Background: Community-based cervical screening based on the single visit approach using the visual inspection approach (VIA) and treatment with cryotherapy is the most appropriate method in limited resource settings in the short- to medium-term for the control of cervical cancer. Aim: The study is aimed at assessing the service providers understanding and perception of community-based cervical screening. Materials and Methods: A cross-sectional study of 31 health workers providing cervical screening services in Ogun State, Nigeria, using closed and open ended questions. Results: There was a huge turnover of health workers who had been involved in cervical screening. Over 90% of the health workers opined that screening should commenced before the age of 25 years. Their opinion of the recommended screening interval for cervical cancer varied; with 54.8%, 16.1%, and 29.0% giving 3, 2 years, and 1 year, respectively. The VIA is the most recommended screening test by the health workers (74.2%). The majority of health workers (87.1%) felt that the logistic and technical support provided for the cervical screening program was not adequate. Cervical cancer screening is thought to be of low priority within the health system by 45.2% of the respondents while 32.3% think that it is of moderate priority. The majority of the health workers (90.3%) said that the health authority in their local government do not budget funds for cervical cancer prevention. Conclusion: The service providers perceive the need for an urgent improvement in the community-based cervical screening through awareness creation, reduction in health worker turnover, and support and integration of cervical screening services.
Keywords: Cervical screening, community, health workers, perception, understanding
Globally, more than 520,000 new cases of cervical cancer are diagnosed annually with about 85% of these cases in developing countries.  In developed countries, the incidence of cervical cancer has declined by over 70% in the last 50 years due to accessible organized cervical cancer screening using the Papanicolaou smear and treatment of pre-cancers.  The cervical cancer mortality in the United States has also decreased by 70% over the past five decades following the introduction of pap smear.  Similarly, in Finland, the incidence of cervical cancer reduced by more than 80% following the introduction of an organized cytology-based screening program. 
The successes reported in developed countries have not been replicated in sub-Saharan African, where cervical cancer remains the commonest cause of cancer deaths and accounts for over a fifth of all cancers in women.  It is estimated that between 60% and 75% of women in sub-Saharan Africa who develop cervical cancer live in rural areas and have no access to cervical screening.  It is possible that the circumstances in these low resource settings with widespread poverty, weak health infrastructure, and other basic challenges make it impossible for organized cervical cancer screening based on Pap smear to be successful. Other possible reasons include high level of competing health needs, wide spread poverty, and inappropriate health seeking behavior.  There was therefore a need to reevaluate the use of cytology as the primary tool for cervical cancer screening in limited resource settings.
Nigeria has a population of 40.43 million women aged 15 years and older who are at risk of developing cervical cancer. Current estimates indicate that every year 14,550 women are diagnosed with cervical cancer and 9,659 die from the disease. Cervical cancer ranks as the second most frequent cancer among women in Nigeria, and the second most frequent cancer among women between 15 and 44 years of age. About 23.7% of women in the general population are estimated to harbor cervical HPV infection at a given time, and over 90% of invasive cervical cancers are attributed to HPVs 16 or 18. It is Projected that in 2025, there will be 22,915 new cervical cancer cases and 15,251 cervical cancer deaths in Nigeria. 
Cervical cancer prevention worldwide is based on screening women using conventional cytology (Pap smear). Pap smear screening was developed in 1928 and named after the inventor, Dr. George Papanicolaou.  Pap smear programs, also known as cytological screening programs, have achieved impressive results in reducing cervical cancer incidence and mortality in some developed countries. Indeed, it has been estimated that cervical cancer incidence can be reduced by as much as 90% where screening quality and coverage are high.  For example, in Finland, a national cervical cancer screening program that was launched in 1963 decreased the cervical cancer rate to 5.5 cases per 100,000 women, a rate that is among the lowest in the world.  In contrast to developing countries, where about 80% of all new cases exist, it has been estimated that only 5% of women have had a Pap smear in the last 5 years.  Pap smear is a multistage process that involves sampling cells from the transitional zone of the cervix using either a wooden spatula or a brush. The cells are smeared on a glass slide and appropriately fixed while the slide is sent to a trained cytopathologist for review and detection of abnormality. This multistage process can take several weeks before the results are available to the client, although in well-organized programs results can be available sooner. A promising cytology-based method is the liquid-based cytology (LBC) which is more sensitive (94.4%) than pap smears  and has a potential to reduce the number of visits by clients for unsatisfactory smears and in addition provides specimen for HPV DNA testing. LBC is, however, more expensive than the Pap smear and requires technical laboratory support for successful implementation. This drawback is an important challenge to its widespread use in limited resource settings.
Various studies have shown different degrees of sensitivity and specificity for Pap smear when conducted at different settings. In a study conducted at Kenya, Pap smear had a sensitivity and specificity of 83% and 94.6%, respectively.  Another study in India, pap smear had a sensitivity and specificity of 53.7% and 50%, respectively,  while in another study carried out in rural Peru, Pap smear had a sensitivity and specificity of 26% and 99%, respectively.  Hence, clients often require more than one smear for a reliable diagnosis to be made before planning for treatment of premalignant lesions detected. This affects client compliance to screening programs especially because premalignant lesions are asymptomatic.
Even where screening coverage is high, the non-detection and treatment of premalignant lesions defeat the overall objective of reducing new cases of cervical cancer. Conventional Pap smear screening is therefore not the ideal technology of choice for a successful population-based screening program in Nigeria, a developing country.
In recent times, the visual inspection approach (VIA) using either 3-5% acetic acid or Lugol’s iodine solution to stain the cervix has been promoted used for cervical cancer screening programs in developing countries. Visual inspection with acetic acid is a simple painless screening procedure that takes about 5 min to perform. The client is counseled on the procedure and an informed consent is obtained. With the client placed in a lithotomy position, a pelvic examination is done, and a 3-5% acetic acid or vinegar solution is applied with a swab on stick within the transitional zone of her uterine cervix and result read after about a minute. The result could be normal if there is no color change or positive if a dense white color is noted within the area of application of the 3-5% acetic acid. The VIA have a specificity and sensitivity of 73.3% and 80.0%, respectively. , This is comparable to rates found for conventional pap smears. The benefit of the visual approach over Pap smear is that the results are immediate and as a result treatment could be offered on the spot for precancerous lesions. The single visit approach (SVA) involves offering cervical screening with the visual inspection method using either 3-5% acetic acid or Lugol’s iodine and treatment offered to clients with noted precancerous lesions. The treatment offered an abnormal VIA screening is either an excision treatment or an ablative method using cryotherapy. Cryotherapy is a painless procedure which takes about 15-20 min to perform; it is relatively inexpensive compared to other treatment modalities and is effective for premalignant lesions. The VIA can be performed by lower cadres of health personnel, does not require high tech expensive technology and infrastructure to perform, is very affordable, and provides almost the same result as the Pap smear used in developed nations. Besides, the health care providers can be trained within 1-2 weeks.  In addition, it is has been observed in some studies that the VIA reduces the percentage of women lost to follow up and the need for multiple visits to the health facility.  However, the VIA is best suited for women whose transformation zone is still visible in the ecto-cervix during speculum examination. Hence, its use may be limited in screening postmenopausal women. 
The HPV DNA test is more sensitive than Pap smear in detecting high grade dysplasia in older women. , The direct detection of HPV in cervical specimen may therefore offer an alternative or complement to population-based cytological screening. The advantages of HPV DNA testing over cytology are that it does not require the same level of technical expertise as cervical cytology; it is amenable to large-scale population-based screening and identifies women with current disease and those at risk of developing the disease over the next 2-3 years.  However, HPV DNA testing is more expensive and may not be readily available or accessible in limited resource settings. The cost of HPV DNA testing should reduce in future and the need for its use in limited resource settings in cervical cancer screening programmes may become more compelling.
In view of the challenges associated with ensuring high-quality cytology-based services in limited resource setting, and the high cost of conducting HPV DNA screening, an organized VIA approach is a useful alternative to the conventional cytology and HPV DNA testing in screening for cervical cancer. It offers a comparatively cheaper screening platform with minimal manpower requirements. The problem of “loss to follow up” associated with cytology-based screening is avoided with a single visit “screen and treat” model, thereby offering treatment for screen-positive persons. However, there is a role for cytology-based screening in focal communities where there is availability of the required man power and a motivated client base. This SVA using VIA and treatment with cryotherapy is the most appropriate in limited resource settings in the short- to medium-term pending the increased accessibility and affordability of newer techniques such as HPV DNA testing. 
Between 2005 and 2009, the World Health Organization supported a study of the effectiveness and acceptability of VIA and Cryotherapy in six African countries namely Madagascar, Malawi, Nigeria, Tanzania, Uganda, and Zambia. The project was structured and implemented in two phases; an initial local demonstration which was followed by a national scale-up programme. The Nigerian project site for the WHO multicenter study was based in the Ogun State, one of 36 States in the Nigerian federation. A total of 100 health care workers in 49 health facilities in Ogun State were trained and equipped to undertake the VIA in their community settings. Women requiring cryotherapy were referred to the project headquarters (Centre for Research in Reproductive Health, Sagamu) where the resources for cryotherapy were only available. 
Years into the project, there is a need to assess the community-based cervical screening in Nigeria. The focus heart of this study is to assess the project from the perspective of the health workers who are involved.
The Ogun State is entirely in the tropics. Located in the Southwest Zone of Nigeria with a total land area of 16,409.26 square kilometers, it is bounded on the West by the Benin Republic, on the South by Lagos State and the Atlantic Ocean, on the East by Ondo State, and on the North by Oyo and Osun States. It is situated between latitude 6.2° N and 7.8° N and longitude 3.0°E and 5.0°E. There are 20 local government areas and 236 political wards in the Ogun State, Nigeria. The WHO equipped 49 VIA centers in the state.
The projected population of Ogun State, Nigeria, is about 4,280,090. The population of women between the ages of 20 and 64 years was put at 921,712 with an annual growth rate of 2.8%. The projected population of women between the ages of 20 and 64 (ages with the most significant risk of cervical changes) in the Ogun State is about 1,058,184. A total of 100 health workers were trained by the WHO to give VIA services in the state.
The study design is cross-sectional.
Total sampling was adopted to reach all the 100 health care workers that were trained under the WHO project.
Self-administered questionnaires were provided to the health workers who were trained on the VIA. The questionnaire which contains both open- and close-ended questions was adapted from “Planning and Implementing a cervical cancer prevention and control programme” (a publication of the program for Appropriate Technology in Health – PATH) and standardized to suite the Research needs.
The data obtained were double-entered into using Microsoft Excel package and screened. Analysis was done using the Statistical Package for Social Sciences (SPSS) Software version 16. Data are presented in the form of frequencies and percentages. The open-ended questions were analyzed by content analysis.
Out of the 100 intended questionnaires, 40 were successfully delivered, while 31 were returned. There was a huge staff turnover making it impossible to reach the majority of trained health workers. Many had resigned and moved to other employments, some had retired while others had been transferred out of sites offering the VIA services.
A total of 5,346 women were screened for cervical cancer in the period 2007-2010 at these health facilities. Large variations were observed in the implementation of screening programmes in the various facilities. Indeed, at more than half of the health facilities, less than 2 women were screened per month on average.
The staff turnover rate was quite on the high side. A lot of the health workers who had the VIA training had either retired, resigned to seek other appointments, or have been posted to departments that has nothing to do with the subject under evaluation. Out of the 31 health workers interviewed, 15 (48.4%) of them were no longer involved with cervical cancer screening.
[Table 1] shows the knowledge and understanding of the health workers about cervical screening. The responses given by health workers about the age to initiate cervical screening was quite diverse, but generally within the risk age group for cervical cancer. Over 90% of them opined that screening should have commenced by the age of 25 years.
The responses given by health workers about the target group for cervical screening were diverse. The ages between 18 and 60 years was given by 32.3% of respondents; 19.4% said sexually active women while 12.9% each said women of child-bearing age and youth but generally within the risk age group for cervical cancer.
There was a varied response to the recommended screening interval for cervical cancer with 54.8%, 16.1%, and 29.0% giving 3, 2 years, and 1 year, respectively. The VIA is the most recommended screening test by the health workers (74.2%), while 7 of the 31 health workers (22.6%) could not remember the appropriate screening test.
A total of 67.8% of the health workers would offer either a referral or cryotherapy to a woman with positive result while 22% would not know what to do.
[Table 2] shows the perception of the health workers’ concerning the support they receive for the programme. The majority of health workers (87.1%) felt that the logistic and technical support provided for the cervical screening program was not adequate.
Cervical cancer screening is thought to be of low priority within the health system by 45.2% of the respondents while 32.3% think that it is of moderate priority. Only 22.6% place it as a high priority issue within the health system. The competing health priorities identified by the health workers in order of popularity include HIV/AIDS, malaria, tuberculosis, immunization and polio eradication, reduction of maternal and child mortality rate, family planning, and diabetes. Others are prevention of sexually transmitted infections and teenage pregnancy and sickle cell anemia. The majority of the health workers (90.3%) said that the health authority in their local government do not budget funds for cervical cancer prevention. However, two of the three health workers who said they had budgetary allocations found the resources to be appropriate.
The health workers identified certain weaknesses of the policies and guidelines for cervical cancer prevention. There is a general lack of political will and backing by governments at all tiers. Cervical screening is accorded a low priority within the health system. There is inadequate funding, lack of manpower, insufficient equipment, and other consumables for the VIA screening. Only a few centers have the necessary resources for cervical screening. The nonintegration of cervical cancer Programme into routine prevention programmes is a major weakness of the current setting. In the absence of a nationally accepted and clear-cut policy of cervical cancer prevention, the present practice may not be sustainable.
They suggested some of the following measures to address the weaknesses in policies and guidelines for cervical cancer prevention. There should be advocacy to gain political will and support of the government, policy makers, and law makers. Awareness creation on the morbidity and mortality of cervical cancer with the inclusion of cervical cancer education in school curriculum is regarded as the most important step to promoting cervical screening. There is a need for the enactment of a national policy and the creation of national prevention programme and its integration with other routine prevention programmes. There also must be a deliberate manpower development and adequate resource allocation for cervical cancer screening. Provision of free cervical screening and treatment for those who are positive that is accessible to all who require it is very important. Prioritizing cervical screening within the health sector was also recommended. There is a need for the development of a multisectoral, local, and international partnership for the prevention of cervical cancer.
There were also weaknesses in the provision of cervical cancer screening services. There is a low patient turnout due to a generally low level of awareness of cervical cancer and screening among the populace. This coupled with the fact that patients are sometimes required to pay and a lack of commitment by health personnel due to poor motivation ensure that services are not accessible to women who should have them. Others include lack of sustainability due to staff turnover, inadequacy of consumables, absence of budgetary allocation for cervical screening, shortage of skilled personnel, and follow-up problem. There is lack of hospital management and government support and shortage of fund coupled with incessant industrial action by hospital staff.
Various measures were proposed to address the weaknesses of the cervical cancer screening services. The recommendations include advocacy to gain political will and support of the local government authorities; awareness creation on the morbidity and mortality of cervical cancer and a deliberate manpower development and adequate monthly resource allocation for cervical cancer screening. Monitoring and evaluation with a view to provide ways to improve the programme is also crucial.
The health workers demonstrated a good understanding of cervical screening. They understood that cervical screening should be done routinely beginning from early adulthood till later in life. However, there was an apparent diversity in their opinion concerning the specifics. The apparent lack of a widely circulated guideline on cervical screening in Nigeria would be responsible for this. Clinical guidelines provide recommendations to assist practitioners in providing appropriate health care based on scientifically valid research. Studies show that these have significant potential to enable provider organizations to improve quality without increasing costs. [21-23] It could have been due to the fact that most of the health workers did not have continued training on cervical screening. It is widely accepted that continuous medical training tends to reinforce knowledge and improve health care delivery and health outcomes. [24-28]
There was inadequate logistic and technical support for the programme apparently and no local funding support for the program in most cases. This can be attributed to the low priority attached to cervical screening in the Nigeria health sector despite the high morbidity and mortality associated to cervical cancer in the country. This is similar to what is seen in Southern Africa where despite the fact that cervical cancer is the leading cause of cancer death among women, new research reveals that governments’ attempts to address the disease have been inadequate. There is still a lack of clear and comprehensive national cervical cancer management guidelines and policies in the region. Neither Namibia nor Zambia has comprehensive guidelines on the management of the illness. Where guidance is available, it tends to be inadequate, focusing on screening, with limited guidance about other forms of prevention or treatments.  Currently, many low- and middle-income countries have health systems that do not meet the requirements for chronic care. In recent years, many of them have invested in vertical national programmes to address HIV/AIDS, tuberculosis, and malaria to the detriment of other diseases such as cervical cancer. 
The weaknesses in the program are those that pertain to policy and guidelines which are not well disseminated and those related to service delivery. There is a low level of awareness of cervical cancer and screening among the populace. The nonintegration of cervical cancer programme into routine prevention programmes is a major weakness of the current setting. In the absence of a nationally accepted and clear-cut policy of cervical cancer prevention, the present practice may not be sustainable. Many studies in the sub-Saharan Africa and indeed developing countries have shown similar findings. [31-34]
It is therefore important to develop a robust integrated programme with well-disseminated guidelines and continuous training for health providers that plays up the importance of cervical cancer control. A deliberate measure must be put in place to address the high turnover of health personnel. It is hereby emphasized that at the heart of every cervical cancer control programme both in Nigeria and indeed the developing nations is the creation of awareness about cervical cancer and screening.
The service providers perceive the need for an urgent improvement in the community-based cervical screening. Awareness creation, funding, logistic, and technical support for the programme and integration of services are some of the issues needing attention to boost cervical screening. There must be concerted efforts to reduce the turnover of staff who have had training in and are thus involved with cervical screening.
The authors acknowledge Mrs Bolanle Idowu-Ajiboye who assisted immensely during administration of questionnaires, especially in reaching the respondents.
Source of Support: None, Conflict of Interest: None
[Table 1], [Table 2]