JOURNAL OF AMERICAN COLLEGE HEALTH, VOL. 63, NO. 1

Major Article

University Students’ Knowledge and Attitudes Regarding Cervical Cancer, Human Papillomavirus, and Human Papillomavirus Vaccines in Turkey Zeliha Ko¸c, PhD

Abstract. Objectives: The current descriptive study aimed to determine university students’ knowledge and attitudes regarding cervical cancer, human papillomavirus (HPV), and HPV vaccines in Turkey. Participants: A total of 800 students participated. Methods: This study was carried out between September 1, 2012, and October 30, 2012, in 8 female dormitories. Results: In response to the question “What are cervical cancer risk factors?” 10.0% of students said HPV; 90.9% were unaware of how to protect themselves from HPV. Of the students, 99.7% had not had an HPV vaccination, only 32.6% wanted to get an HPV vaccination, and 20.7% did not want to be vaccinated, as they believe it “might have adverse effects.” Conclusions: The results of the present study show that female university students have low levels of awareness and knowledge toward cervical cancer risk factors, HPV, and HPV vaccination.

Directorates of Cancer in 8 cities, cervical cancer ranked ninth among female cancers in 2003.7 The cervical cancer incidence declared by the Ministry of Health was reported to be 3.87/100,000 in 2007, compared with 0.7/100,000 in 1996.8 Cervical cancer is a treatable and preventable disease when diagnosed early.9,10 Some risk factors for the development of cervical cancer are human papillomavirus (HPV) infection,6,10,11 first sexual intercourse at an early age, multiple sexual partners,2,6 sexually transmitted infections, smoking,2,11 immunosuppression, and the use of oral contraceptives.6 The majority of cervical cancer cases are caused by HPV.9,10 HPV is transmitted from one person to another through genital contact, mainly by vaginal or anal sex. In cases of multiple sexual partners, the risk of HPV infection increases.9 HPV has more than 100 genotypes. Genital HPV infection is quite common, and its prevalence worldwide is reported to be 440 million.12 Cancer may not develop in all women who are infected with HPV. However, the risk of developing cervical cancer increases with smoking, acquiring human immunodeficiency virus (HIV), reduced immunity, and a lack of regular Pap (Papanicolaou) tests.9 Although some types of HPV (HPV 6 and 11) cause genital warts, other types (mainly HPV 16 and 18) can cause cervical cancer.2,4,12 Although high-risk types of HPV vary from country to country and region, type 16 most frequently leads to cervical cancer. The highest incidence rates are observed in eastern Africa (42.7%), southern Africa (38.2%), Melanesia (38.1%), Caribbean (32.6%), central America (30.6%), western Africa (29.3%), south America (28.6%), middle Africa

Keywords: attitude, cervical cancer, human papillomavirus, knowledge, vaccine

C

ervical cancer is the second-most common type of cancer in women around the world, following breast cancer.1,2 Although mortality related to cervical cancer increases with age,3 it is a significant cause of death among middle-aged women.4 According to the 2002 global cancer risk statistics, the incidence of cervical cancer was 493,243 and number of deaths was 273,505.5 In 2012, the American Cancer Society predicted a total of 12,170 invasive cervical cancer diagnosis and a total of 4,220 deaths due to cervical cancer.6 Although Turkey does not have a large database, according to data from the Dr Ko¸c is with the Samsun School of Nursing at Ondokuz Mayıs University in Samsun, Turkey. Copyright Ó 2015 Taylor & Francis Group, LLC 13

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(28%), south central Asia (26.2%), and southeastern Asia (18.7%).5 The American Cancer Society reported that there are 2 approved vaccines, Gardasil and Cervarix, to prevent the most common types of HPV infection that cause cervical cancer. The American Cancer Society also reported that the most commonly used method in the follow-up of cervical cancer is the Pap test; most cervical cancers develop slowly, and that almost all cancers can be prevented if women have regular gynecological examinations.6 Young women might not consider cervical cancer an important life-threatening issue. However, they become at high risk for cervical cancer when an HPV infection is acquired.13 It is reported in the literature that due to their high-risk sexual activities, HPV is quite a common sexually transmitted infection among university students, that university students are at high risk of developing HPV and other sexually transmitted infections due to unprotected sexual intercourse, that the students have limited information about HPV and its perceived severity and sensitivity, and that they have high-risk sexual behaviors.14 In a study carried out in the United States to determine the prevalence of HPV among women, it was reported that HPV is particularly prevalent among women 20–24 years old, that the half of the population infected with HPV consisted of sexually active individuals mainly 15–24 years of age,15 and that being sexually active at a young age is a risk factor for HPV infection.16,17 Trottier and Franco reported that young age and sexual behavioral characteristics are the key risk factors in HPV acquisition and persistent HPV infection and that factors such as smoking, oral contraceptive use, sexually transmitted infection, chronic inflammation, and immunosuppressive situations including HIV infection, parity, and diet are other mediatory factors.17 Cermak et al reported that despite the increasing epidemic, HPV knowledge and awareness among society in general is rather low, that HPV is generally identified by abnormal Pap test results, and that there is inadequate knowledge about HPV among women who have had Pap testing.18 Turkey is a country geographically located at the crossroads of Asia and Europe, having a population of 76 million, 97% of which are Muslim.19 In other Eastern communities, premarital sex is not approved by Turkish society because of the influence of Islamic culture.20,21 However, social norms in Turkey are changing today,22 which is affecting the conservative structure of Turkish culture involving sexuality and premarital sex, and polygamy is becoming more common.23 On the other hand, according to data from the Turkish Statistical Institute, the young population between the ages of 15 and 24 constitute 16.8% of Turkey’s population. Youth, who constitute around one fifth of Turkey’s population, generally become sexually active during their university years.21 In the literature, it is reported that the rate of sexual experiences increased and the rate of disavowing premarital sex decreased among young adults.22 Turkey reflects both the Islamic culture and a fast Westernization process.20 In this respect, studies aimed at 14

determining the awareness, knowledge, and attitudes of university students concerning cervical cancer, HPV infection, and HPV vaccination is crucial. As a matter of fact, Chan et al reported that adolescents and young adults were the target group for HPV vaccines in determining cervical cancer; hence, it was important to conduct research to determine their knowledge and attitudes concerning HPV.24 Studies conducted on this subject in Turkey are too limited; they have typically been conducted on women8,25–27 and health care professionals.23,28,29 Relatively few have been conducted on university students,30–32 and such studies were aimed at only determining students’ awareness of HPV and willingness to obtain an HPV vaccination. Yanikkerem et al stated that 38.9% of the participants were sexually active, only 2 of 10 university students had heard about HPV, only 7 students had been vaccinated, 62.4% wanted to get an HPV vaccine, and students’ disease knowledge concerning HPV was low in general.32 Another study conducted on this subject reported that 43.5% of nursing students wanted to obtain an HPV vaccine, that only 0.4% were vaccinated, that 92.9% had insufficient knowledge about HPV infections and HPV vaccination, and that 21.3% did not want to receive a vaccine, as they did not consider themselves at risk for HPV.31 This study aimed to determine university students’ knowledge and attitudes regarding cervical cancer, HPV, and HPV vaccines in Turkey, since previous studies14–17 reported that half of the population infected with HPV consists of sexually active individuals. Furthermore, this study provides new insights into the cognitive and attitudinal processes that shape HPV vaccine intentions in university students. The purpose of this study was to answer the following questions:  What are university students’ awareness, knowledge, and attitudes toward acquiring cervical cancer?  What are university students’ awareness, knowledge, and attitudes toward HPV and HPV vaccination?

METHODS Study Design and Sampling Method This survey study was carried out between September 1, 2012, and October 30, 2012, in 8 female dormitories. Female students who were 18 years and older and who volunteered to participate were enrolled in the study. However, female students who were not willing to participate in the study, who completed less than 100% of the questionnaire and did not respond clearly to the questions regarding cervical cancer, HPV, and HPV vaccines were excluded from the research (n D 320). The exclusion criteria were as follows: (1) being 18 years of age, (2) those with a history of cervical cancer, (3) a previous HPV diagnosis, and (4) abnormal Pap smear test results. The study was carried out with 800 voluntary female students. The response rate was 71.4%. JOURNAL OF AMERICAN COLLEGE HEALTH

Turkish Students and Cervical Cancer, HPV, and HPV Vaccines

Data Collection A questionnaire was used for data collection that included questions to gather demographic information about the students (eg, age, department, socioeconomic status, place of residence, family type, smoking) and questions that determined knowledge and practices related to cervical cancer, HPV, and HPV vaccination (cause/causes and symptoms of cervical cancer, methods for the early diagnosis of cervical cancer, modes of HPV transmission, symptoms of HPV, methods for protection from HPV, HPV vaccination, awareness about the effects of HPV vaccines). The questionnaire was based on the literature review.13,33–42 Content and face validity of the instrument were determined via a panel of 7 experts. Panel members included 2 gynecologist, 1 oncologist, 1 infectious diseases expert, and 3 nurse educators. These professionals were selected based on their knowledge and experience regarding HPV and cervical cancer. The questionnaire was tested on a group of 15 female students during a preimplementation study. No changes were made in the questionnaire form following the pilot study. This study was conducted in accordance with the principles of the Helsinki Declaration, and it commenced after approval was granted by the directors of dormitory. Data were collected from female students over a period of 2 months. Before beginning the data collection, each female student was verbally informed about the nature of the study and its objectives and was invited to participate. Participation was voluntary, and only individuals agreeing to participate completed the survey. The participants were given the opportunity to decline involvement in the study; all who agreed to participate were asked to sign a consent form. The surveys contained no personal identifiers, and the completed surveys were collected by the researcher. The response time was estimated to be 15–20 minutes. The internal consistency of the questionnaire form in this study, measured using Cronbach’s alpha, was .87.

Data Analysis Data were analysed using SPSS 15.0 for Windows (SPSS, Chicago, Illinois). Descriptive statistics’ frequency, percentage, mean, and standard deviation were used to evaluate the data. RESULTS Of the students, 64.0% had an income equal to their expenditures, 42.7% of families lived in the city center, and 76.7% had large families. The mean age of the participants was 20.4 § 1.6. Only 2.7% had sexual experience, and 23.0% smoked cigarettes (Table 1). Overall, 97.2% of students thought that early diagnosis was important in treating cancer; 76.0% had previously heard of cervical cancer, and 24.5% believed that cervical cancer can be prevented. In response to the question “What are cervical cancer risk factors?” 17.4% of students said VOL 63, JANUARY 2015

TABLE 1. Sociodemographic Characteristics of Female Students (N D 800) Characteristics Age M SD Departments the students are enrolled in Faculty of Engineering Faculty of Economics Faculty of Agriculture Faculty of Education Faculty of Law Faculty of Science and Faculty of Letters Faculty of Medicine Faculty of Nursing/School of Health Others Grade 1 grade 2 grade 3 grade 4 grade 5 and above Socioeconomic status Income is less than expenses Income is equal to expenses Income is more than expenses Place of residence City Town Village Type of family Large Nuclear Broken family Have you got any sexual experience? Yes No Do you smoke? Yes No

n

%

20.4 1.6 156 10 30 436 12 98 16 26 16

19.5 1.3 3.7 54.5 1.5 12.3 2.0 3.2 2.0

144 179 192 202 83

18.0 22.3 24.0 25.3 10.4

218 512 70

27.2 64.0 8.8

342 336 122

42.7 42.0 15.3

614 172 14

76.7 21.5 1.8

22 778

2.7 97.3

184 616

23.0 77.0

smoking, 10.0% said HPV, and 9.4% said herpes simplex virus. Unfortunately, 83.2% were unaware of the early symptoms of cervical cancer, 87.0% were unaware of the methods used for the early diagnosis of cervical cancer, 94.4% did not believe that cervical cancer can be prevented by vaccine, 91.7% wanted more information about cervical cancer, and only 1.1% had undergone Pap smear testing (Table 2). It was found that 12.0% of students had heard of HPV; that their sources of information about HPV were newspapers/ magazines, television/radio, the Internet, and books (11.7%, 8.1%, 6.4%, and 4.5%, respectively); 88.7% were unaware of the modes of HPV transmission; 90.0% were unaware of the transmission symptoms; and 90.9% were unaware of how to protect themselves from HPV (Table 3). Only 8.7% of the students knew there were HPV vaccines. In response to the question “Does vaccination protect 15

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TABLE 2. Knowledge, Belief, Experiences, and Intention of Students About Cervical Cancer (N D 800) Characteristics Do you think that early diagnosis is important in cancer? Yes No Have you heard of cervical cancer diagnosis before? Yes No Do you think cervical cancer can be prevented? Yes No What are cervical cancer risk factors?a Sexual intercourse at early age High number of pregnancies Herpes simplex virus Cervical lesions Human papillomavirus Contagious diseases of the sexual partner Smoking Poor socioeconomic status What are early symptoms of cervical cancer?a Abnormal vaginal bleeding Abnormal vaginal discharge Bleeding after sexual intercourse I don’t know Do you know the methods used for early diagnosis of cervical cancer? Yes No If your answer is yes, what are used methods?a (n D 104) Pap smear test Gynecological examination Have ever had a Pap smear test? Yes No Have you heard of protective vaccine against cervical cancer? Yes No Do you believe that cervical cancer can be prevented by vaccine? Yes No Does any member of your family has cervical cancer? Yes No Do you want to be informed about cervical cancer? Yes No

n

%

778 22

97.2 2.8

608 192

76.0 24.0

196 604

24.5 75.5

74 43 75 42 80 67 139 91

9.2 5.4 9.4 5.2 10.0 8.4 17.4 11.4

92 76 45 666

11.5 9.5 5.6 83.2

104 696

13.0 87.0

54 104

6.7 13.0

9 791

1.1 98.9

65 735

8.1 91.9

45 755

5.6 94.4

10 790

1.3 98.7

734 66

91.7 8.3

a

More than 1 answer was given.

individuals who have encountered HPV?” 83.6% responded by saying “I don’t know”; 85.8% did not know when one should get vaccinated; and 83.8% did not know how HPV vaccines worked. Of the students, 99.7% had not had an HPV vaccination, only 32.6% wanted to get vaccinated, 37.5% did not “have enough knowledge about the vaccine,” and 20.7% did not want to have the vaccine as they think it “might have adverse effects” (Table 4). COMMENT This study provided a comprehensive understanding of Turkish university students’ knowledge and attitudes 16

toward cervical cancer, HPV, and HPV vaccination. In this study, it was found that students had rather low levels of awareness and knowledge about cervical cancer. Similarly, previous studies reported low levels of knowledge1,14,35,37,43–47 among university students. This finding suggested that effective education strategies should be developed for young people to increase their knowledge and awareness of cervical cancer risk factors and to reduce the incidence of and mortality related to cervical cancer. Students reported the following cervical cancer risk factors: smoking, low socioeconomic status, HPV, herpes simplex virus, having sexual intercourse at an early age, and JOURNAL OF AMERICAN COLLEGE HEALTH

Turkish Students and Cervical Cancer, HPV, and HPV Vaccines

TABLE 3. Knowledge Status of Students About Human Papillomavirus (HPV) (N D 800) Characteristics Have you heard of human papillomavirus before? Yes No If your answer is yes, what are your sources of information?a (n D 96) TV/radio Newspaper and magazines Internet Brochures and posters Books Do you think human papillomavirus is contagious? Yes No I don’t know What are modes of transmission of human papillomavirus?a Sexual intercourse Blood From mother to baby during birth I don’t know What are transmission symptoms of human papillomavirus?a Rash Genital wounds Persistent abnormal discharge I don’t know In which gender can human papillomavirus cause health problems? In women In men In both I don’t know Do you know which test can detect human papillomavirus? Yes No Did you know that human papillomavirus can cause cancer? Yes No Did you know that human papillomavirus can cause genital warts? Yes No Do you know how to get protected from human papillomavirus? Yes No If your answer is yes, what can be done to get protected from human papillomavirus?a (n D 73) Preferring monogamy in sexual life Avoiding unprotected sexual intercourse Using condoms Having Pap smear test Getting vaccinated a

n

%

96 704

12.0 88.0

65 94 51 21 36

8.1 11.7 6.4 2.6 4.5

65 137 598

8.1 17.1 74.8

59 43 48 710

7.4 5.4 6.0 88.7

53 51 76 720

6.6 6.4 9.5 90.0

90 23 41 646

11.2 2.9 5.1 80.8

63 737

7.9 92.1

64 736

8.0 92.0

75 725

9.4 90.6

73 727

9.1 90.9

62 48 72 56 66

7.7 6.0 9.0 7.0 8.2

More than 1 answer was given.

one’s sexual partner having a contagious disease. Consistent with previous research findings, cervical cancer risk factors include the number of sexual partners in one’s life,42 having multiple sex partners,38,46–48 one’s sex partner having multiple sexual partners,42 having sexual intercourse at an early age,42,46,48 sexually transmitted infections,42 HPV infection38,42,48 age,38 smoking,38,42,48 cancer history in the family,38,42,48 oral contraceptive use,38–48 inadequate use of condoms, poor diet, drug use, VOL 63, JANUARY 2015

and alcohol use.42 The number of students who reported HPV as a risk factor for cervical cancer was very low (10.0%). In parallel to our findings, previous researchers reported that women have poor knowledge of cervical cancer risk factors.35 On the other hand, the majority of the participants (77.7%) in one study reported that HPV could cause cervical cancer,42 and those in another study reported preventive measures for cervical cancer including having a Pap smear (60.2%), becoming sexually active at a later age 17

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TABLE 4. Knowledge Status of University Students About Human Papillomavirus (HPV) Vaccine (N D 800) Characteristics Have you heard of human papillomavirus vaccine? Yes No Do you think HPV vaccine is protective for those who encountered human papillomavirus? Yes No I don’t know When do you think one should have human papillomavirus vaccine? Before sexual intercourse After sexual intercourse Immediately after birth I don’t know What kind of effect does human papillomavirus vaccine show? Protects from precancer lesions and cervical cancer Makes the first resistant to HPV infection for a long time HPV completely eradicates I don’t know Have you had human papillomavirus vaccine? Yes No Do you want to have human papillomavirus vaccine? Yes No If your answer is no, write the reasons for not having human papillomavirus vaccinea (n D 539) I don’t think it’s necessary as I am too young I don’t have enough knowledge about the vaccine I think the vaccine can have adverse effects I heard that it was an expensive vaccine

n

%

70 730

8.7 91.3

69 62 669

8.6 7.8 83.6

51 22 40 687

6.4 2.8 5.0 85.8

54 39 37 670

6.7 4.9 4.6 83.8

2 798

0.3 99.7

261 539

32.6 67.4

182 300 166 54

22.7 37.5 20.7 6.7

a

More than 1 answer was given.

(42.4%), and getting an HPV vaccination (42.1%), respectively.35 In this study, participants’ knowledge rates concerning cancer risk factors varied from 5.2% to 17.4%, indicating that only about one tenth of them knew that HPV is a risk factor for cervical cancer. This is thought to result from individuals’ heath care–seeking behavior. Because Turkish women’s need for information increases as they get older and experience more reproductive health problems, an increase in their general education level and income status also positively affects their cervical cancer knowledge level.26 As a matter of fact, S¸ enol et al reported that gynecological and obstetric problems were common in women 25–44 years of age, that cervical cancer knowledge and awareness was high with 19.1%, and that an increase in one’s general education level and knowledge about cervical cancer reduces one’s risk of cervical cancer.26 In the present study, although 17.4% of the students reported smoking as a cervical cancer risk factor, 23.0% of them continued smoking, and the smoking rate was higher than in other studies in which it was found to vary between 8.6% and 21.9%.14,44,46,48 In addition to being an important risk factor for the development of cervical cancer, Winer et al reported that there was a significant relationship 18

between smoking and HPV infection.49 Having a group of friends that smokes, emulating this behavior in one’s group of peers, and one’s sense of belonging to a group or the pressure of exclusion in Turkish culture often cause youth to start smoking.50 As a matter of fact, Ceylan et al reported that the smoking incidence among students entering a university increased to 20.1%–51.2% due to their new freedom from family supervision and being in a more liberal environment.50 When considering that HPV incidence and prevalence is associated with smoking, informing youth and raising their awareness in this regard is highly important. Although almost all of the students (97.2%) in our study believed that the early diagnosis of cancer was important, only one fourth believed that cervical cancer could be prevented. Only 6.7% of students were familiar with Pap smear testing, which is one of the methods for the early diagnosis of cervical cancer, and only 1.1% had undergone a Pap smear test. Previous studies14,38,40,44,46,48 reported that the rate of having a Pap smear test among students varied between 1.5% and 80.8%. Thus, the students in the present study had a much lower rate than other studies. Similar to related data,40 students in this study believed “they had no chance of being infected with HPV or having cervical cancer as they are too young.” Also Turkish society JOURNAL OF AMERICAN COLLEGE HEALTH

Turkish Students and Cervical Cancer, HPV, and HPV Vaccines

does not deem cervical cancer screening (Pap smear) necessary,51 as sexual experience before marriage is not approved.20–22 Uzunlar et al stated that population-based social screening programs were being planned according to the Turkish National Cancer Program; however, those programs covered only 70% of the population. Structural and sociocultural factors reduce the cervical cancer surveillance rate in developing countries such as Turkey.29 The literature indicates that many factors led to the low rate of Pap smear testing in developing countries, primarily the social pressure placed upon women, women being silent in matters involving their own health, their deficiency of awareness and knowledge about the importance of Pap smear testing, their difficulties in accessing health care services, the long waiting periods, their low income, expensive vaccines and test fees, social security deficiencies, and opportunistic approaches instead of systematic surveillance programs.26 Only 2.7% of the students in the present study were sexually active. A comparison of the present findings with those of other studies revealed that the rate of having sexual intercourse was low and this rate varied between 5.5% and 72.9%.14,40,44,46,52 Based on the comparison of this finding with other Western societies, this result could be explained by the more conservative attitude of Turkish society regarding sexual issues and the cultural disapproval of extramarital sex. Aras et al carried out a study to determine the sexual behavior and contraception status among university students in Turkey and found that female students’ sexual attitude and behaviors were affected by multiple factors ranging from “maintaining virginity” and the “expectations of their families.”22 The authors also found that 41.4% of females and 17.4% of males did not approve of sex before marriage and had knowledge about AIDS (acquired immunodeficiency syndrome), hepatitis, and gonorrhea among the sexually transmitted infections. In the literature, it is reported that factors such as religion and social sexual roles in addition to individuals’ beliefs could explain individuals’ adoption of liberal or conservative sexual behaviors.21 In Turkish society, which is currently undergoing the process of Westernization, virginity is still regarded as the most important indicator of purity and chastity, and being a virgin is accepted as the sign of having a high moral standing.20 In this respect, in Islamic societies such as Turkey, a woman who has extramarital sex may suffer serious consequences in both familial and social terms.21 Due to the importance attached to “virginity” in Turkish society, although the rate of sexual activity had increased among women, they could not express when they had sexual activity for familial and social reasons.22 In this study, it was found that 12.0% of students had previously heard of HPV. They had rather low levels of awareness and information about HPV. Although previous studies reported that students had high levels of knowledge about HPV and increasing levels of awareness,33 in parallel to our findings, levels of knowledge and awareness VOL 63, JANUARY 2015

regarding HPV1,13,35,37,44–47,53,54 were low and they did not consider themselves at risk for HPV infection.37 Students’ sources of information on HPV were newspaper/magazines, television/radio, the Internet, and books (11.7%, 8.1%, 6.4%, and 4.5%, respectively). Prior studies reported the following sources of information on HPV: media, school and education environment, health education _ programs, television, radio, friends, family, the Internet, brochures, family doctors, magazines, newspapers, books, and health care providers.42,45,53 Although sources of information on HPV vary among students, making use of audiovisual sources that can reach masses of people will increase students’ knowledge and awareness levels. In this study, it was found that the majority of the students neither knew whether HPV was contagious (74.8%) nor its modes of transmission (88.7%); only 7.4% reported that it was sexually transmitted. Despite these findings, participants in prior studies knew that HPV was transmitted from one person to another by sexual contact and sexual intercourse35,38,41,42 and perceived that they were at risk of having HPV infection35; however, there was still serious confusion about how the disease was acquired and about the specific outlook of the disease.36 Similarly, Baer et al reported that students were uncertain about how HPV was transmitted.1 A comparison of our findings with previous studies36,41,42 revealed that students had low levels of knowledge about HPV infection and they lacked practical behaviors to successfully reduce their risk of transmission. As indicated in the literature,14 it is of great importance to provide intensive education to university students about HPV and preventative behaviors. Only 9.1% of the students knew how to reduce the risk of HPV during sexual activity and recommended using condoms, getting vaccinated, preferring monogamy in their sexual lives, having a Pap smear test done, and avoiding unprotected sexual intercourse (9.0%, 8.2%, 7.7%, 7.0%, and 6.0%, respectively). Although some researchers found that students believed the use of condoms was the most effective method to prevent HPV infection,14,33,42,45 Winer et al reported that condoms did not have a protective effect and that the genital HPV incidence could be related to multiple sex partners, having sex with a partner whom one had known for less than 8 months, and the sexual relationship between the sex partner and his/her other sex partners.49 In the present study, only 8.7% of the students were familiar with HPV vaccines. It was found that students neither knew when they should have an HPV vaccination (85.8%) nor how HPV vaccines worked (83.8%). In parallel to our findings, previous researchers reported that students’ knowledge, attitude, and awareness about HPV were rather low.37,45,46 On the other hand, other researchers13,36 found that students were aware of HPV vaccines to prevent cervical cancer and that their acceptance of level and interest in obtaining such vaccines was high, particularly among young people who were sexually active and had multiple sexual partners.33 19

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As noted, students’ awareness and knowledge concerning HPV vaccines were very low. In several studies conducted in Turkey on this subject, being sexually inactive, monogamous, and having concerns about HPV vaccines’ safety and cost23 were reported to be important factors that could influence this. Among these factors, cost in particular is highly important for the individuals living in developing countries such as Turkey, and Dursun et al reported that cost was a critical obstacle preventing the widespread use of HPV vaccines.25 Since social security agencies do not cover HPV vaccines in Turkey’s health care system, this may limit the widespread use of such vaccines.29 Moreover, if the cost were covered by the state, the rate of vaccinations could go up.23 In this study, almost all of the students (99.7%) were not vaccinated for HPV and only 32.6% were willing to obtain such a vaccine. The students reported the following reasons for not having obtained an HPV vaccine: “I don’t have enough information about the vaccine” (37.5%), “I don’t think it is necessary as I am too young” (22.7%), and “I think the vaccine can have adverse effects” (20.7%). On the other hand, Illiyasu et al reported that 74.0% of students, Wong and Sam reported that 48.0% of students, and Di Guiseppe et al reported that 81.7% of students were willing to get an HPV vaccine.35,37,38 When compared with the findings of other studies, students’ rate of getting an HPV vaccine was low in the present study, and this rate varied between 1.3% and 42.1% in other studies.13,35,52 The students were unwilling to obtain the HPV vaccination, since they did not have enough information about it and they were afraid of its adverse effects. In parallel to our findings, other studies also reported that students were concerned about the reliability and effectiveness of HPV vaccines.35,37,52 Although there are many factors that could positively influence women’s attitudes concerning HPV vaccination, several researchers reported the following factors: visiting a gynecologist within the last 3 years, a history of genital cancer in one’s family, vaccine awareness, and level of knowledge on this subject.30 S¸ enol et al stated that the deficiency of knowledge about HPV in our country could lead to misunderstandings; thus, people could perceive HPV vaccination as needless, and as a result one of the most important strategies to prevent cervical cancer could be easily disregarded.26 As reported in the literature,30 health education and appropriate communication strategies should be applied to prevent misconceptions about HPV vaccination and to increase public awareness. In a study carried out by Dillard and Spear on university students, among the group who were not vaccinated, 35% reported that “it was too late to be vaccinated and the vaccine to be effective,” as they were “sexually active for a long time,” 35% reported that they were “not convinced that the vaccine is really effective,” 26% reported that they “were not sexually active,” 12% reported that they “had sex only with one person,” and 12% reported that they “were not at risk,” as they “made wise decisions about sex.”36 20

Men play great role as transmitter of the HPV to women.55 HPV vaccination is an effective method to prevent most common types of HPV infection that cause cervical, anal, penile, and head/neck cancers, anogenital warts, external genital lesions, and recurrent respiratory papillomatoses.55–57 HPV vaccines alert immunogenicity in females and males.56 One’s willingness to get vaccinated against HPV is closely associated with one’s knowledge of HPV, cancer, and other risk factors. As reported in the literature, education on HPV is an important factor to increase the status of getting vaccinated against HPV. The results of the present study show that female university students have low levels of awareness and knowledge toward cervical cancer risk factors, HPV, and HPV vaccination. The awareness of HPV and HPV vaccination should be increased. Health care professionals must focus not only on the diagnosis and treatment of cervical cancer, but must also provide information about cervical cancer, HPV, and HPV vaccines to university students. There is an urgent need for educational programs to enhance the level of awareness and motivation.

Conclusion In conclusion, cervical cancer is an important health problem due to the fact that it is the most prevalent type of cancer among women around the world: 1 of the 10 most common types of cancer in Turkey and the rate is gradually increasing. As far as the researcher knows, this study is the first to assess the awareness, knowledge, and attitudes of female university students in Turkey about cervical cancer, HPV, and HPV vaccines. Health care professionals have important duties to establish cervical screening programs, to conduct research on HPV vaccination, and to inform individuals. In this context, as indicated in the literature,40 with the aims of preventing cervical cancer and HPV and to encourage health-promoting behaviors among sexually active young people, it might be of benefit to avoid initiation of sexual intercourse at an early age. In addition, limiting the number of sexual partners may also reduce the risk of acquiring HPV over one’s lifetime.

Limitations This study only included female university students. The findings obtained from the study cannot be generalized to male university students. However, it is of great importance to determine the awareness, knowledge, and attitudes of male university students about cervical cancer, HPV, and HPV vaccination. As indicated in the literature, HPV vaccines can be considered cancer prevention vaccines only for women. It might also lead to the opinion that only women are responsible for their sexual health.54 HPV vaccination in males has the potential significantly decrease HPV associated infection and diseases. Therefore, vaccination of both men and women could potentially interception JOURNAL OF AMERICAN COLLEGE HEALTH

Turkish Students and Cervical Cancer, HPV, and HPV Vaccines

the spread of HPV.58 For this reason, future studies can be carried out in a population including both female and male students and compare gender differences.

ACKNOWLEDGMENTS I would like to thank Selma B€ uy€ uk€ unal, Evrim Deniz and Ay¸s e S¸ anlıya who helped in data collection phase of the study. I would also like to thank the students who took part in this study.

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