ABSTRACT
Purpose: To evaluate knowledge, attitudes and factors associated with acceptability of human papillomavirus (HPV) vaccine among undergraduate medical, dental, and nursing students in South India.
Methods: Using a post-test study design, a convenience sample of 988 students (age 18–26 years) were surveyed. The primary outcome was vaccine acceptability (likely to intend to receive the vaccine). Bivariate analysis using Chi-Square test of independence and multivariate binary logistic regression analysis was used to examine factors associated with vaccine acceptability.
Results: Out of 988 students surveyed, majority had heard about cervical cancer (95%), HPV (89.3) or genital warts(77.5). Only 59.7% had heard of HPV vaccine prior to the survey; 65.2% intended to receive the vaccine and 68.3% were willing to recommend the vaccine to others. Participants aged <22 years were less likely to accept the vaccine (OR:0.85, CI:0.76–0.96) compared with participants aged older than 22 years. Medical students (OR:1.12, CI:1.03–1.23), students who reported alcohol use (OR:1.15, CI:1.03–1.29) and those with moderate knowledge scores were more likely to intend to receive the vaccine (OR:1.14, CI:1.04–1.24), compared to others. On multivariate analysis, only course (OR 1.366, CI 1.016–1.835) and attitude score (OR 4.17; CI 2.12–8.2) were statistically associated with intention to receive the HPV vaccine.
Conclusion: Two-thirds of students intended to receive the HPV vaccine. Although the overall awareness of the HPV-related disease and prevention is good, considerable knowledge gaps exists in many areas suggesting that that more education about HPV disease and benefits of vaccination should be included in the undergraduate medical school curriculum.
Keywords: Human papillomavirus (HPV) disease, HPV vaccine, knowledge, attitudes and perception, medical students, India
Introduction
Cervical cancer is the fourth leading cancer worldwide among women, with an estimated 527,624 new cases and 265,672 deaths annually.1 In India, cervical cancer is the second most common cancer among women, accounting for approximately 122,844 new cases and 67,477 deaths annually.2,3 HPV is a common sexually transmitted infection (STI) and causes a wide spectrum of diseases including anogenital warts and cervical cancers.4 Persistent infection with one of the high-risk (oncogenic) HPV types is necessary cause of cervical cancer. In India, high-risk HPV types 16 and 18 account for approximately 80% of cervical cancers and 63% of high-grade cervical precancerous lesions.3 The virus infects epithelial cells of skin and mucosa, and has also been associated with cancer of the oropharynx, vulva, vagina, anus, and penis.4
Despite the recommendations by the World Health Organization (WHO) and the availability of highly effective and safe HPV vaccines in more than 100 countries, HPV vaccine is not currently included as part of the national immunization program (NIS) in India; however, the vaccine is available in the private sector since 2008, and in 2016, the State Government of Delhi and Punjab launched HPV vaccine implementation.5-10 Two types of HPV vaccines are available in India – quadrivalent vaccine (GardasilTM, Merck, USA, HPV4 targeting HPV types 6,11,16 and 18) and bivalent vaccine (CervarixTM, GSK Biologicals, Belgium, HPV2 targeting HPV types 16 and 18).3 The 9 valent HPV vaccine (GardasilTM, Merck, USA) is not currently available in India.11 The Indian Academy of Pediatrics Advisory Committee on Vaccination and Immunization Practices (IAP COVI) recommends offering HPV vaccine to all females aged 9–26 years who can afford the vaccine (Category 2 of IAP categorization of vaccines).11 For girls aged 9–14 years, two intramuscular doses of either of the two HPV vaccines (HPV4 or HPV2) at 6-months interval is recommended. For girls aged 15 years and older, and for immunocompromised girls and women, three doses of the vaccine over a 6-month period is recommended.10,11
Barriers for the implementation of HPV vaccine program in India are the vaccine costs, health prioritization, variable epidemiologic surveillance data on HPV-related cancer burden, lack of awareness of HPV, vaccine safety, and societal and cultural barriers.6,12,13 Community engagement to increase knowledge of HPV disease burden and vaccine safety and efficacy, health care provider training and education, continued advocacy to policy makers for including HPV vaccine as part of the national immunization program are some of the key strategies to address HPV vaccine implementation barriers in India.3,14
Medical as well as other health care professional students (e.g. dental, nursing, pharmacy), as future physicians and health care providers are the key stakeholders in improving awareness of HPV-related disease burden and advocate for HPV vaccination programs.15-17 It is important to assess the knowledge of HPV and the acceptability of the vaccine among medical, dental, and nursing students in the health sector, especially given the controversy and debates related to the cultural aspects, disease prioritization and parental attitudes.6,13 Medical college structure in India differs from those in North America. The Bachelor of Medicine and Bachelor of Surgery (MBBS) degree course in India consists of a 5.5 year (4.5 years of academic education plus 1 year of mandatory rotating internship) and considered as an undergraduate degree (UG) degree program. In general, the candidate should have completed 17 years of age as on December 31 of the year of admission to a school offering a bachelor medical, dental, nursing, or medical and laboratory technology (MLT) UG degree course in India.
The awareness and attitudes about HPV vaccine among undergraduate students have been reported, but data are limited regarding HPV vaccine acceptability and recommendation to others.15–23 It is important to assess the knowledge of HPV and the acceptability of the vaccine among medical students in the health sector, especially given the controversy and debates related to the cultural aspects, disease prioritization and parental attitudes.6,13 Utilizing data from previously published studies for survey development,19-23 we evaluated the acceptability and correlates of HPV vaccination among medical and paramedical students in South India.
Results
Participant characteristics
A total of 1095 participants were approached; 44 were excluded (e.g. inconsistent or incomplete information, unwilling to participate). In addition, 63 participants reported prior receipt of the HPV vaccine and were also excluded from the analysis. The final sample for analysis yielded 988 students 72.3% were females; 50.8% were between the ages of 20–22 years (Table 1). Most were medical students (43.5%) followed by dental (27.9%), nursing (21.1%), and MLT students (7.5%). Majority of participants reported no previous sexual experience (94.5%), did not smoke (93.0%), and did not consume alcohol (86.7%). Eighty-one (79.6%) participants belonged to the middle socio-economic status, defined as those with annual household disposable income between 200,000 Rupees ($3080 at 2017 prices) and 1 million Rupees ($15,398 at 2017 prices) [21].
Table 1.
Socio-demographic characteristics of study participants (n = 988).
| Characteristics | Number | Percentage |
|---|---|---|
| Gender | ||
| Male | 274 | 27.7 |
| Female | 714 | 72.3 |
| Age (years) | ||
| 18–19 | 396 | 40.1 |
| 20–22 | 502 | 50.8 |
| 23–25 | 82 | 8.3 |
| 25–26 | 08 | 0.8 |
| Degree Course | ||
| Medical (MBBS) | 430 | 43.5 |
| Dental (BDS) | 276 | 27.9 |
| Nursing | 208 | 21.1 |
| MLT | 74 | 7.5 |
| Year of Course | ||
| First Year | 318 | 32.2 |
| Second Year | 243 | 24.6 |
| Third Year | 227 | 23.0 |
| Fourth Year | 129 | 13.1 |
| Internship | 71 | 7.2 |
| Smokinga | ||
| Smoker | 65 | 6.6 |
| Non-smoker | 919 | 93.0 |
| Drinking statusb | ||
| Drinks alcohol | 127 | 12.9 |
| Does not drink alcohol | 857 | 86.7 |
| Economic statusc | ||
| High & Middle-High | 152 | 15.4 |
| Middle | 786 | 79.6 |
| Middle-low and Low | 30 | 3.0 |
| Locationd | ||
| Urban | 551 | 55.8 |
| Rural | 396 | 40.1 |
| Father’s professione | ||
| Doctor/healthcare provider | 113 | 11.4 |
| Public employed | 299 | 30.3 |
| Self-employed | 491 | 49.7 |
| Retired/unemployed | 65 | 6.6 |
| Mother’s Professionf | ||
| Doctor/healthcare provider | 102 | 10.3 |
| Public employed | 187 | 18.9 |
| Self-employed | 95 | 9.6 |
| Retired/unemployed | 595 | 60.2 |
| Marital Statusg | ||
| Single | 899 | 91.0 |
| Married | 10 | 1.0 |
| Dating | 68 | 6.9 |
| Sexual statush | ||
| No sexual experience | 934 | 94.5 |
| Sexual experience with contraceptive | 31 | 3.1 |
| Sexual experience without contraceptive | 17 | 1.7 |
a,b,c,d,e,f,g,hMissing data for 4, 4, 20, 41, 20, 9, 11 and 6 students respectively;
Abbreviations: MBBS – Bachelor of Medicine and Bachelor of Surgery; MLT – Medical Laboratory Technology
Awareness of HPV, HPV vaccine and cervical cancer
Out of 988 students surveyed, majority had heard about cervical cancer (95%), HPV (89.3%) or genital warts (77.5%). However, only 59.7% had heard of HPV vaccine prior to the survey.
Sources of information on HPV vaccine
College and universities (42.1%) were the most common source of information followed by TV/internet (12.1%), family or friends (4.9%), and primary care physician (2.9%). However, 37.2% of students had not heard of the WHO recommendations for HPV vaccination.
Knowledge of HPV infection and cervical cancer
Most students (78.0%) knew the sexual route of HPV transmission; 25.8% believed that HPV infection can be asymptomatic (Table 2). Although, 62.6% students knew that cervical cancer is caused by persistent infection with high-risk HPV types, and that HPV can affect males (62.6%), only 37.2% were aware that HPV can cause oropharyngeal cancer. Overall, 49.5% of students stated that condoms protect against HPV infection.
Table 2.
Summary of knowledge statements on HPV, HPV infection, cervical cancer and HPV vaccine (n = 988).
| Q.NO | STATEMENTS | CORRECT ANSWER | TRUE (n/%) | FALSE (n/%) | I DO NOT KNOW (n/%) |
|---|---|---|---|---|---|
| HPV, HPV INFECTION, CERVICAL CANCER RELATED STATEMENTS | |||||
| 1 | Cervical cancer is most commonly associated with persistent HPV infection | True | 618(62.6) | 32 (3.2) | 338(34.2) |
| 2 | HPV sexually transmitted | True | 771 (78.0) | 43(4.4) | 174 (17.6) |
| 3 | More than 50% of sexually active men and women are infected with HPV at some point in their livesa | True | 329(33.3) | 168(17) | 485 (49.1) |
| 4 | HPV is transmitted to the partner only if the carrier shows symptoms | False | 212 (21.5) | 353 (35.7) | 423 (42.8) |
| 5 | HPV can cause oropharyngeal cancer | True | 368(37.2) | 161(16.4) | 459 (46.5) |
| 6 | There are specific HPV types that cause cervical cancer | True | 583 (59) | 35 (3.5) | 370 (37.4) |
| 7 | Most HPV infections will be cleared by the immune system | True | 425 (43.0) | 116 (11.7) | 447(45.2) |
| 8 | HPV can infect males | True | 618 (62.6) | 90(9.1) | 280 (28.3) |
| 9 | Most HPV infections don’t cause any symptoms | True | 255 (25.8) | 235 (23.8) | 498 (50.4) |
| 10 | There is no current antiviral drug to cure HPV | True | 228 (23.1) | 267 (27.0) | 493 (49.9) |
| HPV VACCINE RELATED STATEMENTS | |||||
| 11 | There is a vaccine to prevent HPV infectionb | True | 523 (52.9) | 344(34.8) | 117 (11.8) |
| 12 | Currently available HPV vaccines protect against 2 or more HPV typesc | True | 276 (27.9) | 53 (5.4) | 656 (66.4) |
| 13 | Both, males and females, should be vaccinated | True | 636 (64.4) | 203(20.5) | 149(15.1) |
| 14 | HPV vaccines help clear the existing HPV infection | False | 83 (8.4) | 466 (47.2) | 439 (44.4) |
| 15 | Adolescents and young adults are screened for HPV before getting vaccinatedd | True | 451 (45.6) | 139 (14.1) | 392 (39.7) |
| 16 | Girls/women who have already been vaccinated also require cervical cancer screening | True | 603 (61) | 81 (8.2) | 304 (30.8) |
| 17 | HPV vaccine is currently recommended for the age group between 9 to 26 years | True | 378(38.3) | 257 (26.1) | 353 (35.7) |
| 18 | The market cost of HPV vaccine in India is ranging from 5000 to 10,000 rupees | True | 73 (7.4) | 248 (25.1) | 667 (67.5) |
| 19 | Two or more doses of HPV vaccine are required for protection | True | 405(41.0) | 64 (6.5) | 519 (52.5) |
| 20 | Condoms protect against HPV | False | 489 (49.5) | 88 (8.9) | 411 (41.6) |
a,b,cMissing data for 6,4, 3, 6 respectively.
Knowledge of HPV vaccine
A minority of participants (24.4%) reported that HPV vaccine may be administered to a woman with prior infection; 21.8% knew that HPV vaccine cannot treat the existing infection. However, 64.4% indicated that both males and females should be vaccinated and 61% knew that cervical cancer screening was required for individuals who are already vaccinated. In addition, 38.3% of participants were aware of the recommended age range (9–26 years) for receiving the HPV vaccine, and 7. 4% knew the vaccine cost as <10,000 Indian rupees (<$154).
Combined knowledge score for HPV infection and vaccination
The HPV infection/vaccination knowledge score was in the range 0 to 18, with a mean score of 8.55 (SD 4.055) Of the 20 knowledge statements, participants could score from 0 to 20 (each correct answer given one point and incorrect/do not know answers given 0). Of the 988 respondents, 21 (2.1%) scored zero and 3 (0.3%) scored 18 points; none of the participants scored the maximum of 20 points. A total of 439 (44.1%) respondents received a score of 10 points and above. Our study showed no significant difference between males and females’ HPV infection/vaccine knowledge scores (p = 0.694); 43.4% males (119 out of 274) and 44.8% females (320 out of 714) received a knowledge core of 10 and above.
In binary logistic regression analysis, medical students (OR: 2.31, CI: 1.75–3.05) and medical and dentistry students with clinical rotations as part of their curriculum (OR: 2.14, CI: 1.58–2.89) had more knowledge compared to students studying other courses and without clinical rotations. Students who had heard of the HPV vaccine beforehand (OR: 1.79, CI: 0.161–1.98) scored higher on the knowledge score. Parents’ profession (p = 0.084 for father’s and 0.869 for mother’s) did not reflect high knowledge on the participants. Parents’ profession had no association with participant’s knowledge scores.
Attitude towards HPV vaccination
Majority (87.4%) strongly agreed/agreed that HPV infection is a serious condition, but only 12.0% believed that they could be easily infected by HPV (Table 3). Many participants (86.4%) stated that awareness education on HPV should be implemented at schools; 82.5% of participants stated that government of India must make the HPV vaccine affordable to all adolescents and young adults and 68.4% thought that it is preferable to vaccinate both males and females. Less than half (43.4%) of the participants were willing to undergo PAP smear for cervical cancer screening.
Table 3.
Participant’s attitudes towards HPV vaccination (n = 988).
| Attitude Assessing Statement | Strongly agree n (%) | Agree n (%) | Neutral n (%) | Disagree n (%) | Strongly disagree n (%) |
|---|---|---|---|---|---|
| I think I can be easily infected by HPVa | 23 (2.3) | 96(9.7) | 342 (34.6) | 289 (29.3) | 231 (23.4) |
| I think HPV infection is a serious diseaseb | 331 (33.5) | 533 (53.9) | 99 (10.0) | 12 (1.2) | 5 (0.5) |
| Getting the HPV vaccine would be beneficial to a teenage girl or boy’s future healthc | 393 (39.8) | 425 (43.0) | 125 (12.7) | 33 (3.3) | 7 (0.7) |
| Getting the HPV vaccine will send a message to teenagers that it is OK to have sexd | 58 (5.9) | 172 (17.4) | 354 (35.8) | 284 (28.7) | 111 (11.2) |
| Education on HPV should be implemented at schoole | 457 (46.3) | 396 (40.1) | 106 (10.7) | 11 (1.1) | 5 (0.5) |
| Men can get involved to prevent their partner from getting cervical cancerf | 231 (23.4) | 395 (40.0) | 285 (28.5) | 44 (4.5) | 12 (1.2) |
| People who have only one sexual partner have a low risk of becoming infected with HPVg | 168 (17.0) | 405(41.0) | 300 (30.4) | 86 (8.7) | 20 (2) |
| Using a condom can provide 100% protection against HPV infectionh | 51 (5.2) | 219 (22.2) | 481 (48.7) | 188 (19.0) | 41 (4.1) |
| HPV vaccination is not necessary because a Pap test can be done to rule out cervical canceri | 41 (4.1) | 106 (10.7) | 398 (40.3) | 320 (32.4) | 114 (11.5) |
| It is preferable to vaccinate both men and women against HPVj | 238 (24.1) | 451 (45.6) | 253 (25.6) | 24 (2.4) | 12(1.2) |
| I believe that Government of India must make the HPV vaccine affordable to all adolescents and young adults given the benefits it offersk | 407 (41.2) | 408 (41.3) | 152 (15.4) | 12 (1.2) | 2 (0.2) |
| I have had family/friends sought my opinion regarding HPV vaccinationl | 74 (7.5) | 176 (17.8) | 414 (41.9) | 218 (22.1) | 83 (8.4) |
| I believe that the HPV vaccine should be recommended for all teenage girls and young womenm | 323 (32.7) | 448 (45.3) | 190 (19.2) | 16 (1.6) | 6 (0.6) |
| I believe that vaccination should be recommended for all teenage boys and young menn | 264 (26.7) | 412(41.7) | 252 (25.5) | 40(4.0) | 13 (1.3) |
| I believe it would be difficult and embarrassing for me to ask for the HPV vaccine because it is associated with a sexually transmitted infection.o | 71 (7.2) | 190 (19.2) | 365 (36.9) | 232 (23.5) | 124 (12.6) |
| If other people knew I received the HPV vaccine, I would be embarrassed.p | 54 (5.5) | 144 (14.6) | 340 (34.4) | 296 (30.0) | 148 (15.0) |
| I would worry about what my partner or future partner would think if I received the HPV vaccineq | 69 (7.0) | 154 (15.6) | 321 (32.5) | 282 (28.5) | 153 (15.5) |
| If other people knew I have HPV infection, I would be embarrassed.r | 91 (9.2) | 216 (21.9) | 321 (32.5) | 221 (22.4) | 121 (12.2) |
| I would be willing to get a PAP smear for cervical cancer screenings | 137(13.9) | 292 (29.6) | 380 (38.5) | 80 (8.1) | 51 (5.2) |
| I would like to receive or recommend HPV vaccination, whether or not they come from conservative familiest | 190 (19.2) | 363 (36.7) | 351 (35.5) | 52 (5.3) | 19 (1.9) |
| I believe that all physicians should recommend every teenage girl to be vaccinated and inform them about harmful effects of HPVu | 294 (29.8) | 442 (44.7) | 220 (22.3) | 18 (1.8) | 6 (0.6) |
| Knowing the risks of HPV, I would like to be educated by the experts on HPV vaccinationv | 315 (31.9) | 430(43.5) | 211 (21.4) | 19 (1.9) | 5 (0.5) |
| If this vaccine is freely available in schools/clinics, I would be willing to take the vaccinew | 270 (27.3) | 374 (37.9) | 288 (29.1) | 39(3.9) | 10 (1) |
| If this vaccine is freely available in school/clinics, I would be willing to recommend the vaccine to othersx | 300 (30.4) | 375 (38.0) | 257 (26.0) | 34 (3.4) | 10 (1) |
| Knowing the risks of HPV, I intend on taking HPV vaccine in the future.y | 278 (28.1) | 377 (38.2) | 263 (26.6) | 32 (3.2) | 24 (2.4) |
a,b,c,d,e,f,g,h,i,j,k,l,m,n,o,p,q,r,s,t,u,v,w,x,yMissing data for 7,8,5,9,13,24,9,8,9,10,7,23,5,7,6,6,9,18,48,13,8,8,7,12,14 respectively.
Attitude score towards HPV vaccination
The overall attitude score ranged from 34 to 120 with a mean of 62.29 (SD 9.631). On converting the attitude score into a 5-point scale, the attitude score ranged from 1.36 to 4.80 with a mean of 2.49 (SD 0.385) corresponding to an overall positive attitude to HPV vaccination. The lower the attitude score, the more is the positive attitude towards HPV vaccination. There was no significant difference (p = 0.565) in attitude scores between male and female students [27 (9.85%) out of 274 male respondents and 62 (8.68%) out of 174 female respondents had positive attitude towards HPV vaccination]. Students with a history of smoking (13 out of 65, 20%) demonstrated more positive attitude compared to non-smokers (76 out of 919, 8%; p value = 0.001). Almost half of female students (344 out of 696, 49.43%) expressed their willingness to accept PAP smear for cervical cancer screening; of the 344 female students who were willing to opt for PAP smear screening test, 152 (44.19%) were medical students (pursuing MBBS degree) with clinical rotation experiences with a lower attitude score suggesting a positive attitude towards vaccination (this group represented only 15.4% of the total study participants). Parent’s profession (father’s profession, p value = 0.817 and mother’s profession, p value = 0.265), sexual history (p value = 0.566) and residence location (p value = 0.465) did not play any role in student attitudes.
Participants Likely to Intend to Receive HPV Vaccine and Recommend the Vaccine to Others (Bivariate analysis and binary logistic regression analysis).
In our study, 65.2% of participants intended to receive the HPV vaccine in the future and 68.3% were willing to recommend the vaccine to others, if it was freely available in schools/clinics. On bivariate analysis, participants aged <22 years were less likely to intend to receive the vaccine (OR:0.85, CI:0.76–0.96) and less likely to recommend the vaccine compared with those participants aged older than 22 years (OR:0.75 CI: 0.65–0.87). (Table 4). Medical students (OR:1.12, CI:1.03–1.23) and students who reported alcohol use (OR:1.15, CI:1.03–1.29) were more likely to intend to receive the vaccine, compared to others. Those with good/adequate knowledge scores were more likely to intend to receive the vaccine (OR:1.14, CI:1.04–1.24) and more likely to recommend the vaccine (OR:1.27, CI:1.14–1.42). Participants who showed positive attitude related to HPV vaccination were more likely to recommend the vaccine to others (OR:1.58, CI:1.42–1.77). Based on results of the bivariate analysis, gender (p = 0.788), socio-economic (p = 0.157), clinical rotations (p = 0.577), sexual experience (p = 0.140), smoking (p = 0.238), father’s profession (p = 0.553), and mother’s profession (p = 0.661) were not found to be significant factors for participants likely to intend to receive the HPV vaccine. Based on results of the bivariate analysis, gender (p = 0.42), sexual experience (p = 0.75), smoking (p = 0.047), father’s profession (p = 0.398), and mother’s profession (p = 0.413) were not found to be significant factors for recommending the vaccine to others. Variables that were significant for acceptability of the vaccine included age (p value = 0.03), course (p value 0.008), alcohol (p value 0.020), knowledge score (p value 0.004) and attitude score (p value < 0.001). These variables were then considered for multivariate analysis to see which of these factors cause significant effect on the dependent variable (intention to receive the vaccine). Since the dependent variable is categorical and takes only two values, either yes or no, we performed multivariate binary logistic regression analysis. Results of binary logistic regression analysis for intention to receive the vaccine and recommendations of the vaccine to others are shown in Table 5. In adjusted analysis, only type of degree course (OR 1.366; CI 1.016, 1.835) and attitude score (OR 4.17; CI 2.12, 8.2) were statistically associated with student’s intention to receive the HPV vaccine. Course (OR 1.694; CI 1.286, 2.232), alcohol use (OR 1.790; CI 1.173, 2.734), knowledge score (OR 1.499; CI 1.142, 1.969) and attitude score (OR 4.975; CI 2.747, 9.009) were found to be significant factors associated with student’s recommendation of the vaccine to others.
Table 4.
Acceptability of HPV vaccine among undergraduate students and recommendations of HPV vaccine to others (bivariate analysis).
| ACCEPTABILITY OF HPV VACCINE AMONG MEDICAL STUDENTS |
RECOMMENDATIONS OF HPV VACCINE TO OTHERS |
|||||||
|---|---|---|---|---|---|---|---|---|
| Subject in analysis | N (%) | p value | OR (95% CI) | Subject in analysis | N (%) | p value | OR (95% CI) | |
| Gender | ||||||||
| Male | 271 | 184 (67.9) | 0.788 | 1.01 (0.92–1.117) | 274 | 159 (58.03) | 0.42 | 1.05 (0.93–1.19) |
| Female | 703 | 471 (66.99) | 714 | 394 (55.18) | ||||
| Age | ||||||||
| 17–22 years | 885 | 586 (66.2) | 0.030* | 0.854 (0.76–0.96) | 898 | 488 (67.9) | 0.001* | 0.75 (0.65–0.87) |
| Above 22 years | 89 | 69 (77.5) | 90 | 65 (72.22) | ||||
| Course | ||||||||
| MBBS | 422 | 303 (71.8) | 0.008* | 1.126 (1.03–1.23) | 430 | 278 (64.65) | <0.001* | 1.31 (1.18–1.46) |
| Non-MBBS | 352 | 200 (56.81) | 558 | 275 (49.28) | ||||
| Year | ||||||||
| Clinical | 665 | 451 (67.8) | 0.577 | 1.03 (0.93–1.13) | 670 | 390 (58.2) | 0.04* | 1.14 (1.002–1.29) |
| Non-clinical | 309 | 204 (66.01) | 318 | 163 (51.26) | ||||
| Socioeconomic status | ||||||||
| High and middle-high | 152 | 110 (72.36) | 0.157 | 1.09 (0.98–1.22) | 152 | 98 (64.47) | 0.019* | 1.19 (1.04, 1.36) |
| Middle/middle-low and low | 803 | 534 (66.5) | 816 | 442 (54.17) | ||||
| Father’s profession | ||||||||
| Healthcare | 111 | 77 (69.37) | 0.553 | 1.042 (0.913, 1.19) | 113 | 67 (59.29) | 0.398 | 1.076 (0.91, 1.27) |
| Non-healthcare | 843 | 561 (66.55) | 855 | 471 (55.09) | ||||
| Mother’s profession | ||||||||
| Healthcare | 100 | 69 (69) | 0.661 | 1.033 (0.898, 1.19) | 102 | 53 (51.96) | 0.413 | 0.924 (0.76, 1.124) |
| Non-healthcare | 865 | 578 (66.82) | 877 | 493 (56.21) | ||||
| Smoking | ||||||||
| Smoker | 65 | 48 (73.84) | 0.238 | 1.106 (0.95, 1.29) | 65 | 44 (67.69) | 0.047 | 1.229 (1.03, 1.47) |
| Non-smoker | 905 | 604 (66.74) | 919 | 506 (55.06) | ||||
| Alcohol | ||||||||
| Consumes alcohol | 126 | 96 (76.19) | 0.020* | 1.159 (1.039, 1.29) | 127 | 89 (70.08) | 0.001* | 1.31 (1.15,1.49) |
| Non-alcoholic | 844 | 555 (65.76) | 857 | 460 (53.68) | ||||
| Sexual experience | ||||||||
| Sexual experience with or without condom | 48 | 37 (77.08) | 0.140 | 1.153 (0.98, 1.35) | 48 | 28 (58.33) | 0.75 | 1.04 (0.815, 1.33) |
| No sexual experience | 920 | 615 (66.85) | 934 | 523 (55.99) | ||||
| Calculated knowledge score | ||||||||
| Good/adequate knowledge (10–20) | 434 | 313 (72.12) | 0.004* | 1.14 (1.04, 1.24) | 439 | 279 (63.55) | <0.001* | 1.27 (1.14, 1.42) |
| Poor knowledge (0–9) | 540 | 342 (63.33) | 549 | 274 (49.91) | ||||
| Calculated attitude score | ||||||||
| Positive attitude | 89 | 79 (88.76) | <0.001* | 1.36 (1.24, 1.49) | 89 | 75 (84.27) | <0.001* | 1.58 (1.42, 1.77) |
| Negative attitude | 885 | 576 (65.08) | 899 | 478 (53.17) | ||||
| Information source | ||||||||
| No information | 362 | 237 (65.47) | 0.363 | 0.96 (0.874, 1.05) | 368 | 192 (52.17) | 0.064 | 0.896 (0.796, 1.009) |
| Others (media, college, etc,) | 612 | 418 (68.3) | 620 | 361 (58.23) | ||||
Abbreviations: MBBS, Bachelor of Medicine and Bachelor of Surgery; CI, confidence intervals; OR odds ratios.
Table 5.
Acceptability of HPV vaccine among undergraduate students and recommendations of HPV vaccine to others (binary logistic regression analysis).
| Variables | P value | Odds Ratios | Confidence Intervals |
|---|---|---|---|
| Acceptability of HPV Vaccine (Intention to receive the vaccine) | |||
| Course | 0.039 | 1.366 | 1.016, 1.835 |
| Attitude score | <0.001 | 4.17 | 2.12, 8.2 |
| Recommendations of HPV Vaccine to Others | |||
| Course | <0.001 | 1.694 | 1.286, 2.232 |
| Alcohol use | 0.007 | 1.790 | 1.173, 2.734 |
| Knowledge score | 0.004 | 1.499 | 1.142, 1.969 |
| Attitude score | <0.001 | 4.975 | 2.747, 9.009 |
Discussion
In this study, approximately two-thirds of the students intended on receiving the HPV vaccine and recommending the vaccine to others, which is similar to the findings from the other surveys done in India and China.15,21,24 Low vaccine acceptability among medical students has also been reported in Chennai, South India and Chongqing, China.16,25
Educating the medical and paramedical students about HPV-related disease and the importance of vaccination is a key strategy given the crucial role of HCP recommendation to improve the uptake of adolescent HPV vaccines.26,27 In the current study, the key predictors of intention to receive the HPV vaccine were students enrolled in medical school (compared to nursing or dental students) and positive attitude.26 Factors associated with recommendation of the vaccine to others were students older than 22 years, medical students, alcohol use, moderate knowledge HPV infection/vaccine knowledge and positive attitude.
In the present study, students had moderate knowledge of HPV infection and vaccine. The majority of the participants knew that HPV is a STI and can cause cervical cancer. However, many participants were unaware that HPV infection is often asymptomatic, may cause oropharyngeal cancer, and the absence of specific anti-viral therapy. Only 50% of students were aware of the HPV vaccine. In a study conducted among medical students enrolled in a government medical college in the State of Andhra Pradesh, 54% of participants were aware of the HPV vaccine for cervical cancer prevention.28 In contrast, majority of students surveyed at other medical schools in South Indian States of Karnataka (75.6%) and Tamil Nadu (86.4%) were aware of the availability of HPV vaccine for cervical cancer prevention.15,16 Our study showed no significant difference between males and females’ HPV infection and vaccine knowledge scores. Previous reports from India have found that male students had poor awareness of cervical cancer, HPV disease and vaccine.15,29
The differences in knowledge about HPV infection and availability of HPV vaccine among students in our study compared to other reported studies may be multifactorial such as lack of education about HPV infection and availability of a safe and effective vaccine to prevent cervical cancer, lack of exposure to HPV-related disease burden in certain affluent private medical colleges and university (compared to governmental medical colleges which predominantly serve low-income populations at high risk for cervical cancer), inadequate exposure to print and audiovisual media in some settings, socioeconomic factors, societal and religious factors, and stigma.15-17,30,31
In the present study, senior students exposed to clinical rotations as part of their curriculum had higher knowledge on HPV and positive attitude for PAP smear testing compared to first year students which may be attributed to the medical education system in India where students are exposed to clinical aspects of medicine only after the first year. In one report from India, college students enrolled in a biology major course had higher knowledge and awareness regarding cervical cancer compared to students enrolled in non-biology courses.29
In the present study, medical students had more knowledge compared to students studying other courses. In a study from Malaysia, medical students had the highest level of knowledge about HPV infection and vaccine compared to dental and pharmacy students.24 In contrast, another study reported that nursing students had more knowledge on HPV vaccine compared to medical and dental students.16 In addition to physicians, other health care providers including dentists, nurses and pharmacists play an important role in patient education regarding the benefits of HPV vaccination and offering a strong recommendation.32
In the present study, medical students and students with a more positive attitude towards vaccination was associated with intention to receive the HPV vaccine. Studies conducted in the U.S. have found that parents or young women are more likely to accept the HPV vaccine when they receive written educational information about the risks and benefits; however, other reports suggest that parental attitudes and life experiences play a major role in influencing HPV vaccine acceptability.33-35 In one survey, most parents of adolescent girls in Mysore, India were willing to accept the HPV vaccine for their daughters, regardless of poor awareness of HPV and its association with cervical cancer.36 In another study from Kolkata, 80% of parents agreed to vaccinating their daughters against HPV after they were provided a vaccine information sheet.13 A U.S. study reported that 64% of parents agreed to accept the vaccine for their daughters and recommend it to others.19
In our study, only 6% of the students had received the HPV vaccine prior to the survey despite increased high participant reported awareness of HPV and HPV vaccine. In a study from North India, similar low rate (7%) of HPV vaccine acceptance was reported among college students from higher socioeconomic status indicating that lack of awareness, personal beliefs, societal, religious, and cultural barriers may account for poor uptake of HPV vaccine.6,29,37,38 Other reasons cited for poor acceptability of HPV vaccine in India are the high cost, concerns about vaccine safety, relatively low public health spending, lack of uniform health choices, and lack of national policy on cervical cancer screening.6,12,13 Concerns about adverse effects of HPV vaccine and inadequate information were the most common barriers to vaccine acceptance among medical students in China.21
College/university was the main source of information about HPV among our respondents. Studies have reported news, magazines, mass media, and HCP are primary sources of HPV vaccine information.24,37 In our study, one-third of respondents preferred health clinics set up in school, colleges and universities as preferred sites for receipt of HPV vaccine, consistent with other reports from Greece and China.38,39 In a cross-sectional study from Gaborone, Botswana, 70% of parents reported that they would be willing to have their daughters vaccinated at schools if the vaccine was available.40 Schools and television were regarded as the ideal methods of disseminating HPV vaccine information and cervical cancer prevention in Ghana.41 School-based HPV vaccination have been successfully implemented in in the United Kingdom and Australia.42,43
The present study has many limitations including use of a post-only study design, convenience sampling, and inclusion of a single site. The pilot testing of the questionnaire was conducted on 10 participants which may limit the results of the internal consistency reliability test. Participant self-reported data might also have resulted in selection and information bias. The number of female participants were more in number since the nursing batch had female students more than the males. This study did not investigate religious and other unique cultural barriers including concerns for high-risk sexual behaviour. This study did not use validated measures available in the literature to measure HPV vaccine knowledge and attitudes, which limits our ability to compare data with other studies and settings. In the present study, we combined the HPV infection and HPV vaccination knowledge items into once scale, although measuring HPV infection/vaccination knowledge as separate constructs would have strengthened validity. The negative statements used in the combined attitude questions were not reverse coded which may also limit the psychometric validity and interpretability of the attitude scale used in our study.
This study underscores the need to develop a well-designed educational program on HPV vaccine and cervical cancer control and prevention for medical and paramedical students in India. Future prospective studies could evaluate the impact of innovative multi-component medical school curriculum (e.g. case-based curricular methods coupled with interactive small group discussions, simulation training, communication strategies to address vaccine hesitancy) to improve knowledge and promote HPV vaccine recommendations.44 Given the high burden of cervical cancer and other HPV-associated diseases in India, medical and paramedical students can play a pivotal role in implementing a successful HPV immunization program as future health care providers. Future studies should also evaluate implementation of population-based cervical cancer screening and perform comparative cost-effectiveness analysis of HPV vaccination strategy versus cervical cancer screening in India.3,7 The introduction of HPV vaccine as part of the NIS in India must be considered by policy makers to significantly reduce the cervical cancer burden.3
Conclusion
Two-thirds of students in South India intended to receive the HPV vaccine. Although the overall awareness of the HPV-related disease and prevention is good, there is considerable knowledge gaps in many areas. We suggest that more education about HPV disease and benefits of HPV vaccination should be included in the undergraduate medical school curriculum to address the knowledge barriers among medical and paramedical students.
Methods
Study design, site and participants
Using a post-test study design, we conducted a survey among undergraduate students from November 2016 to February 2017 at a tertiary care teaching hospital in Mangalore, a coastal city in the Southern State of Karnataka, India. Participants included in the study were medical, dental, nursing, and MLT students of both sexes, aged 18– 26 years. Students aged <18 years and >26 years, not enrolled in the above referenced medical and paramedical courses, not willing to participate, surveys with missing data (>5% for any variable) were excluded from the study. Using a convenient sampling method, study participants were surveyed in a private setting at the beginning or at the end of a class. Written informed consent was obtained from all participants. This study was approved by the Institutional Review Board at K.S. Hegde Medical Academy, Deralakatte, India.
Measure
A 61-item, self-administered, semi-structured anonymous questionnaire was designed consisting of 4 sections: The first section determined participant socio-demographic information (Table 1). The second section assessed awareness of HPV infection, cervical cancer, and HPV vaccine. Information on the awareness was determined by using four items with Yes-No responses (have you heard of 1) HPV; 2) cervical cancer; 3) genital warts; and 4) HPV vaccine. The third section determined knowledge of HPV infection (10 questions) and HPV vaccine (10 questions) using one measure with True/False/I don’t know responses (Table 2).
Following completion of the third (knowledge) section of the survey, participants received a brief 1-page information pamphlet about HPV and vaccine after review of which they were asked to complete the remainder of the survey. The fourth section assessed attitudes towards HPV vaccination using 25 statements on a 5-point Likert scale (Table 3). The attitude questions included positive and negative statements about HPV vaccination. Reverse coding was not needed for any of the negative statements. Participants could choose more than one option only for the question about risk factors for cervical cancer, HPV-related diseases, and information sources.
The survey was designed based on prior studies.19-23 After developing the survey items, we conducted a content review by 3 reviewers. Reviewers were selected based on their clinical and research experience in HPV and cervical cancer, expertise in pediatric/adolescent vaccine sciences, infectious diseases, public health and microbiology. Reviewers examined the accuracy of the items in each content domain and also discussed potential concerns that may arise during the administration of the questionnaire. The questionnaire was then pilot tested among 10 random participants to determine the clarity and comprehension of the survey items. The Cronbach’s alpha for Section C (HPV knowledge and HPV vaccine related knowledge), and Section D (Attitude toward HPV vaccination) of the questionnaire was 0.850 and 0.814 respectively.
Outcome measures
All study participants (range, 18–26 years) were eligible for HPV vaccination. In our study, 6% (63/1051) of the students had already received at least one dose of the HPV vaccine series and therefore excluded from the analysis. The final analytic sample consisted of 988 participants who had not received the vaccine.
The main outcome measure was to find the willingness of the respondent to accept the vaccine (likely to intend to receive the vaccine), assessed by the question: “If the HPV vaccine is freely available in schools and clinics in India, would you receive it?” (possible responses: strongly agree, agree, neutral, disagree, strongly disagree). The secondary outcome measure was to find out the willingness of the participant to recommend the HPV vaccine to others, assessed by the question: “If the HPV vaccine was freely available in schools and clinics in India, would you recommend the vaccine to others?” (possible responses: strongly agree, agree, neutral, disagree, strongly disagree).
Knowledge score
The knowledge section included 20 statements (true or false) regarding HPV infection (10 questions) and HPV vaccine (10 questions). Each accurate response to the 20 knowledge questions HPV infection or vaccine received one point, while zero point was given to an incorrect or ‘I do not know’ or a missing response. The knowledge score was dichotomized to facilitate statistical analyses with higher knowledge considered as 10 or more points on the knowledge scale. Higher knowledge score suggested that the participants were more knowledgeable about HPV infection and vaccination.
Attitude score
The attitude section included 25 statements regarding attitude towards HPV vaccination. A 5-point Likert scale was used to compute the attitude score based on the participant responses to the 25 attitude statements: Strongly Agree (1 point), Agree (2 points), Neutral (3 points), Disagree (4 points), and Strongly Disagree (5 points). Thus, the total attitude score corresponding to each respondent could range from 25 to 125. The attitude score was converted into a scale of 1–5. Positive attitude towards HPV vaccination correlated to an attitude score near 1.
Statistical analysis
All statistical analyses were carried out using the Statistical Package for the Social Sciences (SPSS), (version 20.0; SPSS, Chicago, Illinois, USA). Sociodemographic characteristics are presented as frequencies and percentages. The data was summarized using descriptive statistics and first analysed using bivariate analysis. A p value less than 0.05 were considered to be statistically significant. Bivariate analysis using Chi-Square test of independence and multivariate binary logistic regression analysis was used to examine factors associated with vaccine acceptability and recommendation of the vaccine to others.
Differences in HPV infection/vaccine knowledge scores were examined by gender and other demographic characteristics using the chi-squared test of independence. The same analysis was performed on the variables of age, course (whether MBBS or other course), year of study (whether clinical or non-clinical), economic status, father’s profession, mother’s profession and the sexual status. The variables which were found to be highly significant (p value <0.001) were age, course, year of study and the economic status. These significant variables were further considered for binary logistic regression analysis to evaluate which of these factors caused significant difference in the knowledge scores. On binary logistic regression analysis, only course, year of training and economic status caused significant effect on the knowledge score.
Bivariate analysis was done to check for the dependent variable of HPV vaccine acceptability (likely to intend to receive the vaccine) and recommendation of the vaccine to others on gender, age, course, year, socioeconomic status, parents’ profession, smoking and alcohol status, and sexual experience. The inference was drawn using the Chi-Square test of independence of attributes. These tests found that age, course, alcohol use, knowledge and attitude scores had shown significant influence on the acceptability of the vaccine. For recommendation of the vaccine to others, variables of age, degree course, year of training, socioeconomic status, alcohol use, knowledge and attitude scores had shown similar significant influence.
Variables that were found to be significant on bivariate analysis (p value <0.05) were then considered for binary logistic regression analysis to evaluate which of these variables cause significant effect on the dependent variable (Intention to receive the HPV vaccine and Recommendation of the vaccine to others). The association measure was calculated using adjusted odds ratios (OR) and 95% confidence intervals.
Acknowledgments
We thank all the students for their participation.
Disclosure of potential conflicts of interest
No potential conflicts of interest were disclosed
References
- 1.Ferlay J, Soerjomataram I, Ervik M, Dikshit R, Eser S, Mathers C, Rebelo M, Parkin DM, Forman D, Bray F.. GLOBOCAN 2012 v1.0, Cancer incidence and mortality worldwide: IARC CancerBase No. 11 [Internet] Lyon (France): International Agency for Research on Cancer; 2013 [accessed 2018 July28] http://globocan.iarc.fr. [Google Scholar]
- 2.Bruni L, Barrionuevo-Rosas L, Albero G, Serrano B, Mena M, Gómez D, Muñoz J, Bosch FX, de Sanjosé S. ICO/IARC information centre on HPV and cancer (HPV information centre). Human Papillomavirus and Related Diseases in India. Summary Report; 2017. July27 [accessed 2018 Jul 21]. http://www.hpvcentre.net/statistics/reports/IND.pdf.
- 3.Sankaranarayannan R, Bhatla N, Basu P. Current global status & impact of human papillomavirus vaccination: implications for India. Indian J Med Res. 2016;144(2):169–180. PMID 27934795. doi: 10.4103/0971-5916.195023 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 4.Brianti P, De Flammineis E, Mercuri SR. Review of HPV-related diseases and cancers. New Microbiol. 2017;40(2):80–85. PMID:28368072. [PubMed] [Google Scholar]
- 5.Herrero R, González P, Markowitz LE. Present status of human papillomavirus vaccine development and implementation. Lancet Oncol. 2015;16(5):e206–16. doi: 10.1016/S1470-2045(14)70481-4. [DOI] [PubMed] [Google Scholar]
- 6.Chatterjee S, Chattopadhyay A, Samanta L, Panigrahi P. HPV and cervical cancer epidemiology – current status of HPV vaccination in India. Asian Pac J Cancer Prev. 2016;17(8):3663–73. PMID: 27644600. [PubMed] [Google Scholar]
- 7.Prinja S, Bahuguna P, Faujdar DS, Jyani G, Srinivasan R, Ghoshal S, Suri V, Singh MP, Kumar R. Cost-effectiveness of human papillomavirus vaccination for adolescent girls in Punjab State: implications for India’s universal immunization program. Cancer. 2017;123(17):3253–60. doi: 10.1002/cncr.30734. [DOI] [PubMed] [Google Scholar]
- 8.The Indian Express Delhi first state to launch HPV vaccine as public health programme in schools; 2016. March 1 [accessed 2018 Sep 28]. https://indianexpress.com/article/cities/delhi/delhi-first-state-to-launch-hpv-vaccine-as-public-health-programme-in-schools/.
- 9.World Health Organization Punjab launches HPV vaccine with WHO support.[accessed 2018. September 28]. http://www.searo.who.int/india/mediacentre/events/2016/Punjab_HPV_vaccine/en/.
- 10.World Health Organization Immunizations, vaccines and biologicals: human papillomavirus (HPV). Geneva, WHO; 2016. [accessed 2018 September 28]. http://www.who.int/immunization/diseases/hpv/en/.
- 11.Indian Academy of Pediatrics Committee on Vaccines and Immunization Practices (IAP COVI) Cervical cancer and HPV vaccines; [accessed 2018. September 28]. http://acvip.org/parents/columns/cervical-cancer.php.
- 12.Shrinivasan S. HPV vaccine trials and sleeping watchdogs. Indian J Med Ethics. 2011;8(2):73–74. doi: 10.20529/IJME.2011.031. [DOI] [PubMed] [Google Scholar]
- 13.Basu P, Mittal S. Acceptability of human papillomavirus vaccine among the urban, affluent and educated parents of young girls residing in Kolkata, Eastern India. J Obstet Gynaecol Res. 2011;37(5):393–401. doi: 10.1111/j.1447-0756.2010.01371.x. [DOI] [PubMed] [Google Scholar]
- 14.Paul P, Tanner AE, Gravitt PE, Vijayaraghavan K, Shah KV, Zimet GD, Study GC. Acceptability of HPV vaccine implementation among parents in India. Health Care Women Int. 2014; 35(10): 1148–1161. PMID: 23611111. doi: 10.1080/07399332.2012.740115 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 15.Pandey D, Vanya V, Bhagat S, Vs B, Shetty J. Awareness and attitude towards human papillomavirus (HPV) vaccine among medical students in a premier medical school in India. PLoS One. 2012;7(7):e40619. doi: 10.1371/journal.pone.0040619. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 16.Swarnapriya K, Kavitha D, Reddy GM. Knowledge, attitude and practices regarding HPV vaccination among medical and para medical students, India: a cross sectional study. Asian Pac J Cancer Prev. 2015;16(18):8473–8477. PMID: 26745104. [DOI] [PubMed] [Google Scholar]
- 17.Mehta S, Rajaram S, Goel G, Goel N. Awareness about Human papilloma virus and its vaccine among medical students. Indian J Community Med. 2013;38(2):92–94. doi: 10.4103/0970-0218.112438. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 18.Joy T, Sathian B, Bhattarai C, Chacko J. Awareness of cervix cancer risk factors in educated youth: a cross-sectional, questionnaire based survey in India, Nepal, and Sri Lanka. Asian Pac J Cancer Prev. 2011;12(7):1707–1712. PMID: 22126549. [PubMed] [Google Scholar]
- 19.Mitchell AW, Ely G. A pilot study of knowledge and attitudes toward HPV and HPV vaccine in an appalachian Kentucky county; 2008. [accessed 2017 August 05]. www.uky.edu/Programs/CREEK/pdf/MitchellElyHpv.pdf.
- 20.Waller J, McCaffery K, Forrest S, Szarewski A, Cadman L, Wardle J. Awareness of human papillomavirus among women attending a well woman clinic. Sex Transm Infect. 2003;79(4):320–322. PMID:12902585. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 21.Pan XF, Zhao ZM, Sun J, Chen F, Wen QL, Liu K, Song GQ, Zhang JJ, Wen Y, Fu CJ, et al. Acceptability and correlates of primary and secondary prevention of cervical cancer among medical students in southwest China: implications for cancer education. PLoS One. 2014;9(10):e110353. doi: 10.1371/journal.pone.0110353. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 22.Wen Y, Pan XF, Zhao ZM, Chen F, Fu CJ, Li SQ, Zhao Y, Chang H, Xue QP, Yang CX. Knowledge of human papillomavirus (HPV) infection, cervical cancer, and HPV vaccine and its correlates among medical students in southwest China: a multi-center cross-sectional survey. Asian Pac J Cancer Prev. 2014;15(14):5773–5779. PMID: 25081700. [DOI] [PubMed] [Google Scholar]
- 23.Dany M, Chidiac A, Nassar AH. Human papillomavirus vaccination: assessing knowledge, attitudes, and intentions of college female students in Lebanon, a developing country. Vaccine. 2015;33(8):1001–1007. doi: 10.1016/j.vaccine.2015.01.009. [DOI] [PubMed] [Google Scholar]
- 24.Rashwan HH1, Nz S, Abd MDN. Knowledge, attitude and practice of Malaysian medical and pharmacy students towards human papillomavirus vaccination. Asian Pacific J Cancer Prev, 2012; 13(5): 2279–2283. PMID: 22901207. doi: 10.7314/APJCP.2012.13.5.2279 [DOI] [PubMed] [Google Scholar]
- 25.Fu CJ, Pan XF, Zhao ZM, Saheb-Kashaf M, Chen F, Wen Y, Yang CX, Zhong XN. Knowledge, perceptions and acceptability of HPV vaccination among medical students in Chongqing, China. Asian Pac J Cancer Prev. 2014;15:6187–6193. PMID: 25124596. [DOI] [PubMed] [Google Scholar]
- 26.Chang IJ, Huang R, He W, Zhang SK, Wang SM, Zhao FH, Smith JS, Qiao YL. Effect of an educational intervention on HPV knowledge and vaccine attitudes among urban employed women and female undergraduate students in China: a cross-sectional study. BMC Public Health. 2013;13:916. doi: 10.1186/1471-2458-13-916. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 27.Dempsey AF, Davis MM. Overcoming barriers to adherence to HPV vaccination recommendations. Am J Manag Care. 2006. December;12(17Suppl):S484–91. PMID:17203992. [PubMed] [Google Scholar]
- 28.Kamini S, Bhimarasetty DM. Awareness about human papilloma virus vaccine among medical students. Asian J MediSci. 2016;7(4):64–67. doi: 10.3126/ajms.v7i4.14613. [DOI] [Google Scholar]
- 29.Rashid S, Labani S, Das BC. Knowledge, awareness and attitude on HPV, HPV vaccine and cervical cancer among the college students in India. PLoS One. 2016;11(11):e0166713. doi: 10.1371/journal.pone.0166713. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 30.Bhatla N, Joseph E. Cervical cancer prevention & the role of human papillomavirus vaccines in India. Indian J Med Res. 2009;130(3):334–340. PMID: 19901443. [PubMed] [Google Scholar]
- 31.Parikh S, Brennan P, Boffetta P. Meta‐analysis of social inequality and the risk of cervical cancer. Int J Cancer. 2003;105(5):687–691. doi: 10.1002/ijc.11141. [DOI] [PubMed] [Google Scholar]
- 32.Gilkey MB, McRee AL. Provider communication about HPV vaccination: A systematic review. Hum Vaccin Immunother. 2016;12(6):1454–1468. PMID: 26838681. doi: 10.1080/21645515.2015.1129090 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 33.Kahn JA, Rosenthal SL, Hamann T, Bernstein DJ. Attitudes about human papillomavirus vaccine in young women. Int J STD AIDS. 2003;14:300–306. PMID:12803935. doi: 10.1258/095646203321605486. [DOI] [PubMed] [Google Scholar]
- 34.Davis K, Ed D, Ferris D, Jk D. Human papillomavirus vaccine acceptability among parents of 10- to 15-year-old adolescents. J Low Genit Tract Dis. 2004;8:188–194. PMID: 15874862. [DOI] [PubMed] [Google Scholar]
- 35.Dempsey AF, Zimet GD, Davis RL, Koutsky L. Factors that are associated with parental acceptance of human papillomavirus vaccines: a randomized intervention study of written information about HPV. Pediatrics. 2006;117:1486–1493. PMID: 16651301. doi: 10.1542/peds.2005-1381. [DOI] [PubMed] [Google Scholar]
- 36.Madhivanan P, Krupp K, Yashodha MN, Marlow L, Klausner JD, Arthur L, Reingold LA. Attitudes toward HPV vaccination among parents of adolescent girls in Mysore, India. Vaccine. 2009;27(38):5203–5208. doi: 10.1016/j.vaccine.2009.06.073. [DOI] [PubMed] [Google Scholar]
- 37.Unger Z, Maitra A, Kohn J, Devaskar S, Stern L, Patel A. Knowledge of HPV and HPV vaccine among women aged 19 to 26. Womens Health Issues. 2015;25(5):458–462. doi: 10.1016/j.whi.2015.06.003. [DOI] [PubMed] [Google Scholar]
- 38.Michail G, Smaili M, Vozikis A, Jelastopulu E, Adonakis G, Poulas K. Female students receiving post-secondary education in Greece: the results of a collaborative human papillomavirus knowledge survey. Public Health. 2014;128(12):1099–2005. doi: 10.1016/j.puhe.2014.09.005. [DOI] [PubMed] [Google Scholar]
- 39.Zhang SK, Pan XF, Wang SM, Yang CX, Gao XH, Wang ZZ, Li M, Ren ZF, Zhao FH, Qiao YL. Perceptions and acceptability of HPV vaccination among parents of young adolescents: a multicenter national survey in China. Vaccine. 2013;31(32):3244–3249. doi: 10.1016/j.vaccine.2013.05.046. [DOI] [PubMed] [Google Scholar]
- 40.DiAngi YT, Panozzo CA, Ramogola-Masire D, Steenhoff AP, Brewer NT. A cross-sectional study of HPV vaccine acceptability in Gaborone, Botswana. PLoS One. 2011;6(10):e25481. doi: 10.1371/journal.pone.0025481. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 41.Coleman MA, Levison J, Sangi-Haghpeykar H. HPV vaccine acceptability in Ghana, West Africa. Vaccine. 2011;29(23):3945–3950. doi: 10.1016/j.vaccine.2011.03.093. [DOI] [PubMed] [Google Scholar]
- 42.Brabin L, Roberts SA, Stretch R, Baxter D, Chambers G, Kitchener H, McCann R. Uptake of first two doses of human papillomavirus vaccine by adolescent schoolgirls in Manchester: prospective cohort study. BMJ. 2008;336(7652):1056–1058. doi: 10.1136/bmj.39541.534109.BE. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 43.Reeve C, De La Rue S, Pashen D, Culpan M, Cheffins T. School-based vaccinations delivered by general practice in rural north Queensland: an evaluation of a new human papilloma virus vaccination program. Commun Dis Intell Q Rep. 2008;32(1):94–98. PMID:18522312. [PubMed] [Google Scholar]
- 44.Schnaith AM, Evans EM, Vogt C, Tinsay AM, Schmidt TE, Tessier KM, Erickson BK. An innovative medical school curriculum to address human papillomavirus vaccine hesitancy. Vaccine. 2018;36(26):3830–3835. PMID: 9286828. doi: 10.1016/j.vaccine.2018.05.014 [DOI] [PMC free article] [PubMed] [Google Scholar]
Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Data Citations
- Bruni L, Barrionuevo-Rosas L, Albero G, Serrano B, Mena M, Gómez D, Muñoz J, Bosch FX, de Sanjosé S. ICO/IARC information centre on HPV and cancer (HPV information centre). Human Papillomavirus and Related Diseases in India. Summary Report; 2017. July27 [accessed 2018 Jul 21]. http://www.hpvcentre.net/statistics/reports/IND.pdf.