Recommendations for cervical cancer prevention and control in Ghana : public education and human papillomavirus vaccination

1Hugh Adam Cancer Epidemiology Unit, Department of Preventive and Social Medicine, University of Otago, Dunedin, Otago, New Zealand, 2Department of Obstetrics and Gynaecology, Komfo Anokye Teaching Hospital, Kumasi, Ghana, 3Department of Medical Laboratory Sciences, School of Biomedical and Allied Health Sciences, University of Ghana, Legon, Greater Accra, Ghana, 4Department of Epidemiology and Disease Control, School of Public Health, University of Ghana, Accra, Greater Accra, Ghana, 5National Centre for Radiotherapy and Nuclear Medicine, Korle Bu Teaching Hospital, Accra, Greater Accra, Ghana, 6Department of Obstetrics and Gynaecology, Korle Bu Teaching Hospital Accra, Greater Accra, Ghana


INTRODUCTION
Cervical cancer is a significant public health issue worldwide.It is the fourth most common cancer among women with more than 85% of new cases of the disease occurring in low-and middle-incomes countries (LMICs). 1 Cervical cancer is the most common cancer among women in Ghana. 1 The incidence and mortality rates have recently been estimated in some regions. 2,3 e age standardised incidence rate (world standard population) for the Greater Accra and Ashanti regions has been estimated to be 24.5 (95% CI: 22.9-26.1)and 14.0 (95% CI: 12.9 -15.1) per 100,000, respectively. 3n Kumasi, cervical cancer account for 29.4% of all female cancers in 2012. 4cording to GLOBOCAN, 3,052 new cases and 1,556 deaths from cervical cancer were recorded in Ghana in 2012. 1 Human papillomavirus (HPV) infection has been shown to be a necessary initiator of cervical cancer but the infection progresses to cancer only in a fraction of women.Cofactors associated with disease progression are not well understood in many LMICs including Ghana.
We have conducted two studies to assess the incidence, mortality, survival rates and risk factors associated with cervical cancer in Ghana.
The first was a review of medical records of women diagnosed with cervical cancer from January 2010 to December 2013 at the Korle Bu Teaching Hospital (KBTH), Accra and the Komfo Anokye Teaching Hospital (KATH), Kumasi. 2,3,5ructured telephone interviews were also conducted for patients and relatives to gather further information on the outcome of the disease.The second study assessed the risk factors for cervical cancer in Ghana, using a hospital-based case-control study. 2 Women aged 18-95 years with newly diagnosed histologically confirmed invasive cervical cancer were eligible to be cases.They had not received treatment for the disease and had been resident in Ghana for at least 3 years.Controls were randomly selected from the same hospitals as the cases.They fulfilled all the eligibility criteria defined for the cases apart from those relating to diagnosis of cervical cancer.
A structured questionnaire was administered to the women after which a request for a cervical smear was made for the assessment of cytological abnormalities and detection of HPV DNA to establish the HPV types present.The two studies were conducted between July 2014 and May 2015.Ethical approval from the University of Otago Ethics (Health) Committee was obtained by the researchers.Additionally, the Ghana Health Service Ethical Committee and the Committee on Human Research, Publication and Ethics of the Kwame Nkrumah University of Science and Technology (KNUST) and KATH gave approval for the study.
Using the data from the review of medical records and telephone interviews, the incidence, mortality, and survival rates of women diagnosed with invasive cervical cancer were estimated.The incidence and mortality rates of cervical cancer were highest for women aged 75-79 years and decreased at older ages in our study. 2,3  three years from diagnosis, overall disease-specific survival was 39%. 5 Stage at presentation (Hazard ratio (HR) for stage IV compared with stage I was 7.8; 95% CI: 4.1-14.8)and histological type (HR for other histological types compared with squamous cell carcinoma was 1.4; 95% CI: 0.4-5.9,not statistically significant) were strong predictors of cervical cancer survival.Some forms of treatment were also associated with better survival than others.
Many known established risk factors were associated with the occurrence of cervical cancer in the casecontrol study.These included age, an increased number of pregnancies, higher parity and oral contraceptive use.

2, 6, 7
In addition, use of firewood for cooking, use of homemade sanitary towels and having a polygamous husband were associated with an increased risk of cervical cancer.][10] Knowledge of HPV and cervical cancer was very low among women with and without cervical cancer in our study. 2multi-level approach is required to address the burden of cervical cancer in Ghana.A national policy on cervical cancer tailored to the socio-economic and cultural context will need to be established if the disease is to be controlled.This approach needs to take into account the complexities of the disease, the barriers to healthcare access, the determinants of health, and the social and cultural factors that influence health.A national cervical cancer prevention and control program needs to be developed and implemented in Ghana.This should ideally include national policy development and program management structure, planning and preparation, implementation, monitoring, and evaluation. 11his national cervical cancer policy should include prevention, early detection, diagnosis and treatment, and palliative care.The World Health Organization health system framework can be used to plan the program.Additionally, the National Cancer Control Strategy for Ghana can also be a starting point. 12e aim of the current paper is to make recommendations in terms of public education and HPV vaccination for the prevention of cervical cancer.

Prevention and control of cervical cancer in Ghana Public education
Evidence from studies 2,3,[13][14][15][16] conducted in Ghana indicate that knowledge of HPV and other risk factors associated with the development of cervical cancer is limited.However, studies conducted in well-educated women reported relatively good knowledge of cervical cancer 17 but these women are generally at lower risk of cervical cancer. 2A cervical cancer educational program could be implemented as part of a national cervical cancer control program.This may be the most costeffective approach in reducing the burden of the disease. 11A mixture of systems can be used to deliver cervical cancer education program: in healthcare facilities and in the community.
There is lack of an effective curriculum, learning and teaching materials on comprehensive sexual and reproductive education in schools including cervical cancer prevention in Ghana.For this to be achieved, collaboration is needed between the Ministry of Education and Health, and the Ghana Health and Education Services.Such collaboration will need to develop a specific, structured, targeted, age-related and culturally appropriate curriculum for adolescent sexual and reproductive health 18 including cervical cancer education based on evidence from research.The development of the curriculum should ideally involve individuals with various backgrounds in research on cervical cancer and sexual health.
A review of 85 school-based sexual education programs suggested improvement in adolescent knowledge of STIs and recommended the use of curriculum-based programs in adolescent sexual and reproductive health education. 19is could be implemented in schools, communities and health facilities.The content of the curriculum needs to include all aspects of sexual and reproductive health including the causes of cervical cancer, risk factors, signs and symptoms, prevention, HPV vaccination, screening and available health services.A pilot study can be conducted to test the curriculum and make changes when necessary.Misconceptions and beliefs about cervical cancer such as a perceived lack of available treatment for the disease should be addressed if the disease is to be abated.Systematic reviews of school-based education programs in Africa have shown that significant change in adolescents' knowledge and altitude towards HIV/AIDS and other sexually transmitted infections (STIs) can be achieved. 20,21 chool-based sexual and reproductive health education is one way to help adolescents recognise risk and improve their sexual and reproductive health. 22A well-developed program including cervical cancer prevention can influence adolescents' altitude, knowledge and behaviour on sexual and reproductive health greatly. 18,23 ervical cancer education could ideally begin at primary schools (late in primary school) as enrolment at primary school is high but decreases at the junior, senior and tertiary level (Figure 1).
Recently, the Ghana Health Service launched an adolescent health service policy and strategy to provide better direction and improve the effectiveness of adolescent health intervention in Ghana 24 but an action plan for its implementation will be needed.Partnerships with young people are of great importance in designing and implementing cervical cancer prevention education programs.The involvement of young people at the onset of a sexual and reproductive education program develops trust and helps to identify some of the challenges (such as lack of a youth-friendly services) that need to be improved for adolescent health programs to be effective. 25is can build the capacity of young people in the area of advocacy and peer education.Partnerships with youth networks can also help provide training to volunteer peer educators to provide education to adolescents and women in the community using various media such as home visits, radio, television programs and theatre.
Youth networks in Ghana such as The Global Youth Action Network and the Ghana Youth Development Network, if suitable, may be able to train educators at the community and household level.
Many schools have some form of sexual and reproductive education program 26 that can be expanded to include cervical cancer prevention education.Currently, there are some forms of sexual and reproductive education programs at senior high school level.However, only a few students benefit from such education with most education programs focussing mainly or solely on human immunodeficiency virus (HIV) prevention. 26xual and reproductive education programs at senior high schools have been incorporated into courses like Management in Living and Integrated Science at the senior high school level. 26However, Management in Living is an elective course and the majority of students do not take it. 26It would be important to have a comprehensive sexual and reproductive program including cervical cancer education as a stand-alone core subject for the majority of students to benefit.This could be continued at the tertiary level with inclusion of breast and cervical screening education as part of the comprehensive sexual and reproductive education program.The establishment of clubs at schools to discuss adolescent health issues such as HPV infection and the prevention of cervical cancer will also play an important role in educating students about the disease. 27 has been shown that the most effective sexual and reproductive programs are those led by teachers, health professionals, social workers and community members. 28However, many require further training to deliver sexual and reproductive education to their students. 26his could begin at teacher training with periodic workshops for teachers out of school.This pre-service and in-service training will be important to improve the skills of teachers in delivering adolescent sexual and reproductive education.
The development of the curriculum to include cervical cancer prevention should aim at providing students with the knowledge, skills, and understanding to enhance positive attitudes towards sexuality and care for their sexual health now and in the future.
Educational information could be disseminated using a variety of media including seminars, media channels such as television, radio, newspapers, posters, roleplaying and drama, as well as interpersonal contact with healthcare professionals.
Public cervical cancer education can take place at schools, workplaces, churches, mosques, market places and durbars for good coverage to be achieved -our study 2 indicated that the majority of women preferred educational programmes at such venues.Education programs to target women in semi-urban and remote areas and those at increased risk of cervical cancer are also needed.
One of the limitations of sexual and reproductive health education in schools is the difficulty in reaching individuals out-of-school.These are the individuals who are at highest risk of developing cervical cancer. 2For individuals out of school, education programs in the community can be beneficial.Community health nurses can be trained to provide organised cervical cancer education programs in the community, do home visits and give talks at community festivals.
Men usually serve as heads of families in Ghana, and drive most decision-making, including the seeking of healthcare from mainstream healthcare providers. 29hey will need to be involved in the educational program if it is to be effective.Women's groups in the community also need to be involved in cervical cancer prevention program and community volunteers may be trained to provide education on cervical cancer prevention to their members and the wider community.The Ghana hairdressers and Beautician's Association, and the National Tailors and Dressmakers Association among other professional bodies could also be involved in cervical cancer education programs incorporated into their meetings and examinations.
Healthcare professionals could be upskilled to provide education on cervical cancer when they come into contact with women during consultation, family planning, antenatal and postnatal services.Additionally, efforts to improve the level of knowledge of HPV, risk factors, HPV vaccination and cervical screening requires increased involvement of the media and women who have survived the disease.Individuals are often strongly influenced by messages from someone living with or who has survived the disease.Additionally, the involvement of people with disability and head porter (kayayee) will potentially result in increased coverage among the at-risk groups.
Implementation by District Health Management Teams in structured manner would ensure country-wide coverage, similar to immunization programs implemented in a similar fashion.Community Health Nurses have been trained to do childhood immunization and educate mothers at child welfare clinics countrywide.A similar approach would ensure good penetration and coverage.

HPV vaccination
The implementation of a national HPV vaccination programme to vaccinate adolescent girls aged 10-14 years will need to be an integral component of the control and prevention of cervical cancer in Ghana.Results from some studies 2,30-33 support licensing of the nonavalent HPV vaccine in Ghana.][32][33] The nonavalent HPV vaccine prevents infection against nine HPV types (6, 11, 16, 18, 31, 33,  45, 52 and 58).The vaccine has been shown to be efficacious, with an overall estimated rate of prevention of 80% for precancerous lesions, and 90% and cervical cancer. 34[37][38][39] The three doses required may be an obstacle in the implementation of HPV vaccination program in Ghana, however, two doses provide similar antibody levels as the three-dose schedule. 40,41  two-dose regimen will increase HPV vaccine affordability and make for easier implementation.Because HPV vaccines are effective when given before sexual debut, the target age group should be young adolescents aged 10-14 years.Economic modelling will be important in assessing the costeffectiveness of vaccinating girls aged 10-14 years. 42system to keep track of adolescents vaccinated and those who are yet to complete their doses is essential for the programme to be monitored and reduce the risk of the same person being vaccinated on several occasions.There are also other issues which need to be considered such as maintaining the cold chain, vaccine stock, vaccine safety and the monitoring of adverse effects.Experience from childhood immunization can be relied upon.
Cost has prevented the introduction of the HPV vaccine in many LMICs.However, funding of the HPV vaccine by Global Alliance for Vaccines and immunization (GAVI) reduces the price of the vaccine (less than 5USD per dose). 43Donations from GAVI have also led to demonstration projects in some LMICs.With the current reduction of the price of HPV vaccines by GA-VI, the Government of Ghana might take the opportunity to make the vaccine available to young adolescents.GAVI has supported governments in various countries including Ghana with demonstration projects in order to build capacity and infrastructure to deliver a HPV vaccination program.
A HPV vaccine pilot program was launched in the Greater Accra, Central and Northern regions of Ghana in 2013.It has been estimated that over 33,000 primary school girls aged 10-14 were vaccinated with the quadrivalent HPV vaccine in Ghana. 44The results of this demonstration program will inform policy on HPV vaccination.The GAVI supported demonstration project is for a five-year period.However, efforts are being made by the government to extend it to ten years. 44e to low school attendance during later adolescence, particular for girls, vaccination programs in the community will be needed.The use of established immunization network such as those that deliver vaccination program to infants and a network of sexual and reproductive services such as family planning may be able to be used to deliver HPV vaccine to adolescents. 42Thus, a mixture of services might be employed in Ghana involving both HPV vaccine delivery at health facilities and outreach programs.
The HPV vaccination program could initially be rolled out in selected communities, preferably populations with characteristics associated with the highest incidence rates, and gradually increased to cover the whole country.The target age group might receive HPV vaccination at a fixed healthcare facility in the selected communities.A central location for HPV vaccination might be established for girls out of school to be immunised.Thus, both school and community based vaccination programs is essential to improve coverage of at risk groups.
Most sexual and reproductive health services are involved in providing family planning and cervical screening services to women.It will be important for HPV vaccination programs to be integrated into these services.Although the primary target group for HPV vaccination is younger than users of current sexual and reproductive health services, these services provide contact for the education for HPV vaccination when moth-ers attend health services. 42Vaccination of infants in Ghana is possible as the Expanded Program on Immunization (EPI) has maintained in place an infrastructure and logistics system.However, the safety and effectiveness of HPV vaccines in infants are unknown. 42Nevertheless, HPV vaccination might be integrated into the EPI, not to vaccinate infants, but rather adolescents aged 10-14 years.This could be followed by educating women about other vaccines that can be given at various stages of their children lives.
The integration of HPV vaccination into the Community-based Health planning and services (CHPS) program is also important.Community health nurses in CHPS compounds that provide maternal and childcare to women and adolescents could be trained to provide education on cervical cancer and also HPV vaccination.The private sector is important in the health delivery system in Ghana.It is therefore important for both private for profit and not for profit health providers to be included in cervical cancer education and HPV vaccination programs.
Because the target population for HPV vaccination is different from that of current national vaccination programs, a school-based vaccination program is likely to be the most effective strategy. 42Vaccination can be done in schools similar to the pilot project and the community to reach a high number of adolescents (aged 10-14 years).School-based HPV vaccination programs may provide new incentives for the expansion and improvement of adolescent health services. 11However, having an immunization team present at a school for several days may be resource intensive, thus, the establishment of a school health programs with a provider would be helpful. 11e school health provider can be trained to provide HPV vaccination to the target age group.Additionally, the use of schools as HPV vaccination sites and encouraging school children to bring those aged 10-14 years who have left school to the vaccination sites could be evaluated in demonstration projects. 42There are sociocultural issues which need to be considered for HPV vaccination program.Because HPV vaccines are for STIs their acceptance and marketing may be problematic.
Additionally, the stigmatisation of young women with respect to a women-only vaccination program also needs to be avoided. 42The introduction of HPV vaccination among adolescents may, therefore, be misinterpreted as an attempt to reduce fertility rates. 42,45 [48] However, this conjecture has not been supported by studies that have reported no statistically significant increase in sexual behaviour and STIs in adolescents after HPV vaccination. 49,50 lthough the acceptance of the HPV vaccine has been shown to be generally high in many countries [51][52][53][54][55] , these social concerns need to be considered if high coverage is to be achieved in Ghana.
The education of adolescents and parents is critical in reducing misconceptions about HPV vaccination.Studies are needed to assess the acceptability of the vaccine and any misconceptions among the Ghanaian population.Multiple stakeholders need to be involved at the appropriate stages of advocacy and social communication.Any attempt to implement a national HPV vaccination programme should involve clinicians, parents, teachers and other relevant stakeholders to obtain widespread support.
Training of individuals to coordinate and head the program will be required with government sponsorship.The Ghana Ministry of Health (MOH) needs to be the lead agent in coordinating the prevention and control of cervical cancer in Ghana.The establishment of a multidisciplinary team and stakeholder's advisory groups with representatives from various groups and service providers will be necessary. 11Working groups can be established to oversee the various aspect of the program.
The Department of Disease Control and Prevention, Ghana Health Service, could be a base for cervical cancer prevention and control program in Ghana.Collaboration with the Family Health division will ensure high impact and efficiency.Continued evaluation of cervical cancer education and the HPV vaccination program is likely to be necessary to enhance its effectiveness and ensure that the program achieves its objectives and reaches the target population.
Funding is a major challenge for cervical cancer prevention and control in Ghana and many other countries in Africa.Some government funds and technical support would need to be allocated for the cervical cancer prevention and control program. 11Partnership with private companies is a way of improving funding for cervical cancer control; similar to that achieved for cardiovascular disease through the establishment of the National Cardiothoracic Centre.Additionally, support from individuals, private companies, and multinational companies might be sought to complement government funding in the provision of infrastructure, logistics and human resources. 56ncentives, such as awards and tax reductions, may be introduced for the involvement of individuals, private and multinational companies for cervical cancer prevention and control. 56lunteering is also a way for students and individuals to make a positive difference for others and society, and also gain valuable experience and skills for their various careers.Volunteers could also reduce costs and improve access to preventive services for the majority of Ghanaians.Volunteers have been used in New Zealand, United Kingdom, United States of America, and other countries to improve health services. 57This can be incorporated into cervical prevention and control programs in Ghana.
Cervical cancer prevention and control needs focussed infrastructure including human resources, vaccine storage facilities, laboratories, and treatment centres which are scarce in Ghana.Training of health care workers to reduce the shortage of health professionals in Ghana is also an urgent priority for a national cervical cancer control policy to be effective. 56This might be achieved by training some health professionals such as community health nurses which is less expensive.
The provision of incentives as well as mentorship opportunities might help reduce the migration overseas of health professionals.Career opportunities for advancement and specialisation will be important.Further reward may be given to health professionals who accept posting to rural areas to address the staff shortages.All these initiatives would support a cervical cancer education and HPV vaccination program to reduce the burden of the disease in Ghana.

CONCLUSION
Cervical cancer is a very important public health issue in Ghana.There are opportunities to reduce the burden of the disease through education, HPV vaccination, screening and treatment of the disease.Achieving this requires a coordinated systematic approach from the government, private agencies, health professionals and the general population.We recommend a whole-ofgovernment approach involving all the relevant governmental agencies and other key stakeholders to develop an integrated approach for cervical cancer control and prevention in Ghana.

Figure 1
Figure 1 Recommendation for cervical cancer prevention education and HPV vaccination in Ghana.