Abstract
Background:
Cervical cancer is one of the major diseases that affect women of child bearing age. Its main cause is the human papilloma virus; although, other associated factors have been evidenced to increase its risk. Pap-smear screening and vaccination which has been shown to be successful in reducing the incidence and prevalence of the disease in developed countries, has been neglected in developing countries due to lack of knowledge, misconceptions, and cultural beliefs.
Materials and Methods:
A cross-sectional study involving only female Sub-Saharan Africa (SSA) students in a UK university setting.
Results:
One hundred and eighty-six (42%) African female students were recruited from the 442 SSA students attending one of the major Universities in the UK. Seventy-one (38.2%) of the students were aware of cervical screening, but only 20 (10.8%) reported having knowledge of cervical cancer. A small percentage of about 26.9% (50 Students) were already part of this screening program; although, 81 (43.5%) showed willingness to participate in future screening programs. More so, it was evident that student's perception was dependent on their experience of the disease (P = 000) just as their participation in screening program was dependent on their awareness level (P ≤ 0.01).
Conclusion:
Female African students from the SSA region have poor knowledge of the disease which influenced their attitude toward screening. More needs to be carried out to increase awareness and uptake of screening within the school environment as university setting provides a viable platform to promote healthy behavior.
Keywords: Awareness, cervical cancer, cervical screening, human papilloma virus, Sub-Saharan Africa, Sensibilisation, cancer du col utérin, dépistage du cancer du col utérin, virus du papillome humain, Afrique subsaharienne
Résumé
Contexte:
Le cancer du col de l’utérus est l’une des principales maladies qui touchent les femmes en âge de procréer. Sa principale cause est le virus du papillome humain; Bien que, d’autres facteurs associés ont été mis en évidence pour augmenter son risque. Le dépistage du Pap et la vaccination, qui s’est avéré efficace pour réduire l’incidence et la prévalence de la maladie dans les pays développés, a été négligé dans les pays en développement en raison du manque de connaissances, d’idées fausses et de croyances culturelles.
Matériel et Méthodes:
Une étude transversale impliquant seulement des étudiantes d’Afrique subsaharienne (SSA) dans un université britannique.
Résultats:
Cent quatre-vingt-six (42%) étudiantes africaines ont été recrutées parmi les 442 étudiants SSA fréquentant l’une des plus grandes universités du Royaume-Uni. Soixante et onze (38,2%) des étudiants étaient au courant du dépistage du cancer du col, mais seulement 20 (10,8%) ont déclaré avoir une connaissance du cancer du col de l’utérus. Un faible pourcentage d’environ 26,9% (50 étudiants)Font déjà partie de ce programme de dépistage; 81 (43,5%) se sont montrés disposés à participer à de futurs programmes de dépistage. De plus, il était évident que la perception des étudiants dépendait de leur expérience de la maladie (P = 000), tout comme leur participation au programme de dépistage dépendait de leur niveau de sensibilisation (P ≤ 0,01).
Conclusion:
Les étudiantes africaines de la région de l’Afrique subsaharienne connaissent mal la maladie et ont influencé leur attitude envers le dépistage. Davantage de mesures doivent être prises pour accroître la sensibilisation et l’adoption du dépistage dans l’environnement scolaire, car le cadre universitaire constitue une plate-forme viable pour promouvoir un comportement sain.
Introduction
One in ten women is diagnosed with cervical cancer and every 2 min, a woman dies of it globally, making it the second most commonly diagnosed gynecological cancer,[1,2]. Highest incidence of cervical cancer related death occurs among middle age women about 30–40 years. Of the 273,505 deaths recorded, 80% occurred in low and middle income countries.[3] In Sub-Saharan Africa (SSA), of the 78,897 women diagnosed with cervical cancer annually, 61,671 deaths were recorded which makes the disease one of the most prevailing cancers.[4] In Uganda, Mali, Nigeria, and Zimbabwe, cervical cancer is the second most prevailing cancer among women aged 15–44 years.[5,6] A major misconception lies in the treatment of cervical cancer which is viewed as the removal and reinsertion of the womb and believed to cause unavoidable death.[7] In SSA, cervical cancer is yet to be acknowledged as an important public health problem.[5] The low awareness of the disease in Africa which cuts across different literacy levels have been reported.[8,9,10,11,12] In Nigeria, only 22 (4.3%) among 500 attendees of a maternal and child health clinic in Lagos were found to be aware of cervical cancer disease. Over 80% of one hundred and thirty-nine patients with advanced cervical cancer said they have never heard of the disease whereas 10%–30% assumed that the symptoms they presented were related to lower genital infection, menstrual cycle, and irregular menses.[10] Only 9% of the patients knew the disease was cancer related, a condition needing urgent medical attention.[5] Poor awareness of the disease and attribution of symptoms to minor health condition led 98% of patients with advanced invasive cervical cancer to believe that their health problem was incurable.[5] Similar findings of poor awareness of cervical cancer and screening among patients have also been reported in Kenya and Tanzania.[13,14] Students have been reported to have poor knowledge of cervical cancer and screening, especially in developing countries.[5,9,15] In South Africa, the overall knowledge of cervical cancer was very poor among female university students.[9] Sexual intercourse before 18 years of age, multiple sex partners and previous history of sexually transmitted diseases (STD) were major risk factors of cervical cancer.[5] It is crucial therefore, to promote awareness of the disease among young people. Current global changes in population dynamics, with an increasing middle aged population will result in a 4-fold increase in cervical related mortality,[3] which explains the need for immediate public health action to scale up preventive services by creating more awareness and community participation among this population.
Materials and Methods
Ethical approval was obtained from the university's Research Ethics Panel in the Faculty of Medical Sciences. A semi-structured, self-administered questionnaire consisting of four sections with 22 questions was given to 186 SSA female students. The questions were aimed at examining student's knowledge, attitude, perception, and experience of cervical cancer, its risk factors and screening. Students were recruited using two approaches: Online source and convenient sampling which involved recruitment of participants in open spaces such as study lounges, libraries, and cafeterias. Students who expressed an interest to participate were first given a participant information sheet and a consent form. Self-directed web-linked questionnaire only accessible to the researcher was also generated and sent via E-mails and social media with a covering letter explicitly targeting only SSA female students. SPSS version 20 (IBM Corp. Released 2011. IBM SPSS Statistics for Windows, Version 20.0. Armonk, NY: IBM Corp) was used for data analysis. Pearson Chi-square (χ2), multiple response analysis, bivariate, and multinomial logistic regression analysis were calculated, analyzed, and interpreted.
Results
One hundred and 86 (42%) SSA female students of 442 African students in one of the university's campus completed the survey. One hundred and 53 (82%) students completed the survey online and the remaining, at university's open spaces. One hundred and five (56.5%) students were between the ages of 18 and 24 with the least percentage of 0.5% (1) between the ages of 31 and 35. About 103 (55.4%) were Nigerians with the rest percentage from Sub-Saharan countries. Black British students were excluded from the study to ensure unbiased information. One hundred and 43 (76.9%) students were currently undergoing a degree while the least percentage 2.7% (5) were currently in the doctorate level (grouped as “others” for statistical reasons). Students number of years in the UK was not explicitly stated in the study. However, it can be deduced from students’ level of education; although, this could be difficult to ascertain as some of the students might already be resident in the country as a result of academic progression of which this study did not investigate [Table 1].
Table 1.
Characteristics of participants (n=186)
| Students demographic characteristics | Number of students (%) |
|---|---|
| Age group | |
| 18-24 | 105 (56.5) |
| 25-30 | 77 (41.4) |
| 31-35 | 1 (0.5) |
| Above 35 | 3 (1.6) |
| Nationality | |
| Nigeria | 103 (55.4) |
| Ugandan | 22 (11.8) |
| Zambian | 39 (21.0) |
| Zimbabwean | 2 (1.1) |
| Ghana | 15 (8.1) |
| Rwandese | 1 (0.5) |
| Kenya | 4 (2.2) |
| Marital status | |
| Single/never married | 169 (90.9) |
| Married/living with partner | 15 (8.1) |
| Others | 2 (1.1) |
| Level of education | |
| Degree | 143 (76.9) |
| Masters | 38 (20.4) |
| Others | 5 (2.7) |
| Sexual orientation | |
| Heterosexual | 178 (95.7) |
| Homosexual | 1 (0.5) |
| Others | 7 (3.8) |
Knowledge of cervical cancer
Table 2 shows poor knowledge of cervical cancer as reported by some of the students. One hundred and twenty-seven (68.3%) had no knowledge of the disease. More so, in respect to age at risk, 74 (39.8%) students agreed that women aged 20–29 (standardized age in UK) are at a higher risk of contracting the disease, whereas forty female students (21.5%) said cervical cancer is unrelated to age. More than half of the students reported not being confident in identifying cervical cancer signs and risk factors [Table 3].
Table 2.
Knowledge of cancer and cervical cancer (n=186)
| Response | Number of students (%) |
|---|---|
| Unsure | 39 (21.0) |
| Yes | 20 (10.8) |
| No | 127 (68.3) |
Table 3.
Level of confidence (n=186)
| Students confidence level | Number of students (%) |
|---|---|
| Partially confident | 79 (42.5) |
| Not confident | 107 (57.5) |
| Confident | 0 |
Knowledge of cervical cancer risk factors
Fifty-one (27.4%) students were certain that infection with human papilloma virus (HPV) was a risk factor of cervical cancer, 99 (53.2%) viewed cigarette smoking as a major factor that fosters carcinogenesis of the cervix, 122 (65.6%) reported weak immune system as a risk factor, and 55 (29.6%) agreed that prolonged use of contraceptive pills can predispose one to cervical cancer. However, about 175 (94.1%) students viewed STD infection as a major risk factor, 47 (25.3%) reported having too many children as a risk factor while 108 (58.1%) affirmed that early marriage/sex below 18 years is a risk factor. One hundred and sixty-two (87.1%) and 114 (61.3%) students, respectively, affirmed that having multiple sex partners or having a partner with multiple sex partners puts an individual into cervical cancer high risk category, whereas 89 (47.8%) reported none/irregular Pap-smear test as a main factor that encourages cervical cancer.
The above findings were collated using a multiple response analysis to determine the total response of students on cervical cancer risk factors as shown in Table 4. Conclusively, only 102 (54.9%) students had knowledge of the disease risk factors. Table 5 shows the number and percentage of students in relation to their level of knowledge on cervical cancer risk factors. The knowledge score was used to determine the need for increased awareness within the school environment. Seventy-one (38.2%) students reported being aware of cervical screening services provided in the country. However, a greater percentage of about 45.2% (82 students) said they have no knowledge of the screening programs. It is also evident that 58 (31.2%) students who knew about cervical screening services in the UK reported being informed through social/mass media [Table 6].
Table 4.
Multiple response analysis of student’s knowledge on CCA risk factors
| CCA risk factors | Number of students (%) |
|---|---|
| Unsure | 491 (26.4) |
| Yes | 1022 (54.9) |
| No | 347 (18.7) |
| Total | 1860 (100) |
CCA=Cervical cancer
Table 5.
Student’s CCA risk factor knowledge score
| Knowledge level | Knowledge score | Number of students (%) |
|---|---|---|
| High knowledge | 8-10 | 60 (32.3) |
| Moderate knowledge | 5-7 | 84 (45.2) |
| Low knowledge | 3-4 | 25 (13.4) |
| Poor knowledge | 0-2 | 17 (9.1) |
Table 6.
Awareness of NHS CCA screening services based on student’s age
| Age group | Are you aware of the NHS CCA screening services? | |||
|---|---|---|---|---|
| Yes | No | Unsure | Total | |
| 18-24 | 52 | 33 | 20 | 105 |
| 25-30 | 16 | 50 | 11 | 77 |
| 31-35 | 1 | 0 | 0 | 1 |
| Above 35 | 2 | 1 | 0 | 3 |
| Total number and percentage of students | 71 (38.2) | 84 (45.2) | 31 (16.6) | 186 (100) |
CCA=Cervical cancer, NHS=National Health Service
Misconception
Students were asked “if sex with an uncircumcised partner was a risk factor for cervical cancer based on some cultural misconceptions. This question was asked in other to ascertain the authenticity of some misconceptions about the disease of which there was. About 99 (53.2%) students were not certain about the association of circumcision and cervical cancer [Table 7], whereas 65 (34.9%) students reported sex with uncircumcised partner as a risk factor for cervical cancer.
Table 7.
Is sex with an uncircumcised partner a risk factor for CCA?
| Responses | Number of students (%) |
|---|---|
| Unsure | 99 (53.2) |
| Yes | 65 (34.9) |
| No | 22 (11.8) |
Experience of students on cervical cancer
Most of the participants had no prior experience of cervical cancer as reported by 127 (68.3%) students [Table 8]. Experience of cervical cancer in this study refers to student's personal experience or knowledge of someone who has been exposed to cervical cancer disease.
Table 8.
Have you or your family/friends had CCA?
| Responses | Number of students (%) |
|---|---|
| Unsure | 39 (21.0) |
| Yes | 20 (10.8) |
| No | 127 (68.3) |
| Total | 186 (100) |
Perception of cervical cancer and attitude to screening programs
Seventy-seven (41.4%) students perceived cervical cancer to be a deadly disease which needs urgent attention, whereas others emphasized on the need for more awareness on screening services. Nevertheless, 109 (58.6%) students had a negative perception which viewed cervical cancer as a forbidden disease based on cultural differences [Table 9].
Table 9.
What is your perception of CCA?
| Responses | Frequency (%) |
|---|---|
| A deadly disease | 77 (41.4) |
| A forbidden disease | 109 (58.6) |
From the multinomial logistic regression analysis, it was ascertained that students who are unsure of their experience of cervical cancer compared to students who have no prior experience of the disease, are less likely to have a positive perception (odds ratio [OR] = <0.088). However, students with prior experience of cervical cancer compared to students with no prior experience, were more likely to have a positive perception (OR = >1.5). Therefore, it can be denoted that the maximum likelihood ratio (P = 0.000) of student's perception of cervical cancer was dependent on their experience of the disease.
Stigmatization
More than half of the students, 97 (52.2%) reported not being comfortable in associating with cervical cancer victims [Table 10].
Table 10.
Would you comfortably associate with someone who has CCA?
| Responses | Number of students (%) |
|---|---|
| Yes | 89 (47.8) |
| No | 97 (52.2) |
| Total | 186 (100) |
Decision to participate in screening
A small percentage of the students, 50 (26.9%) were already part of a screening program although 81 (43.5%) of the students declared their willingness to participate in screening activities [Table 11].
Table 11.
Willingness to participate in CCA screening program
| Responses | Number of students (%) |
|---|---|
| Yes | 81 (43.5) |
| No | 55 (29.6) |
| Already part of the program | 50 (26.9) |
| Total | 186 (100) |
Analysis suggests a significant co-relation between student's decision to participate in screening and perception of the disease (P = 0.000). A negative association was hypothesized between the variables. However, since the Pearson correlation value is 0.652 and is significant, the findings did not support the study hypothesis [Table 12].
Table 12.
Co-relation (bivariate analysis)
| Do you plan to participate in the CCA screening program? | What is your perception of CCA? | |
|---|---|---|
| Do you plan to participate in the CCA screening program? | ||
| Pearson correlation | 1 | 0.652** |
| Significant (two-tailed) | 0.000 | |
| n | 186 | 186 |
| What is your perception of CCA? | ||
| Pearson correlation | 0.652** | 1 |
| Significant (two-tailed) | 0.000 | |
| n | 186 | 186 |
**Correlation is significant at the 0.01 level (two-tailed). CCA=Cervical cancer
It was observed that 79 (42.5%) students that have been informed of cervical cancer (CCA), plan to participate in screening programs. Similarly, 38 (20.4%) students who were also informed refused participation, whereas 69 (37.1%) were already part of a screening program. Pearson χ2 showed a statistical significance of P ≤ 0.01 which means that the level of participation is dependent on the level of awareness. Some of the reasons students gave for nonattendance is represented in Table 13 of which 135 (72.6%) students had no reason for not participating in screening activities.
Table 13.
Reasons for nonattendance
| Reasons | Number of students (%) |
|---|---|
| I don’t have time for it | 21 (11.3) |
| The reception/GP hours are not suitable for me | 11 (5.9) |
| I am afraid the test will come out positive | 5 (2.7) |
| I don’t think it is necessary | 14 (7.5) |
| Not applicable | 135 (72.6) |
| Total | 186 (100) |
GP=General practitioner
Help seeking and attitude toward uptake of screening
It was also noted that a high percentage of the students, 106 (57.0%) students were willing to contact their general practitioner (GP) immediately they notice any sign of cervical cancer [Table 14].
Table 14.
How soon would you contact your GP if you notice a symptom?
| Responses | Number of students (%) |
|---|---|
| Immediately | 106 (57.0) |
| Wait for other symptoms | 44 (23.7) |
| Never | 36 (19.4) |
| Total | 186 (100) |
GP=General practitioner
Discussion
From the analysis of the knowledge score, it was deduced that SSA female students have poor knowledge of cervical cancer as only 20 (10.8%) students were recorded to have knowledge of the disease. This supports the findings from the previous study conducted in Africa which showed poor knowledge of cervical cancer and its risk factors among students.[16] More so, student's level of confidence in identifying cervical cancer risk factors was low as only 42.5% (79) reported being partially confident while others were not confident at all which remains an issue for concern. This implies that the need to create more awareness within the school environment cannot be over-emphasized. Some of the key factors of cervical cancer identified by students based on multiple response analysis were, HPV infection, smoking, weakened immune system, early teenage marriage, having many children (multi-gravid), vaginal bleeding, lower back pain, painful urination, and dyspareunia. These findings have been supported and evidenced by some studies to be the main key risk factors and warning signs of cervical cancer; although, it has also been noted that the presence of one or two signs does not guarantee that the individual has cervical cancer except diagnostically proven,[17,18,19] which supports why some of the students reported waiting for other symptoms before consulting their GP.
Cross tab analysis suggests that knowledge of cervical cancer risk factors influenced student's decision to participate in screening services. This was evidenced in some studies which showed that increase in acceptance and implementation of screening practices was made successful through awareness.[20,21] However, only 71 (38.2%) students were aware of the National Health Service (NHS) cervical screening services irrespective of the awareness and screening services made available to the public. A study done in Africa however, revealed the failure of screening services,[22] which could have contributed to student's lack of interest.
This study findings also suggest that students’ perception of cervical cancer influenced their association with cervical cancer diagnosed victims. About 109 (58.6%) students who had a negative perception of the disease refused association with cervical cancer victims of which majority viewed it as a forbidden sickness. A significant relationship was also found between student's perception of the disease and participation to screening which could thus, may have affected GP's consultation too. Findings from previous studies have deemed this to be a cultural thing based on misconceptions as most African culture forbids the woman of mentioning her reproductive organ to anyone, especially male health practitioners.[5,6] Some of the reasons for nonattendance to cervical screening included lack of knowledge of Pap-smear test, fear of unknown result outcome, and lack of interest in screening.[23]
The multinomial logistic regression analysis showed that both students with positive and negative perception of the disease were directly or indirectly influenced by their past experience. Peoples’ experience affect them not only financially but intellectually and psychologically which in turn affects their perception of the disease.[24]
Conclusion
The high rate of cervical cancer and screening awareness in the United Kingdom cannot be compared to countries in the SSA region therefore, it is expected that the level of information available will influence students originating from these African countries. It has been noted from this study that students have poor knowledge of the disease because they are yet to understand how vulnerable they are which explains the urgent need to enlighten students on the severity of the disease and encourage them to take up screening programs irrespective of their experience and perception. This will help decrease the trend of the disease both at the national and global level. The use of health education programs and lectures that incorporate cervical cancer and screening messages could be inculcated as part of the school curriculum and offered to all students regardless of their health status or denomination. The use of mini surveys to understand student's knowledge on the disease and screening services will help improve the school GP's screening services. Large scale studies’ exploring the uptake of screening services among all female students irrespective of their race or nationality is highly recommended.
Financial support and sponsorship
Nil.
Conflicts of interest
There are no conflicts of interest.
Acknowledgment
Special thanks to my supervisor who took her time to ensure that this project measures up to standard. My heartfelt gratitude goes to all my lecturers, colleagues, and fellow students who contributed to ensure this project was a success.
References
- 1.American Cancer Society. Cancer Facts and Figures. Atlanta, GA: American Cancer Society; 2013. [Google Scholar]
- 2.GSK. Cervical Cancer Key Facts. United Kingdom: GlaxoSmithKline; 2007. [Google Scholar]
- 3.Kerr DJ, Fiander AN. Towards Prevention of Cervical Cancer in Africa: Report from Meeting at St. Catherine's College. Oxford: 2009. [Google Scholar]
- 4.WHO. Human Papillomavirus and Cervical Cancer in the World 2007 Report. 2007 [Google Scholar]
- 5.Anorlu RI. Cervical cancer: The Sub-Saharan African perspective. Reprod Health Matters. 2008;16:41–9. doi: 10.1016/S0968-8080(08)32415-X. [DOI] [PubMed] [Google Scholar]
- 6.Nwankwo KC, Aniebue UU, Aguwa EN, Anarado AN, Agunwah E. Knowledge attitudes and practices of cervical cancer screening among urban and rural Nigerian women: A call for education and mass screening. Eur J Cancer Care (Engl) 2011;20:362–7. doi: 10.1111/j.1365-2354.2009.01175.x. [DOI] [PubMed] [Google Scholar]
- 7.McFarland DM. Cervical cancer and Pap smear screening in Botswana: Knowledge and perceptions. Int Nurs Rev. 2003;50:167–75. doi: 10.1046/j.1466-7657.2003.00195.x. [DOI] [PubMed] [Google Scholar]
- 8.Ajayi IO, Adewole IF. Knowledge and attitude of general outpatient attendants in Nigeria to cervical cancer. Cent Afr J Med. 1998;44:41–3. [PubMed] [Google Scholar]
- 9.Buga GA. Cervical cancer awareness and risk factors among female university students. East Afr Med J. 1998;75:411–6. [PubMed] [Google Scholar]
- 10.Anorlu RI, Banjo AA, Odoemhum C. Cervical cancer and cervical cancer screening: Level of awareness in women attending a primary health care facility in Lagos. Niger Postgrad Med J. 2000;70:25–8. [Google Scholar]
- 11.Walker AR, Michelow PM, Walker BF. Cervix cancer in African women in Durban, South Africa. Int J Gynaecol Obstet. 2002;79:45–6. doi: 10.1016/s0020-7292(02)00178-9. [DOI] [PubMed] [Google Scholar]
- 12.Wellensiek N, Moodley M, Moodley J, Nkwanyana N. Knowledge of cervical cancer screening and use of cervical screening facilities among women from various socioeconomic backgrounds in Durban, Kwazulu Natal, South Africa. Int J Gynecol Cancer. 2002;12:376–82. doi: 10.1046/j.1525-1438.2002.01114.x. [DOI] [PubMed] [Google Scholar]
- 13.Gichangi P, Estambale B, Bwayo J, Rogo K, Ojwang S, Opiyo A, et al. Knowledge and practice about cervical cancer and Pap smear testing among patients at Kenyatta national hospital, Nairobi, Kenya. Int J Gynecol Cancer. 2003;13:827–33. doi: 10.1111/j.1525-1438.2003.13612.x. [DOI] [PubMed] [Google Scholar]
- 14.Kidanto HL, Kilewo CD, Moshiro C. Cancer of the cervix: Knowledge and attitudes of female patients admitted at Muhimbili national hospital, Dar es Salaam. East Afr Med J. 2002;79:467–75. doi: 10.4314/eamj.v79i9.9118. [DOI] [PubMed] [Google Scholar]
- 15.Ayinde OA, Omigbodun AO. Knowledge, attitude and practices related to prevention of cancer of the cervix among female health workers in Ibadan. J Obstet Gynaecol. 2003;23:59–62. doi: 10.1080/0144361021000043272. [DOI] [PubMed] [Google Scholar]
- 16.Hoque M, Hoque E, Kader SB. Evaluation of cervical cancer screening program at a rural community of South Africa. East Afr J Public Health. 2008;5:111–6. [PubMed] [Google Scholar]
- 17.Fey MC, Beal MW. Role of human papilloma virus testing in cervical cancer prevention. J Midwifery Womens Health. 2004;49:4–13. doi: 10.1016/j.jmwh.2003.10.002. [DOI] [PubMed] [Google Scholar]
- 18.Moini J. Introduction to Pathology for the Physical Therapist Assistant. USA: Jones and Bartlett Learning; 2011. [Google Scholar]
- 19.Bayo S, Bosch FX, de Sanjosé S, Muñoz N, Combita AL, Coursaget P, et al. Risk factors of invasive cervical cancer in Mali. Int J Epidemiol. 2002;31:202–9. doi: 10.1093/ije/31.1.202. [DOI] [PubMed] [Google Scholar]
- 20.Pollack AE, Balkin M, Edouard L, Cutts F, Broutet N. WHO/UNFPA Working Group on Sexual and Reproductive Health and HPV Vaccines. Ensuring access to HPV vaccines through integrated services: A reproductive health perspective. Bull World Health Organ. 2007;85:57–63. doi: 10.2471/BLT.06.034397. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 21.De Vincenzo R, Amadio G, Ricci C, Licameli A, Ferrandina G, Capelli G, et al. Treatment of cervical cancer in Italy: Strategies and their impact on the women. Vaccine. 2009;27(Suppl 1):A39–45. doi: 10.1016/j.vaccine.2008.11.110. [DOI] [PubMed] [Google Scholar]
- 22.Leser KA, Francis SA. Mother-child communication about sexual health, HPV and cervical cancer among antenatal clinic attendees in Johannesburg, South Africa. Afr J Reprod Health. 2014;18:123–6. [PubMed] [Google Scholar]
- 23.Ezem BU. Awareness and uptake of cervical cancer screening in Owerri, South-Eastern Nigeria. Ann Afr Med. 2007;6:94–8. doi: 10.4103/1596-3519.55727. [DOI] [PubMed] [Google Scholar]
- 24.Denny L. Prevention of cervical cancer. Reprod Health Matters. 2008;16:18–31. doi: 10.1016/S0968-8080(08)32397-0. [DOI] [PubMed] [Google Scholar]