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Factors Associated With Intention-to-Recommend Human Papillomavirus Vaccination Among Physicians in Mysore, India
Journal of Adolescent Health 46 (2010) 379–384
Original article
Factors Associated With Intention-to-Recommend Human Papillomavirus Vaccination Among Physicians in Mysore, India Karl Krupp, M.P.H.a, Laura A.V. Marlow, Ph.D.b, Karina Kielmann, Ph.D.c, Narayanappa Doddaiah, M.D.d, Shekar Mysore, M.D.e, Arthur L. Reingold, M.D.f, and Purnima Madhivanan, M.B.B.S., M.P.H., Ph.D.a,g,* b
a Public Health Research Institute, Mysore, India Department of Epidemiology and Public Health, Health Behaviour Research Centre, University College London, London, United Kingdom c London School of Hygiene and Tropical Medicine, London, United Kingdom d JSS Medical College & Hospital, Mysore, India e Mysore Medical College & Research Institute, Mysore, India f School of Public Health, University of California, Berkeley, California g San Francisco Department of Public Health, San Francisco, California Manuscript received May 18, 2009; manuscript accepted October 6, 2009
Abstract
Purpose: This qualitative study investigated physician intention-to-recommend the human papillomavirus (HPV) vaccine to parents of adolescent girls in India. There are currently no data on attitudes to HPV vaccination among healthcare providers in India. Methods: Between June and August 2008, 20 semistructured qualitative in-depth interviews were conducted among physicians from a range of specialties and practice settings in Mysore District, India. Physicians were interviewed about their specialty and the types of patients they saw in their practice, attitudes toward recommending HPV vaccination to parents of adolescent girls, perceived subjective norms surrounding the promotion of vaccines in their work settings, and their perceptions regarding self-efficacy in recommending the HPV vaccine. Results: The study found that knowledge about HPV infection and its relationship to cervical cancer was low among physicians across specialties. While most physicians expressed positive attitudes toward vaccination in general, and HPV vaccination in particular, the overwhelming majority believed that few of their patients would react positively to a vaccine recommendation. Physicians were concerned about talking to parents about their adolescent daughters’ reproductive lives. Certain specialties, particularly obstetrician/gynecologists, suggested that recommending immunization was not appropriate in their work setting. Conclusion: With the HPV vaccine recently being approved in India, there is a strong need to provide more education for physicians about the relationship of HPV infection and cervical cancer and the benefits of vaccinating adolescent girls to prevent cervical cancer in the future. Ó 2010 Society for Adolescent Medicine. All rights reserved.
Keywords:
Human papillomavirus; India; Physicians; Adolescent; Vaccine; Acceptability
PATH USA had no role in the study design, conduct, collection, management, analysis, or interpretation of the data or preparation, review, or approval of the manuscript. *Address correspondence to: Purnima Madhivanan, M.B.B.S., M.P.H., Ph.D., San Francisco Department of Public Health, 1360 Mission Street, Suite 401, San Francisco, CA 94103. E-mail address: [email protected]
Human papillomavirus (HPV) is one of the most common sexually transmitted infections in the world [1], with more than four of five sexually active people acquiring a genital HPV infection at some point in their lifetime [2]. Risk of acquiring the HPV virus is highest among young women, with most infections occurring soon after the initiation of sexual activity [3–5]. Although the majority of infections clear naturally, persistent infection with high-risk HPV
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strains has been shown to cause cervical, vulval, vaginal, and anal cancers, and infection with low-risk HPV (the nononcogenic types) causes genital warts [6]. Two new vaccines have been introduced that protect against high-risk HPV strains responsible for up to 70% of cervical cancer cases. Approved for girls aged 9 to 26 years, the vaccines have been shown to be highly effective in preventing infection with HPV 16 and 18, and protection has been shown to persist for at least 5 years [6]. In many parts of the world, successful uptake of the vaccine will depend in part on whether physicians, including pediatricians and gynecologists, recommend HPV vaccination for their adolescent female patients [7,8]. Understanding more about the knowledge, attitudes, and beliefs of healthcare providers regarding HPV vaccination will therefore be an important first step in ensuring the success of vaccine rollouts. An overwhelming majority of studies on acceptability of HPV vaccination among physicians have been carried out in developed countries [9–19]. Studies that investigated knowledge of HPV and cervical cancer have shown that awareness varies widely by specialty and training [9– 12,19]. When physicians were asked to rate the most important features of an HPV vaccine, responses included good efficacy [13,16,20], high levels of vaccine safety [14,20], and adequate vaccine distribution [15]. Anticipated barriers among physicians included cost [10,21], lack of HPV and cervical cancer knowledge among parents [12–14,17,18], 9 to 13 years as the age for vaccine administration [10], and reluctance to discuss sexuality [12–14]. The age at which physicians felt that females should be vaccinated varied. In two studies, a majority of physicians supported vaccination of 9 to 13-year-old girls [13,15], whereas in other studies, physicians reported preferences for vaccinating girls at ages ranging from 14 to 18 years [9,10,20]. The Government of India has recently approved an optional HPV vaccine for adolescent girls aged 9 to 26 years. Optional vaccines are available in the private sector but are not part of the government universal immunization schedule that provides tuberculosis, diphtheria, pertussis, polio, measles, and tetanus immunization to children and pregnant women. As a consequence, parents usually only learn about these vaccines from their family physician. Pediatricians and family practitioners typically recommend childhood vaccinations such as those against typhoid, H. influenzae type b, varicella, Hepatitis A, and influenza; whereas obstetrician/gynecologists usually only promote the tetanus vaccine to their antenatal cases. As policymakers try to better understand how to optimize uptake of an HPV vaccine, it will be critical to know whether physicians will recommend HPV immunization for their adolescent female patients. This study investigated the knowledge, attitudes, and intention to recommend HPV vaccination to parents of adolescent girls among health care providers in Mysore, India.
Methods Study location and population The study was conducted in Mysore City, the administrative capital of Mysore District. The district is located in the southern part of the state of Karnataka, India. It is bounded by Mandya District to the northeast, Chamrajanagar District to the southeast, Kerala state to the south, Kodagu District to the west, and Hassan District to the north. The district has a population of 2,641,027 (2001 census), of which 37% is urban and 63% rural. Hindus constitute 87% of the population, Muslims 8.9%, and the remainder is made up of Christians, Buddhists, and other religious groups. Kannada and Urdu are the dominant languages in this region, and 64% of population is literate. We conducted 20 in-depth interviews between June and August 2008 with physicians from Mysore District. The number of interviews was selected a priori to ensure that data were obtained from a broad mix of specialties and practice settings serving adolescent girl patients. Interviewees were referred from the Public Health Research Institute partner organizations or identified through snowball sampling (asking recruited participants to refer colleagues who met the study criteria). To be included in the study, physicians had to fulfill the following criteria: they should have practiced for more than a year, they should be currently practicing allopathic medicine (pediatrics, family practice, general practice, or a general internist specialty) in Mysore District, spending more than 20 hours a week in direct patient care, and they should have more than 20% female patients between 9 and 15 years of age. On being identified as potential participants, physicians were sent a letter requesting an interview. After the letter, they were telephoned to ascertain their interest and after the informed consent process, an interview was scheduled for a convenient time and location. Before conducting the interview, they were provided with general information about the interview topic, told that the interview would be recorded, provided with an assurance that their responses would remain confidential, and asked to sign a formal consent form. The interviews were conducted in English and lasted between 45–60 minutes. All interviews were recorded and transcribed verbatim. Respondents received no remuneration for participation. The protocol for this study was approved by the Ethics Committee at PATH, USA and the Institutional Ethics Review Board at C.S.I. Holdsworth Memorial Hospital in Mysore, India. Interview guide development A screener instrument and an interview guide were developed for the study. The guide was based on a review of the relevant literature on physician attitudes toward HPV vaccination. It explored physician knowledge about HPV, cervical cancer, and HPV vaccination; attitudes toward recommending an HPV vaccine; perceptions about the
K. Krupp et al. / Journal of Adolescent Health 46 (2010) 379–384
attitudes of the management and colleagues towards recommending immunization against HPV; and barriers and facilitators to HPV vaccine recommendation and uptake of the vaccine among parents of adolescent girls. Before use, the guide was pretested in four mock interviews with physicians at C.S.I. Holdsworth Memorial Hospital, and revisions were made to ensure that there was sufficient time to cover all topics. Data analysis The study used an iterative analytic process where the investigator reviewed sets of three to four transcripts independently to identify key themes. Emergent themes were used to develop a preliminary framework. Subsequent sets of interviews were similarly assessed with the goal of further clarifying core themes. Once a final set of themes was selected, all transcripts were reanalyzed using the final framework. Quotations were selected based on whether they were illustrative of either widely held or deviant views. Because of the small number of interviews, analysis was conducted manually without the assistance of qualitative data analysis software for coding and text retrieval. Results Sample description The mean age of the participants was 31 years (range 28– 43 yrs). Eight (40%) were male, and 12 (60%) were female. Six participants (30%) specialized in obstetrics/gynecology, nine (45%) in pediatrics, and five (25%) in either family or general practices. Eight of the physicians (40%) owned their private practice, three (15%) worked in government hospitals, and the remainder (nine, 45%) worked in private hospitals. The vast majority (15, 75%) practiced in urban settings whereas the remainder (five, 25%) worked in periurban or rural locations in Mysore District. Physician attitudes about recommending HPV vaccination Most physicians interviewed (18, 90%) stated that physicians should recommend HPV vaccination to their patients. In most cases this view seemed to be related to positive views about vaccination in general as opposed to the HPV vaccine in particular. More than half of the participants (13, 65%) admitted to having little or no information about the HPV vaccine, although all said they had heard about the relationship between HPV infection and cervical cancer before being invited to the study. A pediatrician expressed this commonly held view in the following way: ‘‘I will recommend the [HPV] vaccine because cancer [of the] cervix is one thing the whole of Indian women are scared of. Prevention is always better than a cure.[but] most doctors don’t know [enough about] this vaccine. If they knew more they would push it through.’’
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The two physicians who felt that recommending HPV vaccination was not appropriate at the present time also cited lack of knowledge as the main reason for their reservation. A pediatrician who had more than 20 years of experience in vaccination programs expressed his reasons in the following way: ‘‘I don’t recommend unless there is full knowledge of side effects and safety.If there is any accident or some intolerable side effect the public opinion can be very bad. We had some incidents with measles vaccinations; there was a furor about it [across] the whole country. Once it gets into news media, it has a negative effect on our other immunizations so I won’t recommend it unless I’m sure it’s safe.’’
Despite the fact that most participants expressed broadly positive views about HPV vaccination, many had mixed feelings about whether recommending the vaccine would help to encourage uptake among their patients The high cost of the HPV vaccine, at rupees 8400 (USD $186) for three doses, was the most commonly mentioned obstacle to vaccine uptake. The majority of physicians (16, 80%) expressed concern that most patients would be unable to afford the vaccine unless it became part of India’s Universal Immunization Program schedule. A pediatrician working in a private hospital summarized it this way: ‘‘People have money, but they don’t want to spend. A vaccine like this has to be pocket-friendly otherwise people won’t take it. I treated a child with Pneumonia. He almost died but his family was still hesitating to immunize [their] other children with Pneumococcal vaccine. They said they will think about it and then left. They are optional vaccines. so people resist. I asked them ‘Is your child optional?’ but they don’t listen. This will be the biggest problem with the HPV vaccine. Unless it is part of the immunization schedule most people won’t take it even if I tell them they should.’’
According to physicians, the second most common reason for parents not electing their daughters for vaccination despite recommendation was that the vaccine offered protection against a sexually transmitted infection. Parents did not want to acknowledge that their daughters would become sexually active, and therefore believed that they were unlikely to be exposed to the HPV infection. An obstetrician/gynecologist working in private practice expressed this concern in the following way: ‘‘These things are very personal, particularly in our country. People don’t want to talk to their children about sex. It becomes very difficult so I think most of my patients will not respond well..Maybe when we are talking about menstrual hygiene we can be indirectly talking about some subjects. Talking about sexually transmitted infections is hard since most people won’t think their daughter could be sexually active. This is a problem for this vaccine.Most parents will not consider it and I think it would be hard in a private practice to try to make people understand why they should take it.’’
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Subjective norms impacting physician intention to recommend HPV vaccination Although many expressed positive attitudes toward vaccines in general and the HPV vaccine in particular, most were quick to point out that recommending vaccination was not appropriate in their work setting. An obstetrician/gynecologist practicing in a government hospital expressed it in the following way: ‘‘Our work is mainly dealing with pregnancy and reproductive problems such as white discharge and other things like menstrual problems. Our patients are not expecting us to talk about immunization. That is Pediatrics. They would not come to us for that.’’
Other specialties, including pediatrics, family practice, and general practice seemed to feel that promotion of immunization was an appropriate and important role in their specialty. A pediatrician in a government hospital summarized how he felt about promoting vaccination: ‘‘We are taught this way. Immunization is better than disease. I start to educate my patients from newborn about diseases that can be prevented. I explain to them what is likely to come and what is preventable. I have 25 years of practice in pediatrics so I am strong about prevention. I will not care for a patient without making sure about their status even with optional vaccines like Hepatitis B and pneumococcal vaccines.’’
Seven of the nine (78%) pediatricians interviewed in the study indicated that they looked to the Indian Academy of Pediatrics (IAP) for guidance on vaccines and immunization. Several of the participants indicated that they would not promote any vaccine, which had not been recommended by the IAP Committee on Immunization. A pediatrician working in a large private hospital described his reasons for relying on the IAP in this way: ‘‘As Pediatricians we need to keep in touch with journals, with the latest developments, and newer vaccines in the pipeline. I take the words of the Indian Academy of Pediatrics because they conduct updates on immunizations and give us information on new vaccines and safety. In last 10 years, I recommended the hemophilus influenzae conjugate vaccine and pneumococcal vaccine because of IAP recommendations.’’
Interestingly, there were no other professional associations mentioned by physicians. Several (two, 10%) said they relied on information from continuing education meetings at their hospital or clinic, one physician (5%) said that he looked to the World Health Organization for vaccine information, and 14 of the 20 physicians (70%) indicated they relied on journals in their field. Perceived behavioral control and physician intention to recommend HPV vaccination The most common perceived difficulty mentioned by physicians was the lack of time to counsel patients because
of the high caseloads. Physicians in a government hospital setting typically see more that 40 patients during a workday—and this equates to less than 10 minutes per consultation. In such a situation, many of the physicians felt that it would be difficult to recommend an optional vaccination like the HPV vaccine in this limited period. A pediatrician working in a government hospital explained it this way: ‘‘We have morning OPD. maybe 25 or 30 patients. It is difficult to talk in-depth. We try to make sure of the main vaccinations. People know from the government schedule so it is not so hard. An optional vaccine.this is harder. If they have read and come to us to ask it is ok because they are already aware, then it is different. If they are not, it is hard to answer [questions] in a short time.’’
As mentioned earlier, another perceived difficulty mentioned by physicians was talking with parents about a vaccine for a sexually transmitted infection for their adolescent daughters. In general, the pediatricians were the least concerned about their patients’ reactions to this topic, whereas obstetricians and gynecologists expressed the most concern. Physicians based in private practices saw this as more of a concern than those working in either private or government hospitals. One obstetrician/gynecologist practicing in a private hospital expressed it this way: ‘‘This is very controversial. In our country there is trouble about whether sex education as such should be introduced to the adolescents in the school curriculum or not. This debate is going on and the government is against it. Many of these subjects are taboo, so it is hard for a doctor to talk about a vaccine that concerns sex especially if it’s about an adolescent girl of 9 or 10 years. It might be ok if it was just a cancer vaccine but not otherwise.’’
Finally, three of the physicians who worked in government hospitals said that they would be unable to recommend vaccines that were not currently part of the government universal vaccine schedule. A pediatrician at a major government hospital explained it this way: ‘‘It is a government setup. We must offer the vaccines that the government has decided. Also, most of our patients are from lower socioeconomic groups. They will take the compulsory vaccines but they don’t have money for other things.’’
Discussion This study examined knowledge and attitudes about HPV vaccination among healthcare providers from a mix of specialties and practice settings in Mysore, India. The study found that although most physicians expressed positive attitudes toward vaccination in general, and HPV vaccination in particular, an overwhelming majority believed that few of their patients would react positively to a vaccine recommendation. Many physicians providing services to adolescent girls aged 9 to 15 years, particularly those practicing
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obstetrics/gynecology, suggested that recommending immunization was not appropriate in their work setting—a belief that would likely constrain the promotion of the vaccine among adolescent girls. Additionally, it seemed that workplace constraints, particularly patient load was perceived by many physicians as a key obstacle in promoting the vaccine. In this case, many physicians seemed to think it would be very difficult to promote an optional vaccine, particularly one that could be considered controversial, to their patients. In general, Indian physicians had strikingly similar attitudes to their counterparts from other parts of the world. Like studies from the United States, many expressed concerns that parents would be worried that HPV vaccination may encourage risky sexual behaviors among their daughters [10]. As with others studies from both the developed and the developing world, they also perceived the same barriers to vaccine uptake including cost [10,21], reservations about recommending vaccination for girls 9 to 13 years as the age [10], and reluctance to discuss sexual issues with adolescent patients or their parents [12–14]. Also, as with studies from the United States, Canada, and Mexico, physician knowledge of cervical cancer, HPV, and HPV vaccination varied widely by training and specialty [9,10,19]. Because of the small sample and the qualitative nature of the study, the findings may not be representative of the views of all physicians in India. Additionally, we cannot rule out the possibility that additional important themes might have emerged if further interviews had been conducted. Furthermore physicians were asked to discuss their intention-torecommend an HPV vaccine, and this may not reflect their actual recommendations. Despite these limitations, these formative findings contribute to a conceptual framework to better understand the issues related to HPV vaccine acceptability in India. This study has focused on factors related to intention-torecommend HPV vaccination among healthcare providers in India, and the findings will be useful for planners working to increase uptake of this new vaccine against HPV. There seems to be a very low level of knowledge among providers about the vaccine, and the first challenge for policymakers is therefore to address this ‘knowledge gap’ if efforts to introduce the vaccine are to be successful. Second, while specialties like obstetrics/gynecology currently provide services to adolescent girls in the target age range, workplace norms seem to suggest that promotion of the HPV vaccine may not receive much support in this setting. Policymakers should consider working closely with obstetric and gynecology associations to change work norms and educate members about the value of primary as well as secondary prevention of cervical cancer. In addition, efforts to increase vaccine uptake should focus on specialties already familiar with the administration of childhood vaccines, particularly pediatricians and family practitioners. Finally, many physicians in India look at their professional organizations for information about vaccination, so communication strategies should target professional organizations and journals to provide
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information about the safety and efficacy of vaccines and giving general recommendations for HPV immunization. While this study points up some of the unique challenges of promoting the HPV vaccine among physicians in India, it also illustrates striking similarities in attitudes to their counterparts from other areas of the world. Given these parallels, it seems reasonable to suggest that policymakers should consider carefully the lessons learned about HPV immunization from both developed and developing countries as they consider how to best optimize uptake in India. Such an approach would help speed the day when cervical cancer will not be one of the major killers of women in India.
Acknowledgments The authors thank Thomas Butler, Yashodha MN, and Varalakshmi Chandrasekaran for assisting on the project and all the physicians who took the time to participate in the study. Special thanks to staff at Public Health Research Institute and CSI Holdsworth Memorial Hospital for helping carry out the research. Support for this project was provided by PATH, USA. The views expressed by the authors do not necessarily reflect the views of PATH.
References [1] Baseman JG, Koutsky LA. The epidemiology of human papillomavirus infections. J Clin Virol 2005;32(Suppl 1):S16–24. [2] Koutsky L. Epidemiology of genital human papillomavirus infection. Am J Med 1997;102(5A):3–8. [3] Braaten KP, Laufer MR. Human papillomavirus (HPV), HPVrelated disease, and the HPV vaccine. Rev Obstet Gynecol 2008; 1(1):2–10. [4] Zhang WY, Xue YZ, Chen M, et al. Prevalence of high-risk human papillomavirus infection in different cervical lesion among organized health-examination women in Shanghai, China. Chin Med J (Engl) 2008;121:1578–82. [5] Molano M, Posso H, Weiderpass E, et al. Prevalence and determinants of HPV infection among Colombian women with normal cytology. Br J Cancer 2002;87:324–33. [6] Stanley M. Prevention strategies against the human papillomavirus: the effectiveness of vaccination. Gynecol Oncol 2007;107(2 Suppl. 1): S19–23. [7] Tiro JA, Meissner HI, Kobrin S, Chollette V. What do women in the U.S. know about human papillomavirus and cervical cancer? Cancer Epidemiol Biomarkers Prev 2007;16(2):288–94. [8] Zimet GD, Mays RM, Winston Y, et al. Acceptability of human papillomavirus immunization. J Womens Health Gend Based Med 2000;9: 47–50. [9] Duval B, Gilca V, McNeil S, et al. Vaccination against human papillomavirus: A baseline survey of Canadian clinicians’ knowledge, attitudes and beliefs. Vaccine 2007;25:7841–7. [10] Daley MF, Liddon N, Crane LA, et al. A national survey of pediatrician knowledge and attitudes regarding human papillomavirus vaccination. Pediatrics 2006;118:2280–9. [11] Jain N, Irwin KL, Montano D, et al. Family physicians’ knowledge of genital human papillomavirus (HPV) infection and HPV-related conditions, United States, 2004. Fam Med 2006;38:483–9.
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[12] Esposito S, Bosis S, Pelucchi C, et al. Pediatrician knowledge and attitudes regarding human papillomavirus disease and its prevention. Vaccine 2007;25:6437–46. [13] Riedesel JM, Rosenthal SL, Zimet GD, et al. Attitudes about human papillomavirus vaccine among family physicians. J Pediatr Adolesc Gynecol 2005;18:391–8. [14] Kahn JA, Zimet GD, Bernstein DI, et al. Pediatricians’ intention to administer human papillomavirus vaccine: the role of practice characteristics, knowledge, and attitudes. J Adolesc Health 2005;37:502–10. [15] Raley JC, Followwill KA, Zimet GD, Ault KA. Gynecologists’ attitudes regarding human papilloma virus vaccination: A survey of Fellows of the American College of Obstetricians and Gynecologists. Infect Dis Obstet Gynecol 2004;12:127–33. [16] Kahn JA, Rosenthal SL, Tissot AM, et al. Factors influencing pediatricians’ intention to recommend human papillomavirus vaccines. Ambul Pediatr 2007;7:367–73.
[17] Jaspan DM, Dunton CJ, Cook TL. Acceptance of human papillomavirus vaccine by gynecologists in an urban setting. J Low Genit Tract Dis 2008;12:118–21. [18] Tissot AM, Zimet GD, Rosenthal SL, et al. Effective strategies for HPV vaccine delivery: The views of pediatricians. J Adolesc Health 2007;41: 119–25. [19] Aldrich T, Becker D, Garcı´a SG, Lara D. Mexican physicians’ knowledge and attitudes about the human papillomavirus and cervical cancer: A national survey. Sex Transm Infect 2005;81: 135–41. [20] de Carvalho NS, Teixeira LM, Pradel EM, et al. Vaccinating against HPV: physicians’ and medical students’ point of view. Vaccine 2009;27:2637–40. [21] Wong LP. Physicians’ experiences with HPV vaccine delivery: Evidence from developing country with multiethnic populations. Vaccine 2009;27:1622–7.
Original article
Factors Associated With Intention-to-Recommend Human Papillomavirus Vaccination Among Physicians in Mysore, India Karl Krupp, M.P.H.a, Laura A.V. Marlow, Ph.D.b, Karina Kielmann, Ph.D.c, Narayanappa Doddaiah, M.D.d, Shekar Mysore, M.D.e, Arthur L. Reingold, M.D.f, and Purnima Madhivanan, M.B.B.S., M.P.H., Ph.D.a,g,* b
a Public Health Research Institute, Mysore, India Department of Epidemiology and Public Health, Health Behaviour Research Centre, University College London, London, United Kingdom c London School of Hygiene and Tropical Medicine, London, United Kingdom d JSS Medical College & Hospital, Mysore, India e Mysore Medical College & Research Institute, Mysore, India f School of Public Health, University of California, Berkeley, California g San Francisco Department of Public Health, San Francisco, California Manuscript received May 18, 2009; manuscript accepted October 6, 2009
Abstract
Purpose: This qualitative study investigated physician intention-to-recommend the human papillomavirus (HPV) vaccine to parents of adolescent girls in India. There are currently no data on attitudes to HPV vaccination among healthcare providers in India. Methods: Between June and August 2008, 20 semistructured qualitative in-depth interviews were conducted among physicians from a range of specialties and practice settings in Mysore District, India. Physicians were interviewed about their specialty and the types of patients they saw in their practice, attitudes toward recommending HPV vaccination to parents of adolescent girls, perceived subjective norms surrounding the promotion of vaccines in their work settings, and their perceptions regarding self-efficacy in recommending the HPV vaccine. Results: The study found that knowledge about HPV infection and its relationship to cervical cancer was low among physicians across specialties. While most physicians expressed positive attitudes toward vaccination in general, and HPV vaccination in particular, the overwhelming majority believed that few of their patients would react positively to a vaccine recommendation. Physicians were concerned about talking to parents about their adolescent daughters’ reproductive lives. Certain specialties, particularly obstetrician/gynecologists, suggested that recommending immunization was not appropriate in their work setting. Conclusion: With the HPV vaccine recently being approved in India, there is a strong need to provide more education for physicians about the relationship of HPV infection and cervical cancer and the benefits of vaccinating adolescent girls to prevent cervical cancer in the future. Ó 2010 Society for Adolescent Medicine. All rights reserved.
Keywords:
Human papillomavirus; India; Physicians; Adolescent; Vaccine; Acceptability
PATH USA had no role in the study design, conduct, collection, management, analysis, or interpretation of the data or preparation, review, or approval of the manuscript. *Address correspondence to: Purnima Madhivanan, M.B.B.S., M.P.H., Ph.D., San Francisco Department of Public Health, 1360 Mission Street, Suite 401, San Francisco, CA 94103. E-mail address: [email protected]
Human papillomavirus (HPV) is one of the most common sexually transmitted infections in the world [1], with more than four of five sexually active people acquiring a genital HPV infection at some point in their lifetime [2]. Risk of acquiring the HPV virus is highest among young women, with most infections occurring soon after the initiation of sexual activity [3–5]. Although the majority of infections clear naturally, persistent infection with high-risk HPV
1054-139X/10/$ – see front matter Ó 2010 Society for Adolescent Medicine. All rights reserved. doi:10.1016/j.jadohealth.2009.10.001
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strains has been shown to cause cervical, vulval, vaginal, and anal cancers, and infection with low-risk HPV (the nononcogenic types) causes genital warts [6]. Two new vaccines have been introduced that protect against high-risk HPV strains responsible for up to 70% of cervical cancer cases. Approved for girls aged 9 to 26 years, the vaccines have been shown to be highly effective in preventing infection with HPV 16 and 18, and protection has been shown to persist for at least 5 years [6]. In many parts of the world, successful uptake of the vaccine will depend in part on whether physicians, including pediatricians and gynecologists, recommend HPV vaccination for their adolescent female patients [7,8]. Understanding more about the knowledge, attitudes, and beliefs of healthcare providers regarding HPV vaccination will therefore be an important first step in ensuring the success of vaccine rollouts. An overwhelming majority of studies on acceptability of HPV vaccination among physicians have been carried out in developed countries [9–19]. Studies that investigated knowledge of HPV and cervical cancer have shown that awareness varies widely by specialty and training [9– 12,19]. When physicians were asked to rate the most important features of an HPV vaccine, responses included good efficacy [13,16,20], high levels of vaccine safety [14,20], and adequate vaccine distribution [15]. Anticipated barriers among physicians included cost [10,21], lack of HPV and cervical cancer knowledge among parents [12–14,17,18], 9 to 13 years as the age for vaccine administration [10], and reluctance to discuss sexuality [12–14]. The age at which physicians felt that females should be vaccinated varied. In two studies, a majority of physicians supported vaccination of 9 to 13-year-old girls [13,15], whereas in other studies, physicians reported preferences for vaccinating girls at ages ranging from 14 to 18 years [9,10,20]. The Government of India has recently approved an optional HPV vaccine for adolescent girls aged 9 to 26 years. Optional vaccines are available in the private sector but are not part of the government universal immunization schedule that provides tuberculosis, diphtheria, pertussis, polio, measles, and tetanus immunization to children and pregnant women. As a consequence, parents usually only learn about these vaccines from their family physician. Pediatricians and family practitioners typically recommend childhood vaccinations such as those against typhoid, H. influenzae type b, varicella, Hepatitis A, and influenza; whereas obstetrician/gynecologists usually only promote the tetanus vaccine to their antenatal cases. As policymakers try to better understand how to optimize uptake of an HPV vaccine, it will be critical to know whether physicians will recommend HPV immunization for their adolescent female patients. This study investigated the knowledge, attitudes, and intention to recommend HPV vaccination to parents of adolescent girls among health care providers in Mysore, India.
Methods Study location and population The study was conducted in Mysore City, the administrative capital of Mysore District. The district is located in the southern part of the state of Karnataka, India. It is bounded by Mandya District to the northeast, Chamrajanagar District to the southeast, Kerala state to the south, Kodagu District to the west, and Hassan District to the north. The district has a population of 2,641,027 (2001 census), of which 37% is urban and 63% rural. Hindus constitute 87% of the population, Muslims 8.9%, and the remainder is made up of Christians, Buddhists, and other religious groups. Kannada and Urdu are the dominant languages in this region, and 64% of population is literate. We conducted 20 in-depth interviews between June and August 2008 with physicians from Mysore District. The number of interviews was selected a priori to ensure that data were obtained from a broad mix of specialties and practice settings serving adolescent girl patients. Interviewees were referred from the Public Health Research Institute partner organizations or identified through snowball sampling (asking recruited participants to refer colleagues who met the study criteria). To be included in the study, physicians had to fulfill the following criteria: they should have practiced for more than a year, they should be currently practicing allopathic medicine (pediatrics, family practice, general practice, or a general internist specialty) in Mysore District, spending more than 20 hours a week in direct patient care, and they should have more than 20% female patients between 9 and 15 years of age. On being identified as potential participants, physicians were sent a letter requesting an interview. After the letter, they were telephoned to ascertain their interest and after the informed consent process, an interview was scheduled for a convenient time and location. Before conducting the interview, they were provided with general information about the interview topic, told that the interview would be recorded, provided with an assurance that their responses would remain confidential, and asked to sign a formal consent form. The interviews were conducted in English and lasted between 45–60 minutes. All interviews were recorded and transcribed verbatim. Respondents received no remuneration for participation. The protocol for this study was approved by the Ethics Committee at PATH, USA and the Institutional Ethics Review Board at C.S.I. Holdsworth Memorial Hospital in Mysore, India. Interview guide development A screener instrument and an interview guide were developed for the study. The guide was based on a review of the relevant literature on physician attitudes toward HPV vaccination. It explored physician knowledge about HPV, cervical cancer, and HPV vaccination; attitudes toward recommending an HPV vaccine; perceptions about the
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attitudes of the management and colleagues towards recommending immunization against HPV; and barriers and facilitators to HPV vaccine recommendation and uptake of the vaccine among parents of adolescent girls. Before use, the guide was pretested in four mock interviews with physicians at C.S.I. Holdsworth Memorial Hospital, and revisions were made to ensure that there was sufficient time to cover all topics. Data analysis The study used an iterative analytic process where the investigator reviewed sets of three to four transcripts independently to identify key themes. Emergent themes were used to develop a preliminary framework. Subsequent sets of interviews were similarly assessed with the goal of further clarifying core themes. Once a final set of themes was selected, all transcripts were reanalyzed using the final framework. Quotations were selected based on whether they were illustrative of either widely held or deviant views. Because of the small number of interviews, analysis was conducted manually without the assistance of qualitative data analysis software for coding and text retrieval. Results Sample description The mean age of the participants was 31 years (range 28– 43 yrs). Eight (40%) were male, and 12 (60%) were female. Six participants (30%) specialized in obstetrics/gynecology, nine (45%) in pediatrics, and five (25%) in either family or general practices. Eight of the physicians (40%) owned their private practice, three (15%) worked in government hospitals, and the remainder (nine, 45%) worked in private hospitals. The vast majority (15, 75%) practiced in urban settings whereas the remainder (five, 25%) worked in periurban or rural locations in Mysore District. Physician attitudes about recommending HPV vaccination Most physicians interviewed (18, 90%) stated that physicians should recommend HPV vaccination to their patients. In most cases this view seemed to be related to positive views about vaccination in general as opposed to the HPV vaccine in particular. More than half of the participants (13, 65%) admitted to having little or no information about the HPV vaccine, although all said they had heard about the relationship between HPV infection and cervical cancer before being invited to the study. A pediatrician expressed this commonly held view in the following way: ‘‘I will recommend the [HPV] vaccine because cancer [of the] cervix is one thing the whole of Indian women are scared of. Prevention is always better than a cure.[but] most doctors don’t know [enough about] this vaccine. If they knew more they would push it through.’’
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The two physicians who felt that recommending HPV vaccination was not appropriate at the present time also cited lack of knowledge as the main reason for their reservation. A pediatrician who had more than 20 years of experience in vaccination programs expressed his reasons in the following way: ‘‘I don’t recommend unless there is full knowledge of side effects and safety.If there is any accident or some intolerable side effect the public opinion can be very bad. We had some incidents with measles vaccinations; there was a furor about it [across] the whole country. Once it gets into news media, it has a negative effect on our other immunizations so I won’t recommend it unless I’m sure it’s safe.’’
Despite the fact that most participants expressed broadly positive views about HPV vaccination, many had mixed feelings about whether recommending the vaccine would help to encourage uptake among their patients The high cost of the HPV vaccine, at rupees 8400 (USD $186) for three doses, was the most commonly mentioned obstacle to vaccine uptake. The majority of physicians (16, 80%) expressed concern that most patients would be unable to afford the vaccine unless it became part of India’s Universal Immunization Program schedule. A pediatrician working in a private hospital summarized it this way: ‘‘People have money, but they don’t want to spend. A vaccine like this has to be pocket-friendly otherwise people won’t take it. I treated a child with Pneumonia. He almost died but his family was still hesitating to immunize [their] other children with Pneumococcal vaccine. They said they will think about it and then left. They are optional vaccines. so people resist. I asked them ‘Is your child optional?’ but they don’t listen. This will be the biggest problem with the HPV vaccine. Unless it is part of the immunization schedule most people won’t take it even if I tell them they should.’’
According to physicians, the second most common reason for parents not electing their daughters for vaccination despite recommendation was that the vaccine offered protection against a sexually transmitted infection. Parents did not want to acknowledge that their daughters would become sexually active, and therefore believed that they were unlikely to be exposed to the HPV infection. An obstetrician/gynecologist working in private practice expressed this concern in the following way: ‘‘These things are very personal, particularly in our country. People don’t want to talk to their children about sex. It becomes very difficult so I think most of my patients will not respond well..Maybe when we are talking about menstrual hygiene we can be indirectly talking about some subjects. Talking about sexually transmitted infections is hard since most people won’t think their daughter could be sexually active. This is a problem for this vaccine.Most parents will not consider it and I think it would be hard in a private practice to try to make people understand why they should take it.’’
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Subjective norms impacting physician intention to recommend HPV vaccination Although many expressed positive attitudes toward vaccines in general and the HPV vaccine in particular, most were quick to point out that recommending vaccination was not appropriate in their work setting. An obstetrician/gynecologist practicing in a government hospital expressed it in the following way: ‘‘Our work is mainly dealing with pregnancy and reproductive problems such as white discharge and other things like menstrual problems. Our patients are not expecting us to talk about immunization. That is Pediatrics. They would not come to us for that.’’
Other specialties, including pediatrics, family practice, and general practice seemed to feel that promotion of immunization was an appropriate and important role in their specialty. A pediatrician in a government hospital summarized how he felt about promoting vaccination: ‘‘We are taught this way. Immunization is better than disease. I start to educate my patients from newborn about diseases that can be prevented. I explain to them what is likely to come and what is preventable. I have 25 years of practice in pediatrics so I am strong about prevention. I will not care for a patient without making sure about their status even with optional vaccines like Hepatitis B and pneumococcal vaccines.’’
Seven of the nine (78%) pediatricians interviewed in the study indicated that they looked to the Indian Academy of Pediatrics (IAP) for guidance on vaccines and immunization. Several of the participants indicated that they would not promote any vaccine, which had not been recommended by the IAP Committee on Immunization. A pediatrician working in a large private hospital described his reasons for relying on the IAP in this way: ‘‘As Pediatricians we need to keep in touch with journals, with the latest developments, and newer vaccines in the pipeline. I take the words of the Indian Academy of Pediatrics because they conduct updates on immunizations and give us information on new vaccines and safety. In last 10 years, I recommended the hemophilus influenzae conjugate vaccine and pneumococcal vaccine because of IAP recommendations.’’
Interestingly, there were no other professional associations mentioned by physicians. Several (two, 10%) said they relied on information from continuing education meetings at their hospital or clinic, one physician (5%) said that he looked to the World Health Organization for vaccine information, and 14 of the 20 physicians (70%) indicated they relied on journals in their field. Perceived behavioral control and physician intention to recommend HPV vaccination The most common perceived difficulty mentioned by physicians was the lack of time to counsel patients because
of the high caseloads. Physicians in a government hospital setting typically see more that 40 patients during a workday—and this equates to less than 10 minutes per consultation. In such a situation, many of the physicians felt that it would be difficult to recommend an optional vaccination like the HPV vaccine in this limited period. A pediatrician working in a government hospital explained it this way: ‘‘We have morning OPD. maybe 25 or 30 patients. It is difficult to talk in-depth. We try to make sure of the main vaccinations. People know from the government schedule so it is not so hard. An optional vaccine.this is harder. If they have read and come to us to ask it is ok because they are already aware, then it is different. If they are not, it is hard to answer [questions] in a short time.’’
As mentioned earlier, another perceived difficulty mentioned by physicians was talking with parents about a vaccine for a sexually transmitted infection for their adolescent daughters. In general, the pediatricians were the least concerned about their patients’ reactions to this topic, whereas obstetricians and gynecologists expressed the most concern. Physicians based in private practices saw this as more of a concern than those working in either private or government hospitals. One obstetrician/gynecologist practicing in a private hospital expressed it this way: ‘‘This is very controversial. In our country there is trouble about whether sex education as such should be introduced to the adolescents in the school curriculum or not. This debate is going on and the government is against it. Many of these subjects are taboo, so it is hard for a doctor to talk about a vaccine that concerns sex especially if it’s about an adolescent girl of 9 or 10 years. It might be ok if it was just a cancer vaccine but not otherwise.’’
Finally, three of the physicians who worked in government hospitals said that they would be unable to recommend vaccines that were not currently part of the government universal vaccine schedule. A pediatrician at a major government hospital explained it this way: ‘‘It is a government setup. We must offer the vaccines that the government has decided. Also, most of our patients are from lower socioeconomic groups. They will take the compulsory vaccines but they don’t have money for other things.’’
Discussion This study examined knowledge and attitudes about HPV vaccination among healthcare providers from a mix of specialties and practice settings in Mysore, India. The study found that although most physicians expressed positive attitudes toward vaccination in general, and HPV vaccination in particular, an overwhelming majority believed that few of their patients would react positively to a vaccine recommendation. Many physicians providing services to adolescent girls aged 9 to 15 years, particularly those practicing
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obstetrics/gynecology, suggested that recommending immunization was not appropriate in their work setting—a belief that would likely constrain the promotion of the vaccine among adolescent girls. Additionally, it seemed that workplace constraints, particularly patient load was perceived by many physicians as a key obstacle in promoting the vaccine. In this case, many physicians seemed to think it would be very difficult to promote an optional vaccine, particularly one that could be considered controversial, to their patients. In general, Indian physicians had strikingly similar attitudes to their counterparts from other parts of the world. Like studies from the United States, many expressed concerns that parents would be worried that HPV vaccination may encourage risky sexual behaviors among their daughters [10]. As with others studies from both the developed and the developing world, they also perceived the same barriers to vaccine uptake including cost [10,21], reservations about recommending vaccination for girls 9 to 13 years as the age [10], and reluctance to discuss sexual issues with adolescent patients or their parents [12–14]. Also, as with studies from the United States, Canada, and Mexico, physician knowledge of cervical cancer, HPV, and HPV vaccination varied widely by training and specialty [9,10,19]. Because of the small sample and the qualitative nature of the study, the findings may not be representative of the views of all physicians in India. Additionally, we cannot rule out the possibility that additional important themes might have emerged if further interviews had been conducted. Furthermore physicians were asked to discuss their intention-torecommend an HPV vaccine, and this may not reflect their actual recommendations. Despite these limitations, these formative findings contribute to a conceptual framework to better understand the issues related to HPV vaccine acceptability in India. This study has focused on factors related to intention-torecommend HPV vaccination among healthcare providers in India, and the findings will be useful for planners working to increase uptake of this new vaccine against HPV. There seems to be a very low level of knowledge among providers about the vaccine, and the first challenge for policymakers is therefore to address this ‘knowledge gap’ if efforts to introduce the vaccine are to be successful. Second, while specialties like obstetrics/gynecology currently provide services to adolescent girls in the target age range, workplace norms seem to suggest that promotion of the HPV vaccine may not receive much support in this setting. Policymakers should consider working closely with obstetric and gynecology associations to change work norms and educate members about the value of primary as well as secondary prevention of cervical cancer. In addition, efforts to increase vaccine uptake should focus on specialties already familiar with the administration of childhood vaccines, particularly pediatricians and family practitioners. Finally, many physicians in India look at their professional organizations for information about vaccination, so communication strategies should target professional organizations and journals to provide
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information about the safety and efficacy of vaccines and giving general recommendations for HPV immunization. While this study points up some of the unique challenges of promoting the HPV vaccine among physicians in India, it also illustrates striking similarities in attitudes to their counterparts from other areas of the world. Given these parallels, it seems reasonable to suggest that policymakers should consider carefully the lessons learned about HPV immunization from both developed and developing countries as they consider how to best optimize uptake in India. Such an approach would help speed the day when cervical cancer will not be one of the major killers of women in India.
Acknowledgments The authors thank Thomas Butler, Yashodha MN, and Varalakshmi Chandrasekaran for assisting on the project and all the physicians who took the time to participate in the study. Special thanks to staff at Public Health Research Institute and CSI Holdsworth Memorial Hospital for helping carry out the research. Support for this project was provided by PATH, USA. The views expressed by the authors do not necessarily reflect the views of PATH.
References [1] Baseman JG, Koutsky LA. The epidemiology of human papillomavirus infections. J Clin Virol 2005;32(Suppl 1):S16–24. [2] Koutsky L. Epidemiology of genital human papillomavirus infection. Am J Med 1997;102(5A):3–8. [3] Braaten KP, Laufer MR. Human papillomavirus (HPV), HPVrelated disease, and the HPV vaccine. Rev Obstet Gynecol 2008; 1(1):2–10. [4] Zhang WY, Xue YZ, Chen M, et al. Prevalence of high-risk human papillomavirus infection in different cervical lesion among organized health-examination women in Shanghai, China. Chin Med J (Engl) 2008;121:1578–82. [5] Molano M, Posso H, Weiderpass E, et al. Prevalence and determinants of HPV infection among Colombian women with normal cytology. Br J Cancer 2002;87:324–33. [6] Stanley M. Prevention strategies against the human papillomavirus: the effectiveness of vaccination. Gynecol Oncol 2007;107(2 Suppl. 1): S19–23. [7] Tiro JA, Meissner HI, Kobrin S, Chollette V. What do women in the U.S. know about human papillomavirus and cervical cancer? Cancer Epidemiol Biomarkers Prev 2007;16(2):288–94. [8] Zimet GD, Mays RM, Winston Y, et al. Acceptability of human papillomavirus immunization. J Womens Health Gend Based Med 2000;9: 47–50. [9] Duval B, Gilca V, McNeil S, et al. Vaccination against human papillomavirus: A baseline survey of Canadian clinicians’ knowledge, attitudes and beliefs. Vaccine 2007;25:7841–7. [10] Daley MF, Liddon N, Crane LA, et al. A national survey of pediatrician knowledge and attitudes regarding human papillomavirus vaccination. Pediatrics 2006;118:2280–9. [11] Jain N, Irwin KL, Montano D, et al. Family physicians’ knowledge of genital human papillomavirus (HPV) infection and HPV-related conditions, United States, 2004. Fam Med 2006;38:483–9.
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K. Krupp et al. / Journal of Adolescent Health 46 (2010) 379–384
[12] Esposito S, Bosis S, Pelucchi C, et al. Pediatrician knowledge and attitudes regarding human papillomavirus disease and its prevention. Vaccine 2007;25:6437–46. [13] Riedesel JM, Rosenthal SL, Zimet GD, et al. Attitudes about human papillomavirus vaccine among family physicians. J Pediatr Adolesc Gynecol 2005;18:391–8. [14] Kahn JA, Zimet GD, Bernstein DI, et al. Pediatricians’ intention to administer human papillomavirus vaccine: the role of practice characteristics, knowledge, and attitudes. J Adolesc Health 2005;37:502–10. [15] Raley JC, Followwill KA, Zimet GD, Ault KA. Gynecologists’ attitudes regarding human papilloma virus vaccination: A survey of Fellows of the American College of Obstetricians and Gynecologists. Infect Dis Obstet Gynecol 2004;12:127–33. [16] Kahn JA, Rosenthal SL, Tissot AM, et al. Factors influencing pediatricians’ intention to recommend human papillomavirus vaccines. Ambul Pediatr 2007;7:367–73.
[17] Jaspan DM, Dunton CJ, Cook TL. Acceptance of human papillomavirus vaccine by gynecologists in an urban setting. J Low Genit Tract Dis 2008;12:118–21. [18] Tissot AM, Zimet GD, Rosenthal SL, et al. Effective strategies for HPV vaccine delivery: The views of pediatricians. J Adolesc Health 2007;41: 119–25. [19] Aldrich T, Becker D, Garcı´a SG, Lara D. Mexican physicians’ knowledge and attitudes about the human papillomavirus and cervical cancer: A national survey. Sex Transm Infect 2005;81: 135–41. [20] de Carvalho NS, Teixeira LM, Pradel EM, et al. Vaccinating against HPV: physicians’ and medical students’ point of view. Vaccine 2009;27:2637–40. [21] Wong LP. Physicians’ experiences with HPV vaccine delivery: Evidence from developing country with multiethnic populations. Vaccine 2009;27:1622–7.