Willingness and acceptability of cervical cancer screening among HIV positive Nigerian women

Each year about half a million women develop invasive cancer of the uterine cervix, with more than 80% occurring in low income countries [1, 2]. A majority of the cases presents in late stages when available treatments are ineffective [1, 3]. The scenario is entirely different in high-income countries where cervical cancer has almost been eliminated as a result of efficient cervical cancer prevention programmes [1, 4].

In sub Saharan African countries where cervical cancer is endemic; HIV infection has become one of the leading causes of death in women [5], making the interactions between the diseases a major public health challenge [6]. The risk of developing cervical cancer and increased aggressiveness of existing cervical cancer has been reported in HIV infected women [7, 8]. Integrating cervical cancer prevention within HIV care services will not only decrease the morbidity and mortality associated with invasive cervical cancer but will also improve HIV treatment outcomes [5, 7, 8]. Investigators in Zambia in a report of the evaluation of the success of their integration of cervical cancer prevention services into existing HIV care services concluded that the model be adopted as an implementation platform low-cost cervical cancer prevention [9].

The new Nigerian National HIV treatment guidelines recognizing the potential benefit of cervical cancer prevention in HIV infected women, recommended the introduction of cervical cancer screening within HIV programmes as a standard of care [10]. Unfortunately, this important recommendation is not yet operational in most HIV clinics, either as a result of lack of will to do so or for the fear of possible disruption of the successful HIV services [1, 8, 11, 12]. The latter reason is not backed by scientific evidence, as the only published study from Nigeria on the subject in women of known HIV positive status showed a 96.0% ‘willingness to screen’ in future [13]. However this study was among women who have just completed posttest counseling and not yet enrolled into HIV care, making it difficult to use the information to extrapolate what the situation would be in HIV care and treatment setting. In addition, varying refusal rates have been reported from other high HIV prevalent countries ranging from 12-87% [14‐17]. Determining the cervical cancer screening refusal rates among HIV positive Nigerians already in HIV care is therefore necessary as it will not only be useful for the refinement of programmes but as an advocacy tool.

This study was therefore conducted to determine the acceptability of cervical cancer screening among HIV infected women using a sample population that is sufficiently powered to make generalization possible. In addition, the predictors of acceptance of cervical cancer screening among these women were also determined. Information obtained will be used to fine-tune the integration of cervical cancer screening process, which is ongoing in our HIV treatment centre and hopefully in similar clinics in Nigeria and elsewhere.

A total 1675 women were invited to participate in the study; of which 1558 accepted and received the questionnaire. Forty-one of these were either not returned or returned uncompleted (response rate of 90.6%; 1517).

This study showed a relatively high cervical cancer screening acceptance rate of 79.8% despite a moderate level of awareness of cervical cancer and it’s testing among the HIV positive women. Having a tertiary education, no living child, recent HIV diagnosis and awareness of cervical cancer were found to be associated with acceptance of cervical cancer screening. The level of awareness of cervical cancer as a disease (56.2%) and its testing (34.5%) among the respondents in this study though similar to findings from some previous studies [12, 19, 20] is lower than the finding in two recent studies conducted in our environment in 2009 and 2011 [21, 22]. One would have expected that the present study being among a group at risk for cervical cancer, that the awareness level would have been much higher. Secondly, as our study was conducted after the two most recent studies [21, 22], we were expecting at least a modest increase on awareness level due to the introduction of cervical cancer programme by the Government of Nigeria. A plausible reason for the lower awareness in this study could be the lower educational attainment of the respondent in this study compared to the studies by Bukar et al [21] and Dim et al. [22]. Supporting the above assertion of the positive role of educational attainment to cervical cancer awareness and test uptake is the finding in this study in which women with tertiary education were 1.4 times likely to take the test than women with lower qualification. The finding also underscores the importance of education in increasing cervical cancer awareness and screening uptake. A more intensified health education on cervical cancer and testing should be introduced in our programme and other HIV programmes in other to increase the awareness of cervical cancer and screening among these at risk group. In addition, the abysmally low “ever tested for cervical cancer” response (9.4%) in this study confirms the poor state of cervical cancer prevention and control in Nigeria. This is one of the reasons for the unacceptable morbidity and mortality associated with cervical cancer in Nigeria.

Puzzling, however in this study is the obvious disconnect between low awareness of cervical cancer and screening, high- low self-risk assessment of self to have cervical cancer (68.2%) and the high test acceptance rate (79.8%) among the respondents when compared to the acceptance rate of 44.0% reported by McKenzie et al. among HIV positive Kenyan women [23]. Although the Kenyan study restricted their enrollment to only women aged 30–39 years compared to this study with no age restriction, the main reason may be the almost absolute trust and relationship that exists between HIV positive clients and their primary Physician. The daily counseling and health talk by Counselors and Nurses obviously has a positive role in the high rate. To further strengthen the cervical cancer prevention programme, identification of the reason for the high rate of 79.8% among our cohort calls for an in-depth study using qualitative research methodology.

The present study apart from determining the level of awareness and acceptability of cervical cancer screening in future, determined the risk factors associated with future cervical cancer test uptake with the aim of using the information as counseling and advocacy tool. Awareness of cervical cancer screening and testing was found to be independently associated with the acceptance of cervical cancer screening. Respondent who were aware of cervical cancer as a disease were 1.5 times likely to accept the screening than those who are not aware. With awareness, one is likely to know the benefits of the test and thus opts for it. Awareness and education has been shown to improve the health seeking behaviour of individuals as it relates to uptake of cervical cancer services including testing [21‐24]. The finding of respondents with tertiary education being 1.4 times likely to take the test compared to their peers with lower educational attainment support the above assertion. Educational attainment has been shown to be associated with acceptance of reproductive services and this is not only linked to women’s empowerment of making decision but ability to pay for these services without recourse to their partners [22]. Education is also linked with patient's self-perception of cervical cancer and understanding health education and counseling that goes on with it [21].

Another surprise finding in this study is that women who are relatively new in our programme are almost 2 times more likely to accept screening than women who have been in the programme for a longer time. Though the other previous studies did not evaluate this variable, making it difficult for comparison, evidence has shown that health seeking behaviour of individuals are better during symptomatic illness than if there is no symptom [25]. Also as opportunistic illness disappears and quality of life improves with antiretroviral therapy, other life events become more important than performance of test that the usefulness is not immediately obvious. Health education and counseling among HIV positives should therefore increase rather than decrease as the client’s health get better. The cervical cancer test acceptance in this study was found to be 1.5 times higher in respondent who do not have any living child compared to their peers with living children. The higher acceptance rate among the respondents with no living children may be due to their expected better knowledge as a result of their higher educational attainment. It is therefore expected that well-educated and knowledgeable persons will opt for a healthier life style of cervical cancer screening.

In as much as one may be tempted to accept the acceptance rate of 79.8% as good, looking at the other side of the flip- a refusal rate of 20.2% is unacceptably high especially for a lethal illness among a group of person at increased risk for the disease. If we must reduce the morbidity and mortality associated with cervical cancer, we should reduce the refusal rate to single digit if not to 0%. With the reduction of refusal rate in mind, we determined the reasons for test refusal among the respondents. The anticipated cost of testing (35.2%), religious denial (14.0%), need to obtain partners’ permission (12.4%) and long waiting time (12.7%) were found to be main reasons for non-acceptance of the test (see Table 4). It is rather surprising that respondents attributed cost as the major reason for their refusal to take the test, as cervical cancer screening is free at the centre. The obvious explanation might be that either they are unaware that it is free just like other HIV services or the cost they referred to may be cost related to transportation and loss of revenue as a result of having to spend almost a whole day at the clinic. Supporting the last reason is the fact that long waiting time was also a common reason for refusal. While transport cost can be reduced by taking services closer to client homes, it could also lead to decentralization and reduction in waiting time. Tasks shifting is the ultimate strategy to solving the challenge of long waiting time at the clinic. Evidence has consistently shown that delegation of tasks, whether from doctors to non-physician health workers especially the midwives can lead to improvement in access, coverage and quality of health services at comparable or lower cost than traditional delivery models [14, 15, 26]. In addition, it will reduce the workload on the physicians who are already overwhelmed from providing HIV services. We have successfully task shifted some HIV services to other health care workers and thus task shifting cervical cancer screening will build on the existing task shifting model. In addition, scheduling the cervical cancer screening during routine HIV clinic consults and drug refill will ensure that all the women who want to be tested do not spend extra days and time accessing this service. This will ultimately increase the acceptance rate. The other reasons for refusal ‘need partner’s permission’ and religious denials should be addressed urgently. The government through advocacy and possibly legislation needs to urgently address the encroachment of the religious miscreants into health without providing health infrastructure like the traditional mission hospitals. This encroachment has dire consequences as the poor and vulnerable groups now believe these men to a higher extent than the health care workers [16]. It is therefore not a surprise finding in this study that the second most common reason for refusal of the test was related to client’s religious belief and teaching. Some clients think that they cannot actually have cervical cancer because of their religious belief. This belief is as a result of activities of some religious leaders that diseases are only from the devil and children of God do not have diseases [16, 17].

Low status of women and lack of autonomy in taking decisions should be seriously addressed. The current situation where a significant number of women cannot take decision whether to participate in a lifesaving test as a result of sociocultural and religious impediment is regrettable. Government of Nigerian and Ministry of Women Affairs in particular should focus on it and bring it to the front burner.

A possible limitation of the study was possible biased answers from the patient to please researchers who are their primary care provider. This could have overestimated the acceptance rate of cervical cancer test. We tried to eliminate getting bias answers by only administering the questionnaire to the patients after they had completed their routine HIV care for the day. In addition the questionnaire and informed consent process were administered by peer counselors who are HIV positives and members of the clinic support group.

Finally, it is important to state that educating women on the importance of cervical cancer screening and providing cervical cancer screening services is just not enough. Even more important is the provision of accessible and affordable treatment services. Government of Nigeria at all levels are urged not stop at creating awareness and screening services, but endavour to provide affordable and accessible treatment services.

The study shows that HIV positive women in our centre are willing to be screened for cervical cancer and thus service integration will only strengthen rather than disrupt the existing HIV services. The refusals as a result of anticipated cost, long waiting time and spousal approval need to be urgently addressed through advocacy and public enlightenment.