Introduction

Cervical cancer is the leading cause of cancer-related mortality among women in India [1]. In 2012, there were an estimated 122,000 cases of and 67,000 deaths from cervical cancer in India, which accounts for almost one-quarter of all cases and deaths worldwide [2, 3]. It is well documented that essentially all cases of cervical cancer are associated with infection with human papillomavirus (HPV). An estimated 7 % of women in India are infected with HPV [4]. Use of Papanicolau (Pap) smear screening and HPV vaccination are believed to significantly reduce the burden of cervical cancer [5, 6]. Unfortunately, in low and middle income countries such as India, these preventive strategies have not yet been universally implemented, and additional information on feasibility of scaling up these prevention efforts is needed.

The HPV vaccines available cover two of the most common oncogenic strains of the virus, HPV 16 and 18, which together are responsible for the majority of all invasive cervical cancer cases worldwide [7]. A study among female adolescents suggests that HPV 16 and 18 are also the most prevalent oncogenic strains in India [8]. Prior to the availability of HPV vaccination, cervical cancer screening using the Pap smear was the principal option for reducing cancer burden, and reductions in cervical cancer incidence and mortality have been attributed to increased uptake of Pap smear screening [6, 9]. More recently in India, visual inspection with acetic acid has started to gain ground as an efficacious method to reduce cervical cancer mortality in India [10]. We specifically focus on Pap smears in this study as this was the primary method of screening offered at the time that the study was conducted. Modeling of the impact of combined vaccination and screening in India found that these strategies could be effective in reducing cancer burden by as much as 63 % and could prove to be a cost-effective health strategy for the country as a whole [11].

This study focuses on the Indian state of Karnataka which is the ninth most populous state with a population of approximately 61 million, 61 % of whom live in rural areas [12]. The literacy rate in rural populations is estimated at 69 % compared to 85 % in urban areas [12]. The health care system in India is dichotomous due to the increasing economic disparities between rich and poor, rapid urbanization, and the rural-urban divide in health care systems [13]. Cervical cancer mortality rates (age-standardized) in Karnataka (16.5 per 100,000) are very similar compared to India overall (16.0 per 100,000) [1]. There is very limited information on sexual behavior and prevalence of HPV and other sexually transmitted diseases among adolescents and young women in our setting. In one cross-sectional study, the prevalence of sexual activity was found to occur in 5.5 % of adolescents aged 15–19 years [14]. In another study of 890 women aged 20–70 years, the incidence of HPV infection was 11.7 % [15]. The purpose of this study is to assess the knowledge, acceptability, attitudes, and feasibility concerning HPV and cervical cancer among adult women in Dakshina Kannada district of the southern state of Karnataka, India.

Methods

The study was approved by the Wake Forest School of Medicine Institutional Review Board and the ethics committee of the K.S. Hedge Medical Academy (KSHEMA). Participants were selected by convenience sampling from family practice and obstetrics and gynecology clinics as well as from postnatal wards within the hospital at KSHEMA in Deralakatte, Karnataka, India between June and August 2008. All women between the ages of 18 and 44 were eligible for inclusion. Women who had previously had an abnormal pap or cervical cancer were not specifically excluded. Participants who were enrolled gave their informed consent and completed a 92-item questionnaire concerning HPV and cervical cancer-related topics. Women responded with either “agree/yes,” “disagree/no,” or “I do not know” to all of the questions asked, except where otherwise specified.

The first section of the survey collected demographic information. The second section explored the participant’s knowledge regarding HPV-related topics. The third and fourth sections of the questionnaire investigated the attitudes and concerns that participants had toward the idea of HPV and HPV vaccination. The final section examined the feasibility of vaccine or screening implementation. Survey questions were selected based on a literature review of similar studies that included measurements of interest. The initial questions selected were first pilot tested in English. Adjustments were made to the questionnaire and then translated in the local language, Kannada. This version was again pilot tested for appropriateness and understanding among 20 randomly chosen women in Karnataka, and minor changes were made to facilitate better comprehension of the survey prior to implementation.

Statistical analysis was conducted using STATA 9.2 (StataCorp, College Station, TX, USA). Statistical comparisons were calculated using chi-square test for categorical variables. Knowledge and attitude factors were investigated for correlation with two primary outcomes using logistic regression to calculate unadjusted odds ratios (OR). The first outcome was willingness to accept HPV vaccination, which was based on response to the question, “If the HPV vaccine was available in India, would you accept using it on yourself?” The second outcome was willingness to accept Pap smear based on response to the question, “Would you get a Pap smear to screen for cervical cancer?” Women who responded “yes” were compared with those who responded “no” or “I do not know”. P values of less than 0.05 were considered statistically significant.

Results

Sociodemographic Characteristics of Participants (Table 1)

Table 1 Demographics among 202 women participating in HPV and cervical cancer survey in Karnataka, India
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Of the 225 women approached, 202 (90 %) women completed the survey. The age of participants ranged from 18 to 44 years with the most common age group (42 %) between 25 and 29 years old. A little more than half of the population (56 %) lived in Mangalore city, while the remainder was from rural areas outside of Mangalore. The majority were Hindus (90 %) and married (90 %) with children (68 %). There was a diverse range of educational backgrounds with one-fifth having completed primary school, 47 % completing secondary school, and 31 % with a bachelor’s level degree or higher. Most women (73 %) were working as a housewife. None of the demographic variables were significantly associated with willingness to accept HPV vaccination. Women willing to accept Pap smear were significantly more likely to have children (p value 0.029); otherwise, no other demographic factors were related to Pap smear acceptance.

Knowledge Regarding HPV and Cervical Cancer (Table 2)

Table 2 Knowledge of HPV and cervical cancer topics among 202 women participating in HPV Survey
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Overall cervical cancer and HPV knowledge was low. Fifteen percent of women reported that they knew what cervical cancer is, and 36 % had heard of HPV, with over half (51 %) of those being informed through the media (television, magazine, or radio) and 30 % informed by a doctor. Twenty-eight percent recognized HPV as a cause of cervical cancer.

There was a moderate understanding of cervical cancer risk factors and symptoms. Half of participants identified that HPV can be transmitted sexually; 60 % recognized that HPV can be prevented by condoms; and one-third agreed that cervical cancer risk increases with multiple sexual partners. Approximately, half of the women recognized that cervical cancer is preventable (49 %) and treatable (57 %). The lowest level of knowledge was related to cervical cancer screening with only 7 % reporting that they knew what a Pap smear is, compared with 26 % of the population who were aware of a vaccine for HPV.

Despite gaps in knowledge, 57 % of participants were interested in receiving more information regarding HPV, genital warts, and cervical cancer (data not shown), and 76 % of women found it acceptable to have a government campaign to increase awareness regarding these topics. The most preferred method for receiving information was through a doctor (78 %) with considerably fewer preferring the media (16 %) or internet (4 %).

Attitudes Related to HPV, Cervical Cancer, and Vaccination (Table 3)

Table 3 Attitudes related to HPV, cervical cancer, and vaccination among 202 women participating in HPV survey
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Perceived risk of contracting HPV was low (4 %) and was associated with willingness to accept HPV vaccination (OR 8.7, 95 % CI 1.0–72). Sixty-three percent of women reported at least one negative attitude toward HPV infection. A little more than half of participants (52 %) believed that a woman should be evaluated for cervical cancer throughout her life, and 69 % felt that a doctor should evaluate a woman for cervical cancer; however, only 21 % of women were willing to get a Pap smear.

The majority of HPV and cervical cancer-related beliefs were significantly associated with acceptance of HPV vaccination but were not significantly associated with acceptance of Pap smears. The one notable exception to Pap smear acceptance was the belief that a doctor should evaluate a woman for cervical cancer in which women who agreed had over five times the odds of accepting Pap smear screening (OR = 5.7, 95 % CI 1.9–17).

Although most women were amenable to vaccinations for their children (62 %) and believed that vaccines are effective (66 %), few were interested in using vaccines (15 %). Roughly, half of surveyed women reported that they would use a vaccine against HPV if it were available in India (46 %); however, the percent of women who were interested in vaccination dropped to 12 % at a proposed cost of $360 USD for the vaccine series. Acceptance of the HPV vaccine among women did not differ according to age of administration, but acceptance of HPV vaccination for men (26 %) was lower than for women. Perceived stigma related to HPV vaccination was also low, specifically with little concern that HPV vaccination would lead to increased premarital sexual activity (12 %).

Among women who accepted HPV vaccination, the greatest concern was the cost (39 %, data not shown), followed by the concern that the vaccine is not applicable (23 %), ineffective (13 %), or would have side effects (8 %). The largest concerns for women refusing the HPV vaccine were that it is not applicable to them (42 %), that it would be ineffective (19 %), that it may have side effects (15 %), or that they do not take vaccines in general (12 %).

Health Seeking Practices and Perceived Barriers to Vaccination (Table 4)

Table 4 Health seeking practices and potential barriers to cervical cancer screening and HPV vaccination among 202 women completing HPV survey
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The final section of the questionnaire evaluated potential barriers to screening and vaccination with respect to general health seeking practices. Approximately one-third (31 %) of the population reported that they have health insurance while nearly two-thirds (60 %) have to pay for medical visits. Only one-quarter of the population (27 %) reported that they can always afford to go to the doctor. Eighty-two percent of women have transportation to the doctor; however, 54 % reported that transportation is expensive or that the doctor’s office is far (57 %). The majority reported that they see a doctor regularly (69 %). Most women feel that they can talk to their doctor about anything (61 %), and 44 % reported that they talk to their doctor about sexual health. Nevertheless, only 9 % reported that their doctor performs a yearly Pap smear and an even smaller percentage (5 %) reported ever having a Pap smear.

Discussion

This survey examined knowledge and attitudes toward HPV vaccination and cervical cancer screening, two important public health interventions which have potential to greatly reduce cervical cancer morbidity and mortality in India [3]. Almost half of women surveyed were willing to accept HPV vaccination if it were available. Another half agreed that a woman should be evaluated for cervical cancer throughout her life; however, only one-fifth of women were willing to get a Pap smear and 5 % reported ever having a Pap smear. Low knowledge of HPV and cervical cancer, low perceived risk of infection, and infrequent discussions about HPV with health care providers may be in part responsible for the low uptake of Pap smear screening and present potential barriers to uptake of HPV vaccination.

The first barrier identified was the low level of HPV- and cervical cancer-related knowledge. Other surveys of women across other regions of India have shown similar findings. Awareness about cancer screening in general (not specific to cervical cancer) among women in Mumbai was estimated at 35 %; whereas only 7 % of women in our survey were aware of Pap smears for cervical cancer [16]. This may suggest that knowledge of cervical cancer is low even in comparison with other types of cancer. Another study in Mumbai among married couples found that 38 % of women were aware of cervical cancer, and among those aware of cervical cancer, only 10 % were aware of Pap testing [17]. Other estimates of Pap smear awareness have ranged from 11 % among a population of female college students in Kolkata [18] to 16 % among a group of older women [19]. Knowledge of the term HPV in our population (36 %) was higher than that of the Kolkata college student population (15 %) but lower than that found among college students from Delhi and Mangalore (49 %) [20]. Low levels of cervical cancer-related knowledge were also reported among parents of adolescent girls in Mysore [21] and among a group of healthy patients attending a gynecology clinic in Kolkata [22].

In addition to low knowledge, the level of perceived risk of HPV infection was extraordinarily low, despite estimates that 7.5 % of women in India are currently infected with HPV [4]. Perceived risk of infection was strongly associated with HPV vaccination acceptance. This finding should be interpreted with caution given the wide confidence interval; however, this finding would not be unprecedented. A survey in Eastern India examining women who opted-out of cervical cancer screening found that the most common reason cited for non-participation was that the test was unnecessary in light of a lack of symptoms [23]. Similarly, Shekhar, et al. demonstrated that among 239 nurses surveyed in rural India, 93 % had never been screened for cervical cancer, and 90 % of the reasons cited for not being screened were “no reason,” “not feeling at risk,” and “lack of symptoms” [24]. Raising awareness of infection risk may consequently be an important step in expanding screening and vaccination programs.

The third potential barrier identified was a lack of discussion about HPV and cervical cancer between patients and health care providers. In this survey fewer than half of women reported that they discuss sexual health with their doctor. This is consistent with the finding that most women had heard of HPV through the media rather than through her doctor and contrasts with the finding that 78 % of women who wanted to learn more about HPV would prefer to hear it from her doctor. One survey of parents in Kolkata found that 60 % of mothers who agreed to vaccinate her daughter cited that a doctor’s recommendation was the most important reason for vaccine acceptance [25]. Another survey in Mysore found that parents were significantly more willing to accept HPV vaccination for their daughter if it were recommended by a doctor [26]. Taken together with the fact that 70 % of women reported seeing her doctor regularly along with the low level of HPV-related knowledge, it suggests that spreading awareness of cervical cancer screening and HPV vaccination by health care providers is currently a missed opportunity in India.

In considering strategies for scaling up HPV vaccination and cervical cancer screening, apart from the potential role for health care providers, our findings suggest that a government-sponsored immunization program would be feasible. While government-led vaccination programs have seen variable success in other countries [27, 28], government-sponsored immunization campaigns in India have enjoyed a relatively higher approval among the public. Findings from focus groups in two separate surveys investigating HPV acceptance in India found a positive attitude toward the government universal immunization program in general [21, 29].

The HPV vaccine acceptance rate of 46 % was relatively high considering that perceived risk of HPV infection was nearly nonexistent and that only 15 % of women reported that they would use vaccines for themselves in general. While there appeared to be no preference for targeting vaccination toward any particular age group (9 to 14 vs 15 to 20 vs over 20), overall acceptance of vaccination for these ages was only in the 31–33 % range. These rates are considerably lower than 71 % acceptance by parents in Mysore reported by Madhivanan et al. [26]. They are also lower than actual vaccine coverage rates reported from vaccine delivery pilot projects in Andhra Pradesh and Gujarat which demonstrated a relatively high uptake (77–88 %) of HPV vaccination among girls ages 10 to 14 [30]. Whether the lower acceptance rates reported in our survey are related to low levels of knowledge and perceived risk as described above merits further investigation. One survey among parents in Kolkata found that HPV vaccination approval for their daughters rose from 26 % initially to 74 % after providing a simple, educational fact sheet regarding cervical cancer and HPV [25].

There are a number of limitations of this survey. Participants were selected based on convenience sampling rather than random sampling, which could introduce selection bias. The participants were selected from a clinic population and so may overestimate accessibility to health care compared with the general population of India. The study population’s low knowledge of cervical cancer is a limitation as it calls into question the validity of responses to other sections of the questionnaire. Attitudes may therefore be expected to change accordingly over time as knowledge of the subject matter changes. Another limitation is that the study population only partially included the target ages for the vaccine (11–26 years). This study was conducted prior to formal recommendations in India for the HPV vaccine, and therefore, a broad demographic of adult women was selected. It is relevant to note, however, that women over 26 years of age did not differ significantly from ages 26 and younger in their acceptance of HPV vaccination (data not shown). Additionally, not all potential barriers could be anticipated, and therefore, some barriers may not have been identified through the use of a closed-ended questionnaire. Therefore, addressing the issues outlined above may not be sufficient to guarantee increased vaccination or screening uptake.

Conclusion

Current uptake of cervical cancer screening among this population of South Indian women is low. Our findings suggest that low knowledge of HPV and cervical cancer, low perceived risk of infection, and infrequent discussions about HPV with health care providers may be in part responsible for this low uptake. Despite these findings, there was a moderate level of approval for HPV vaccination. These results will be potentially useful in designing information, education, and communication materials for adolescent girls and women who attend primary care clinics in South India. Given the high burden of cervical cancer among women in India and the current low level of screening or vaccination, there is an urgent need to raise awareness of HPV infection risk and cervical cancer and improve uptake of prevention methods to reduce cervical cancer morbidity and mortality.