 (90.5%) while the proportion of women who were aged 18–35 and 36–55 years and had normal cytology was 173 (77.2%) and 116 (66.3%), respectively [Table 6]. The difference was statistically significant (X = 9.56, df = 2, P = 0.001). Women aged between 18–35 and 56–65 years were more likely to have normal Pap smears as compared to those between 36 and 55 years. Similarly, the proportion of women with four or less children and had normal cervical cytology was 168 (77.8%), while those that had five or more children was 140 (68.6%). The difference was statistically significant (χ2 = 4.477, df = 1, P = 0.03). Other sociodemographic characteristics such as age at first intercourse, lifetime number of sexual partners, and smoking were not associated with abnormal cervical cytology.
|Table 6: Relationship between risks factors for cervical cancer and pattern of cervical intraepithelial neoplasia among the women|
Click here to view
| Discussion|| |
The success in reducing the incidence of cervical cancer in developed countries is attributed to cytology-based cervical cancer screening programs. Of the 422 women who participated in this study, 91.9% were from the urban areas while 8.1% were from the rural areas. We found that although the majority of the study participants came from the urban areas, only 30.8% of the participants were aware of Pap smear screening. Several Nigerian studies have reported a similar low level of Pap smear awareness including 12.6% in Anambra (Southeast Nigeria), 23.1% in Enugu (Southeast Nigeria), and 37.1% in Osun (Southwest Nigeria); these figures are comparable with 30.7% reported in India. However, a study in Ilorin, North Central Nigeria, found a high level of awareness (67%) among participants. Differences in the sociodemographic characteristics of the two study populations could be responsible for the higher awareness level in the Ilorin study; while our study respondents were mostly unemployed, a majority of the Ilorin study respondents were civil servants; such study participants may likely have more access to health-care information. However, similar to our study, there was a low level of utilization of cervical screening, despite the study being conducted in an urban area. Similarly, a study conducted in Argentina, South America, found that women who were unemployed were under-users of Pap smear screening.
This study found a poor uptake of Pap smear screening at 19.1%. This proportion of Pap smear uptake was, however, higher than 5.1% uptake in a community-based study conducted in Lagos. This might be attributed to the fact that our study was hospital based and therefore it is assumed that women who visit such services may be more aware of Pap smear screening services. In addition, the level of education of the study participants may have contributed to the higher utilization compared to the Lagos study as 29.9% and 35.8% of the women had secondary and tertiary levels of education, respectively. In the United States, a study found 96.7% awareness and 93% utilization, but proportions were lower among those with low educational level and low incomes. However, a study in Taiwan showed that low-income earners were more likely to utilize Pap smear screening than high-income earners. This was because health insurance was compulsory with up to 99% coverage in 2009; therefore, these low-income earners take advantage of the free Pap smear test offered by the National Health Insurance. The study also found that high-income earners usually pay for Thin-prep Pap test or human papillomavirus screening and forego the free Pap smear screening. This presents an opportunity for developing nations where there are no organized screening programs.
Various reasons were provided for nonutilization of Pap smear in this study; these included ignorance of the existence of such a procedure (34.2), no reason (14.3%), not having time (8.2%), being afraid of the results (2.3%), and not recommended (36.9%). These were corroborated by previous studies., Furthermore, because 73.9% of the women were unemployed, coupled with the fact that screening services were neither free nor subsidized in our setting, they may not see the need to utilize such screening services because they are asymptomatic of the disease.
The pattern of CIN in the current study found that 74% of the participants had normal cytology, while 25% had inflammatory cells, 0.8% had LGSIL, and 0.2% had HGSIL lesions, respectively. Kolawale et al., in Kogi State, North Central Nigeria, found that 95.07% of women had normal cytology while 4.93% produced abnormal findings. Similarly, a study in Maiduguri among 2082 women found that 36.3% of them had normal cytology, 40.3% had inflammatory changes, while 6.3% revealed infective agents. The variations across the regions may be a result of variations in the age of sexual exposure, multiple sexual partners, and sexually transmitted infections such as HIV. For example in Jos, North Central Nigeria, a study found that 68.3% of the participants had abnormal cytology. Among women with abnormal cytology, 57.5% had atypical squamous intraepithelial cells (ACUS), 22.2% had LGSIL, and 20.2% had HGSIL. This finding was as a result of a high prevalence HIV infection among the study participants. However, it should be noted that some inflammatory cells are normally seen in virtually all multiparous adult women, particularly immediately before, during, and immediately after the menses, and this is usually of little clinical importance.
In the current study, those women with four or less children had a higher proportion of normal cervical cytology (77.8%) compared to those women with five or more children (68.6%). This finding was found to be statistically significant. Furthermore, 33.7% of the women aged 36–55 had abnormal cytology compared to those women aged 18–35 and 56–65 years whom 22.8% and 9.5% had abnormal cytology respectively. This finding was also found to be statistically significant. The higher prevalence in the age group of 36–55 years may be attributed to the fact that changes in cervical epithelium manifest 10–20 years after the onset of HPV infection.
The strengths of the study are as follows: the researcher personally collected all the Pap smear samples and was also involved in reading most of the slides with the histopathologist. This enhanced the validity of the findings. Furthermore, two histopathologists were involved in reading all the slides. When there was a disagreement between the two of them based on the slide reading, a third histopathologist was contacted for further clarification. Similarly, the sampling technique, which was a systematic sampling technique, was adhered to throughout the research in order to avoid selection bias.
This study being a hospital-based study and conducted in an urban setting could not be generalized to those women living in rural areas.
| Conclusion|| |
This study revealed a low awareness and utilization of Pap smear screening. Therefore, there is a need to address factors such as poverty and illiteracy, which predispose women to cervical cancer due to their lack of awareness of screening tests; this highlights the importance of girl–child education. Furthermore, women should be empowered through skill acquisition programs for them to bear the cost of such screening services.
I will like to acknowledge the two histopathologists who read the slides for this study: Drs. Yusuf and Imam: I appreciate your support and efforts. To my research assistants: Aisha, Fati, and Zubaida: words cannot express my gratitude to you.
Financial support and sponsorship
The study was sponsored by the author.
Conflicts of interest
There are no conflicts of interest.
| References|| |
Ferlay J, Soerjomatram I, Ervik M, Dikshit R, Eser S, Mathrs C. Cancer Incidence and Mortality Worldwide: IARC Cancer Base No. 11 Lyon, France; 2013. Available from: http://www.globocan.iarc.fr
. [Last accessed on 2015 Dec 20].
Abiodun OA, Olu-Abiodun OO, Sotunsa JO, Oluwole FA. Impact of health education intervention on knowledge and perception of cervical cancer and cervical screening uptake among adult women in rural communities in Nigeria. BMC Public Health 2014;14:814.
Oguntayo O, Zayyan M, Kolawole A, Adewuyi S, Ismail H, Koledade K, et al.
Cancer of the cervix in Zaria, Northern Nigeria. Ecancermedicalscience 2011;5:219.
WHO. Human Papillomavirus and Related Cancers. Geneva: WHO; 2010. p. 1-52.
Agosti JM, Goldie SJ. Introducing HPV vaccine in developing countries-key challenges and issues. N Engl J Med 2007;356:1908-10.
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-Western Nigeria. Niger J Clin Pract 2012;15:326-32. [Full text]
Peto J, Gilham C, Fletcher O, Matthews FE. The cervical cancer epidemic that screening has prevented in the UK. Lancet 2004;364:249-56.
Nnadi D, Singh S, Ahmed Y, Siddique S, Bilal S. Histo-pathological features of genital tract malignancies as seen in a tertiary health center in North-Western Nigeria: A 10-year review. Ann Med Health Sci Res 2014;4:S213-7.
Ojiyi E, Dike Ie, Okeudo C, Ejikem C, Nzewuihe A, Agbata A, et al.
Local risk factors in genital human papilloma virus infection in cervical smears. Ann Med Health Sci Res 2013;3:529-35.
] [Full text]
Hyacinth HI, Adekeye OA, Ibeh JN, Osoba T. Cervical cancer and pap smear awareness and utilization of pap smear test among federal civil servants in North Central Nigeria. PLoS One 2012;7:e46583.
Beevi N, Sreenivas K. Awareness of cervical cancer and papsmear and its utilization among health care workers in medical college, Kozhikode. J Evid Based Med Health 2014;1:12-7.
Isa I, Gani O, McFubara K. Cervical cancer screening among female undergraduates and staff in the Niger delta region of Nigeria. Open J Obstetr Gynecol 2013;3:61-6.
Nayar R, Wilbur DC. The pap test and bethesda 2014. The reports of my demise have been greatly exaggerated. (After a quotation from mark twain). Acta Cytol 2015;59:121-32.
Ali F, Kuelker R, Wassie B. Understanding cervical cancer in the context of developing countries. Ann Trop Med Public Heal 2012;5:3-15.
Mbamara SU, Ikpeze OC, Okonkwo JE, Onyiaorah IV, Ukah CO. Knowledge, attitude and practice of cervical cancer screening among women attending gynecology clinics in a tertiary level medical care center in Southeastern Nigeria. J Reprod Med 2011;56:491-6.
Aniebue PN, Aniebue UU. Awareness and practice of cervical cancer screening among female undergraduate students in a Nigerian university. J Cancer Educ 2010;25:106-8.
Olowokere A, Ojo M. Cervical cancer screening knowledge and utilisation among rural women in Ife East local government area of Osun State in Nigeria. Afr J Nurs Midwifery 2014;16:145-57.
Idowu A, Olowookere SA, Fagbemi AT, Ogunlaja OA. Determinants of cervical cancer screening uptake among women in Ilorin, North Central Nigeria: A Community-based study. J Cancer Epidemiol 2016;2016:6469240.
Arrossi S, Ramos S, Paolino M, Sankaranarayanan R. Social inequality in pap smear coverage: Identifying under-users of cervical cancer screening in Argentina. Reprod Health Matters 2008;16:50-8.
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;2014:950534.
Hawkins NA, Cooper CP, Saraiya M, Gelb CA, Polonec L. Why the pap test? Awareness and use of the pap test among women in the United States. J Womens Health (Larchmt) 2011;20:511-5.
Lee FH, Wang HH. The utilization of pap test services of women: A nationwide study in Taiwan. Cancer Nurs 2011;34:464-9.
Udigwe GO. Knowledge, attitude and practice of cervical cancer screening (pap smear) among female nurses in Nnewi, South Eastern Nigeria. Niger J Clin Pract 2006;9:40-3.
] [Full text]
Adeleke N, Komolafe J. Knowledge, attitude and practice of cervical cancer screening among women of reproductive age group in Osogbo, South Western Nigeria. Sex Heal Matters 2007;8:70-3.
Kolawole O, Ogah J, Alabi O, Suleiman M, Amuda O, Kolawole F, et al.
Utilization of human papillomavirus DNA detection for cervical cancer screening in women presenting with abnormal cytology in Lokoja, Nigeria. Jundishapur J Microbiol 2015;8:e22620.
Bukar M, Mayun A, Musa A. Review of papanicolaou smears in Maiduguri - A 15-year study. BOMJ 2007;4:1-4.
Agaba PA, Thacher TD, Ekwempu CC, Idoko JA. Cervical dysplasia in Nigerian women infected with HIV. Int J Gynaecol Obstet 2009;107:99-102.
Steven W, Susan M. Sexually transmitted diseases and pelvic infections. In: Alan H, Lauren N, editors. Current Obstetrics and Gynaecologic Diagnosis and Treatment. 9th
ed. USA: McGraw-Hill Companies; 2003. p. 716-50.
[Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6]