Knowledge, awareness and attitudes about cervical cancer among women attending or not an HIV treatment center in Lao PDR

Cervical cancer is the second most common cancer in women worldwide, with over 90% of cases occurring in developing countries [1]. A persistent infection with a high risk oncogenic Human papillomavirus (HR-HPV) is involved in almost all cases [2]. HPV infection is very common in young women with early sexual activity, with a peak before 25 years, usually without clinical consequence [3]. In nearly 10% of cases, this infection persists and is associated after 5 to 10 years with lesions that may regress, remain stable or progress to a higher grade and invasive cancer. Evolution of cervical intraepithelial neoplasia (CIN) to invasive cancer is slow, about 10 to 20 years for an immunocompetent woman [4]. This slow progression allows an effective secondary prevention based on screening and treatment of precancerous lesions, using cervical cytological testing according Papanicolaou (Pap smear or Pap test), visual inspection of the cervix with 3–5% acetic acid (VIA), or more recently HPV DNA testing.

Immunosuppression, especially due to human immunodeficiency virus (HIV) infection, is a predisposing factor for persistent infection with HR-HPV [5] and the development of squamous intraepithelial lesions (SIL) [6]. High HIV viral loads and low CD4 counts are associated with a higher risk of HR-HPV infection and cervical abnormalities [7]. The risk of recurrence or progression of cervical lesions is 4–5 times higher in women living with HIV [8]. Infection with one of the 15 HR-HPV genotypes is significantly more common in HIV-infected women [9], while the distribution of low-risk oncogenic HPV is not affected by HIV status [10]. This reflects a higher propensity of HR-HPV in determining persistent infections [11].

Before the era of antiretroviral therapy, the life expectancy of HIV-infected women was too short for a systematic cervical cancer screening program to demonstrate effectiveness [12]. Today, despite highly active antiretroviral therapy (HAART) guided by CD4 count, the probability of developing invasive cervical cancer remains high and stable in this population at risk [13, 14]. Thus, the follow-up of women on antiretroviral therapy offers an opportunity for cervical cancer screening in resource-poor countries [15, 16]. A prospective study with a follow-up over 10 years on a cohort of 1760 HIV-infected and 472 non HIV-infected women showed that HIV-positive women who benefitted from regular screening had no greater risk of developing invasive cancer than HIV-negative women [17].

Laos has a female population of 1.79 million aged 15 and older. Cervical cancer is the most common cancer in women with a 15.8 per 100,000 estimated crude incidence. It is also the second leading cause of cancer death in women, but the primary cause between 15 and 44 years [18]. As in most low-income countries, there are no national screening and prevention programs for cervical cancer in Lao PDR and awareness of women is still very low.

The prevalence of HIV infection in Lao PDR is relatively low compared to neighboring countries, around 0.2% among adults aged 15–49 in the general population. In 2011, the number of women living with HIV was estimated at 5,263 and 50.9% of eligible women were receiving HAART under the National HIV/AIDS Program supported by the Global Fund [19]. Patients are followed in seven treatment centers, two in the capital of Vientiane, the other five in the provinces of Luang Prabang, Savannakhet, Luang Namtha, Bokeo and Pakse. There is currently no routine screening program for cervical cancer in women living with HIV in Laos. As the primary prevention of cervical cancer by vaccination is not effective in women already infected by HPV, the only recourse is the secondary prevention through early detection and treatment of SIL [13]. Attending HIV treatment centers is an opportunity to educate women about the risks and the value of cytological screening. The aim of this study was to determine the knowledge and awareness of Lao women about cervical cancer and to evaluate the impact of medical care for HIV-infected women on their risk awareness and prevention behaviors.

The theoretical sample size of 640 women was achieved in the three sites: 434 in Savannakhet (67.8%), 146 in Vientiane (22.8%) and 60 in Luang Prabang (9.4%). Only three women refused the interview. At each site, 50% of recruited women were cases and 50% were matched controls.

Early detection of pre-cancerous lesions is universally recognized as the most effective method of preventing cervical cancer. However low-income countries, where this cancer has the highest incidence, still face many challenges to establish national prevention programs [21]. Thus in Laos the screening coverage for women aged 18 to 69 years was estimated at 2.2%, 5.2% in urban areas and 1.4% in rural areas [18]. The level of women’s knowledge about risk factors and prevention of cervical cancer is a major determinant to undergo screening tests [22]. This survey is the first one conducted among Lao women aged 25 to 65 on knowledge, awareness and attitude about cervical cancer. It has been conducted in three different regions of the country and involved a representative sample of the female population living with HIV and a matched control group.

The first result of this study is that the general level of knowledge of the women interviewed is very poor, most being unable to mention any STI, never having heard of HPV and knowing no way to prevent cervical cancer. Knowledge mean scores are even lower than those found in Chiang Mai, Thailand, in a survey upon 402 sex workers. This difference could be explained by the fact that Thai STI services also offer a Pap screening for exposed women [20]. The best knowledge scores were observed in women with a secondary education level and earning more than 85 US dollars per month. Similar results are found in different studies conducted in low-income countries such as Cameroon [22], Nigeria [23], Tanzania [21], and Ethiopia [24]. In addition, the civil servant status which gives access to social insurance in Laos and the residence in Vientiane capital, where access to care is easier than in the provinces, are factors independently associated with a higher level of knowledge.

Almost half of women have heard of cervical cancer and consider it as a serious and common disease in Laos. But being aware does not necessarily correspond to a correct understanding of the disease [25]. Although a large majority cites unprotected sex and multiple sex partners as main risk factors, only 6% know the causal link between HR-HPV infection and cervical cancer. This rate was 14% among sex workers in Chiang Mai [20] and reached 64% in a multicenter survey in the United States [26], but in both cases, the questionnaire offered a multiple-choice question for this item.

The other interesting aspect highlighted by the survey is that HIV infected women have a significantly higher level of knowledge than their controls, although their average level of education is lower. The same observation was made in a study conducted in the United States on 1588 women, including 71% HIV positive, showing that women living with HIV had better understanding of the prevention of cervical cancer than HIV-negative women [26]. In our survey, this difference is observed mainly on issues related to sexually transmitted nature of the infection, HIV and HPV sharing common routes of transmission. There is also evidence that women living with HIV are more likely to use condoms and to consult a gynecologist than controls.

However, knowledge about risk factors for cervical cancer, screening methods and means of prevention are similarly poor in both groups. Few women consider themselves at risk of developing cervical cancer. Although this awareness is four times higher among HIV-infected women (35.9%) than among controls (8.4%), it does not lead to a greater practice of smear screening. Indeed, only 5.6% of HIV infected women had undergone a Pap test. A similar proportion (5%) was found in a study conducted among 300 women attending an HIV treatment center in Lagos, Nigeria, in the absence of national program for cervical cancer screening [27]. In addition, half of HIV-infected women in our study had a CD4 count below 200/mm³. This immune deficiency is associated with an increased risk of cervical dysplasia, but has also been identified as a risk factor for non-adherence to Pap smear program in a US survey [28].

It is noteworthy that the absence of symptoms was the reason given by one third of women and 46% of women infected with HIV for not performing testing. The same reason, advanced by 67% of sex workers in a study in Thailand, reflects a total ignorance of the natural history of cervical cancer and the principle of Pap screening, hence the need to strengthen the education of these highly exposed women [20].

The finding that nearly 90% of women in both groups hope national recommendations for vaccination against HPV and would agree to receive it should be interpreted with caution. This wish ignores that vaccination is only for girls who have not started their sexual life, while commercial vaccines do not protect against all types of HPV circulating in Southeast Asia [29].

Health personnel represent the main source of information for women living with HIV, before media and family or friends entourage. Regular attendance of HIV treatment centers has an obvious impact on the awareness of the risk of cervical cancer, but it still has no effect on screening behavior. Several reasons could be advanced. First, physicians responsible for monitoring and treatment of HIV patients do not have sufficient training to counsel their patients on the prevention of cervical cancer. A survey conducted in Karachi, Pakistan, amongst interns and nursing staff in tertiary care hospitals showed that only 40% knew the Pap smear as a screening tool for cervical cancer [30]. Second, the HIV post-test counseling and the therapeutic monitoring are not used to discuss the screening of cervical cancer. As in many low-income countries, this screening is not part of the routine management of HIV-infected women and health practitioners in HIV treatment centers do not receive proper training [27]. Third, the screening capacities in the Lao health system do not yet allow responding to a systematic demand for all women at risk. In addition, the cost of Pap smear, around 10 U.S. dollars, is a deterrent for a majority of women who do not have social insurance.

Our study has some limitations like all surveys by questionnaire covering information about private life. Response biases through default of sincerity are hard to avoid completely. Regarding the cases, it was not possible to determine the anteriority and regularity of consultations in HIV treatment centers. In addition, the HIV-negative status of controls could not be confirmed, this position being assumed on the non-attendance of HIV treatment centers.

The main result of this survey is the highlight of a wide ignorance on cervical cancer and its prevention amongst Lao women. It urges to implement information campaigns on a national scale specifically targeting women aged 25 to 65. This health education must take into account the ability to understand and the cultural characteristics of women. It is necessary to improve the communication skills to effectively convey prevention messages to women less educated [31]. This is the case of women belonging to various ethnic minorities in Southeast Asia, who also accumulate a large number of risk factors for cervical cancer as young age of marriage, early sexual activity and a high number of pregnancies [32]. The sessions should ensure not to stigmatize less educated women by exposing their ignorance [26]. Trainers should also avoid causing cancer anxiety among women as observed after the launch of an awareness and screening program In Khon Kaen, Thailand [33].

However, even well-conducted, an health education campaign will remain ineffective if the means of secondary prevention are lacking. Counseling and screening for cervical cancer should be included in the National HIV/AIDS programs [34] and implemented in all HIV treatment centers [27]. Knowing the high prevalence of SIL in HIV-infected women, the screening cannot be targeted on the basis of clinical considerations [35] but has to become routine from the age of 25 years. Where cytological screening is not available, it would be relevant to integrate low cost rapid testing at such as VIA, allowing immediate treatment with cryotherapy within a single “see-and-treat” visit. Then, when the screening service is implemented, it can be extended to all women, regardless of their HIV status [36].

Given the screening tools for cervical cancer currently available (cytology, VIA, HPV DNA), it is up to each country to determine, according to its capacities, the most cost-effective strategy for women living with HIV [37]. In Lao PDR, further studies will determine the screening policy best adapted to the scarcity of resources in view of an increasing incidence of cervical cancer.

Dying from cervical cancer is not a fatality in the karma of Lao women whose vulnerability is primarily due to their ignorance of the HR-HPV infection and its consequences. Despite they are significantly more aware, women living with HIV who bear additional risk of cervical cancer, still have a very poor understanding of the means to prevent it. They should be better informed by the health personnel and be offered a more systematic access to testing.

The implementation of routine screening for cervical cancer in HIV treatment centers would be a significant first step toward a national prevention program aiming at the elimination of a deadly but preventable cancer.