Human Vaccines & Immunotherapeutics

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Sustaining motivation to immunize Kalpana Manthiram, Kathryn Edwards & Areej Hassan To cite this article: Kalpana Manthiram, Kathryn Edwards & Areej Hassan (2014) Sustaining motivation to immunize, Human Vaccines & Immunotherapeutics, 10:10, 2930-2934, DOI: 10.4161/hv.29871 To link to this article:

Accepted author version posted online: 01 Nov 2014.

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Date: 05 November 2015, At: 14:53

COMMENTARY Human Vaccines & Immunotherapeutics 10:10, 2930--2934; October 2014; © 2014 Taylor & Francis Group, LLC

Sustaining motivation to immunize Exchanging lessons between India and the United States Kalpana Manthiram1,*, Kathryn Edwards1,y, and Areej Hassan2,y 1

Vanderbilt Vaccine Research Program; Division of Pediatric Infectious Diseases; Vanderbilt University Medical Center; Nashville, TN US; 2Division of Adolescent

Medicine; Boston Children’s Hospital; Harvard Medical School; Boston, MA US y

Both authors contributed equally as senior authors on this commentary


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n our recent study on vaccine uptake and parental attitudes toward immunizations in urban South India, we found strong support for vaccination due to fear of vaccine-preventable diseases and confidence in the recommendations made by health care professionals. In this commentary, we will characterize the reasons behind strong parental motivation to immunize in South India and consider ways these motivators can be enhanced in the United States, where vaccine hesitancy has led to outbreaks of vaccine-preventable disease. In addition, we will also discuss lessons that can be learned from the hesitancy movements in the United States and applied in India to maintain strong support for vaccination.


Keywords: immunization delivery, parental attitudes, polio eradication, vaccine hesitancy, vaccine uptake *Correspondence to: Kalpana Manthiram; Email: [email protected] Submitted: 06/25/2014 Accepted: 07/09/2014 2930

In 1974, the World Health Organization (WHO) launched the Expanded Programme on Immunization (EPI) to increase immunization rates of young children following the success of the smallpox vaccination campaign. The EPI initially recommended inclusion of immunizations against six vaccine-preventable diseases (tuberculosis, poliomyelitis, diphtheria, tetanus, pertussis, and measles) in national immunization schedules. Since then, additional vaccines such as pneumococcal conjugate vaccine, Hemophilus influenzae type b vaccine, and rotavirus vaccine have been incorporated into the schedules of an increasing number of countries. Enhancing uptake of these newer vaccines has been a priority for WHO, UNICEF, and Human Vaccines & Immunotherapeutics

the GAVI Alliance as these vaccines dramatically reduce mortality.1 However, with the expansion of immunization schedules has come “vaccine hesitancy.” The WHO’s Strategic Advisory Group of Experts defined vaccine hesitancy as “a behavior influenced by a number of issues of confidence (do not trust vaccine or provider), complacency (do not perceive need for vaccine, do not value vaccine), and convenience (access).”2 Hesitancy movements have been reported in diverse populations including Nigeria, the Philippines, the United Kingdom, and the United States among others, and have lead to serious lapses in immunization uptake and outbreaks of infectious diseases.3-5 In order to strengthen the resilience of parents to withstand unfounded concerns about vaccines, motivators for vaccine acceptance must be understood and supported. We sought to evaluate these motivators by qualitatively assessing parental knowledge about and attitudes toward vaccination in an urban South Indian community.6 In our study, we interviewed 21 parents of children aged 18 to 36 months old in the Pallavapuram municipality, which is a suburb of Chennai, the largest city in the southern state of Tamil Nadu. Uptake of routine immunizations was high in Pallavapuram. However, not surprisingly, uptake of optional vaccines (which are vaccines not included in the routine vaccine schedule but available for purchase in the private sector) was considerably lower due to high cost and lack of awareness of availability. Despite these barriers, we found high public confidence Volume 10 Issue 10

in vaccination and a desire from parents to obtain the additional available vaccines for their children. The primary motivators for immunization uptake were (1) fear of vaccine-preventable diseases and (2) trust in health care professionals and the vaccination system. No parents showed “hesitancy” in accepting vaccines for their children. What can we learn from this community to help us address vaccine hesitancy and maintain public confidence in vaccines in the United States, India and other locales?

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Motivators of Vaccination Fear of disease Generalized fear of vaccine-preventable diseases was a major driver of pro-vaccination behavior in our study. However, although parents easily articulated the general purpose of vaccines, few had detailed knowledge about or reported direct experience with vaccine-preventable diseases with the exception of poliomyelitis. Anxiety about polio permeated throughout participant responses and many parents held the feared consequences of polio as motivating factors for obtaining not only polio vaccine but all immunizations. “ When people don’ t get immunizations, they get handicaps or problems in their arms and legs. We get immunizations to keep that from happening.” Less than a quarter of parents directly or indirectly knew a specific person who had polio, but most parents knew that polio could lead to disability. (In comparison, only a few were able to describe the symptoms associated with chicken pox, influenza, or measles.) Nearly all parents expressed significant fear that their children would become disabled if they did not receive the polio vaccine and felt that polio was a very severe disease. “ If the child has a handicap in their body, their life is lost. So we have to be careful and get immunizations. If we are not careful, the child’ s life, that’ s it, it’ s gone.” These quotes underscore the effect India’s polio eradication campaign has had in shaping parental perceptions about all vaccines, not just polio. The polio eradication campaign has utilized mass media

promotions through television and radio. Other integral components of this effort include national polio vaccination days during which thousands of vaccinators immunized millions of children, close surveillance of communities with polio cases, and grassroots engagement of vaccine hesitant families and communities with community mobilisers.7-9 This massive effort heightened public awareness about the consequences of poliomyelitis. In our study, parents reported hearing about the value of polio vaccine from multiple sources including medical professionals, anganwadi or lay health workers, friends and family, public health messages on television and radio, and community leaders, highlighting the value of comprehensive communication campaigns in stimulating vaccine demand. Socio-economic status and education have been observed to influence vaccine uptake in many countries.10 Although we saw significant differences in routine and optional vaccine uptake based on socioeconomic status, we did not see differences in vaccine confidence based on income, parental education, or location of vaccination (private vs. public clinic). Low income and low parental education may hinder vaccine access and awareness of the child’s vaccine status but did not hamper vaccine acceptance in Pallavapuram. This finding indicates the effectiveness of provaccination messages in reaching diverse audiences.

Confidence in health care providers The second major motivator of vaccine demand was trust in physicians, other health care providers, and the health systems that deliver vaccines. Reliable and accessible immunization services foster trust.11,12 However, the faith that parents have in their medical providers has an even more powerful effect on vaccine behavior. Several studies have shown that a medical professional’s recommendation to vaccinate is positively correlated with vaccination.13–16 In our study, parents voiced high confidence in their doctor’s recommendations. One parent said: “ Doctor’ s advice; it’ s the best advice. They tell us to get immunizations and we do.”

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In addition to physicians, many parents were encouraged to obtain immunizations by nurses and other medical providers who lived in their neighborhoods as well as family and friends. Positive reinforcement of the value and safety of immunizations from these community members made immunization a “social norm.”

Interpretation of Adverse Events after Immunization In 2011, a 2-y-old boy died two hours after receiving OPV near Pallavapuram.17,18 The child’s death was later reported to be unrelated to OPV, but nearly all parents mentioned this event, and several were apprehensive about immunizing their child following it. However, all parents ultimately decided to continue to vaccinate their children after their trusted providers told them the vaccine was not related to the death and provided counsel that the benefit of vaccination outweighed the risk of adverse events. Several parents suspected the affected child had another medical condition that put him at risk for an adverse event while others blamed the “disreputable” hospital for administering the vaccine incorrectly. All in all, most parents felt that the benefits of vaccination outweighed the risks for their child, even in the face of this serious adverse event temporally associated with vaccine administration. “ In the newspaper, I read that a child got. . .polio drops . . . a one or two year old child, and died. In January, when they were giving polio drops, I didn’ t get them right away. I got scared. So, I didn’ t get the drops. They give them for three days in a row; I didn’ t go the first day but I went the second day. The nurse told me, it’ s nothing and told me to get the drops for my child.” In the face of a challenge that could have easily diminished parents’ trust in vaccination, communication with medical providers and fear about poliomyelitis instilled by the polio vaccine campaign prevented vaccine hesitancy. When asked about post-vaccination fever, pain, and swelling, nearly all parents reported that their children experienced these symptoms. However, most parents


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considered these symptoms to be minor (particularly in comparison to the severity of the diseases they prevent), temporary, or expected consequences of immunization. In fact, nearly a quarter of parents stated that they considered fever to be a sign of vaccine efficacy. “ Every child definitely gets a fever. Only if the fever comes is there an effect.” Several parents reported that their physicians warned them of these side effects prior to immunization and assured them that the child would not have longterm consequences. In other countries (both low and high-income), such minor adverse effects are reported to influence parental decisions to immunize.19,20 However, in our Indian study population, these events did not faze parents who were more fearful of the consequences of vaccine-preventable diseases and confident of their provider’s guidance.

Applying these Motivators to the United States In his 1995 article, Nichter classifies demand for immunization as “active” or “passive.”12 Parents and communities exhibiting “active demand” seek immunizations because they believe they have great benefit. In contrast, those with “passive acceptance” obtain immunizations because they are compulsory. In the Indian community that we interviewed, we found many signs of active demand for vaccination. We believe active demand is less vulnerable to events or ideas that lead to vaccine refusal and must be supported in communities. In the United States, we have seen a surge in vaccine hesitancy.21 Compared with parents of vaccinated children, those of unvaccinated children are less likely to perceive vaccine-preventable diseases to be severe or believe that their own children are susceptible to these diseases.13 Parents of unvaccinated American children also reported less trust in the government, the vaccine industry, and vaccine researchers.13 Because of this distrust, some parents continue to voice concerns about vaccine safety even after these concerns have been scientifically refuted in large studies.22 In Pallavapuram, we saw that


strong messages about the severity of vaccine-preventable diseases from health professionals and public health campaigns were ingrained in parents’ minds, particularly about polio, even in those not personally familiar with the diseases. We believe some of the principles learned in our studies in India can be applied in the United States. Public health campaigns similar to India’s polio vaccine campaign invoking trusted individuals (including individuals not in health care like parents and celebrities) should be utilized to heighten awareness about vaccinepreventable disease, particularly in the setting of recent surges in measles and pertussis cases. These messages should be directed to a wide audience including parents, grandparents, physicians, nurses, medical assistants, school officials, and journalists, who all play a role in shaping a parent’s perceptions about vaccine-preventable diseases. In addition to widereaching health messages, grassroots efforts with local leaders and parents in areas with high hesitancy similar to what was done in India with community mobilisers would likely be highly effective. However, in concert with these awareness campaigns, efforts to foster trust in vaccine safety, research, and public health systems must be implemented as well. Cooper et al., recommended enhancing public trust in vaccine safety by educating the public on vaccine safety systems, engaging community members in decision-making about vaccines, and investing in immunization safety studies.22 Similar to India, parents in the US (including many parents of unvaccinated children) report confidence in their own health care providers.21 Therefore, preparing individual health care providers to educate parents and confidently combat misconceptions is a cornerstone to increasing trust in vaccine systems.21,23

Maintaining Active Demand in India Just as motivators can be extrapolated to other countries, India and other middle- and low-income countries can learn from hesitancy movements in the United States. In post-polio eradication India,

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polio awareness and fear may be less forceful drivers of immunization uptake. In addition, introduction of new vaccines may cause discomfort to both providers and parents due to unfamiliarity and concerns about safety.20 Here, we outline three strategies to maintain active demand for immunization. First, we recommend that government and public health officials identify and address unmet information needs proactively. As noted above, we saw that many parents had minimal understanding of vaccine-preventable illnesses aside from polio. Interestingly, many parents had an exaggerated view of the protection vaccines afforded. When asked to name vaccine-preventable diseases, over half of parents mentioned non-vaccine preventable disease like malaria, elephantiasis, and cholera or broad, non-specific conditions like fever, seizures, jaundice and rash. Although this may be bolstering immunization uptake in the short term, parents may become confused about the purpose of new vaccines or have unreasonable expectations of vaccine efficacy in the long-run.12 In addition, in Pallavapuram, many parents believed that immunizations should be delayed when a child has a mild upper respiratory illness; over half of parents reported that their child’s immunizations were delayed due to this, which represent missed immunization opportunities. Many parents in our study stated that they desired more detailed information about newly introduced vaccines from their providers. Despite high confidence in vaccines across socioeconomic groups in our study, some parents expressed concerns about the quality of vaccines, abilities of the vaccinator, cleanliness at government health centers, and vaccine safety especially after hearing about the child who died after receiving the polio vaccine. These parents tended to be from higher socioeconomic groups. These concerns mirror some of the safety concerns expressed by American parents of unvaccinated children, who are also largely of higher socioeconomic status and education level.21 Identifying these parents and addressing their concerns before they lead to passivity or hesitancy is important. Second, we recommend that vaccine education be provided not only to parents, but also to local public health officials, physicians (at both private and

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government hospitals), nurses, anganwadi workers, and local political leaders to create a cocoon of motivation. During vaccine safety scares and when new vaccines are introduced, these professionals are at the frontline of addressing parent concerns. In the US, health care workers with doubts about vaccination were more likely to have patients who refuse vaccination suggesting that providers may validate parental fears of vaccines by not forcefully combating concerns.24,25 For example, because few providers were equipped to make strong endorsements of human papilloma virus vaccine when it was first introduced in the US, uptake of the vaccine suffered.26 In a large country like India, provider education is not an easy feat, but the existing infrastructure for polio eradication campaigns can be leveraged to accomplish this. Since 46% of the children we studied received most of their immunizations from the private sector, it is important to educate private practitioners as well. The Indian Academy of Pediatrics, medical schools, non-governmental organizations, and media are resources to reach these physicians. Lastly, we recommend that health departments keep their fingers on the pulse of vaccine attitudes in their communities. Larson et al. urge health ministries to develop “surveillance systems” for vaccine hesitancy much the same way they monitor for infectious diseases.27 Preemptive action is often more effective than trying to change long-held beliefs. Focus groups and interviews with parents and vaccinators can be employed. In a closely connected world, concerns in one part of the globe can quickly travel to others. In addition, in a diverse country such as India, regional differences in attitudes exist. For example, during the polio eradication campaign, high levels of hesitancy were found among parents in the northern state of Uttar Pradesh, who were concerned that OPV could lead to sterilization.9,28 On the other hand, we did not find these concerns in the south Indian population we studied. Cognizance of regional differences helps to create a nuanced approach to vaccine hesitancy and helps to engage local leaders and health professionals who have significant impacts on particular constituents.

Conclusions Despite cultural and economic differences between the US and India, similarities in parents’ decision-making processes to vaccinate exist. Lessons from the success of India’s polio eradication campaign in fostering pro-vaccine attitudes in parents and health care providers can be applied to the United States. Likewise, India must be prepared to handle vaccine hesitancy particularly as additional vaccines are introduced into the routine vaccination schedule. We recommend that public health officials launch communication campaigns to educate parents and providers about the consequences of vaccine-preventable diseases, teach providers effective communication techniques to engage vaccine-hesitant parents, and closely monitor public opinion for changes in vaccine demand. An ounce of prevention is worth a pound of cure. Disclosure of Potential Conflicts of Interest

No potential conflicts of interest were disclosed. Acknowledgments

We are grateful to Dr. Yolanda Martins for her assistance in designing the qualitative methods, Dr. Athi Narayan for initiating this study, Vasanthan Kuppuswamy and the staff at Pallavaram Children’s Medical Centre for their assistance in data collection, and YRG-CARE IRB in Chennai and Children’s Hospital Boston IRB for their review of this study. References 1. Lee LA, Franzel L, Atwell J, Datta SD, Friberg IK, Goldie SJ, Reef SE, Schwalbe N, Simons E, Strebel PM, et al. The estimated mortality impact of vaccinations forecast to be administered during 2011-2020 in 73 countries supported by the GAVI Alliance. Vaccine 2013; 31(Suppl 2):B61-72; PMID:23598494; http:// 2. SAGE Vaccine Hesitancy Working Group, World Health Organization. What influences vaccine acceptance: A model of determinants of vaccine hesitancy. 2013. http:// 1_Model_analyze_ driversofvaccineConfidence_22_ March.pdf. Accessed 12 June 2014. 3. Gross L. A broken trust: lessons from the vaccine– autism wars. PLoS Biol 2009; 7:e1000114; PMID:19478850; pbio.1000114 4. Mitka M. Vaccine rumors, funding shortfall threaten to derail global polio eradication efforts. JAMA 2004; 291:1947-8; PMID:15113793; 10.1001/jama.291.16.1947

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5. Emmons K. It takes a community to eliminate tetanus. html#.U6tBWo1dXAd. Accessed on 25 May 2014. 6. Manthiram K, Blood EA, Kuppuswamy V, Martins Y, Narayan A, Burmeister K, Parvathy K, Hassan A. Predictors of optional immunization uptake in an urban south Indian population. Vaccine 2014; 32:3417-23; PMID:24736005; 2014.04.012 7. John TJ, Vashishtha VM. Eradicating poliomyelitis: India’s journey from hyperendemic to polio-free status. Indian J Med Res 2013; 137:881-94; PMID:23760372 8. Obregon R, Chitnis K, Morry C, Feek W, Bates J, Galway M, Ogden E. Achieving polio eradication: a review of health communication evidence and lessons learned in India and Pakistan. Bull World Health Organ 2009; 87:624-30; PMID:19705014; 10.2471/BLT.08.060863 9. United Nations Children’s Fund, Regional Office for South Asia. When Every Child Counts: Engaging Underserved Communities for Polio Eradication in Uttar Pradesh, India. Working Paper 2004. 10. Larson HJ, Jarrett C, Eckersberger E, Smith DM, Paterson P. Understanding vaccine hesitancy around vaccines and vaccination from a global perspective: a systematic review of published literature, 2007-2012. Vaccine 2014; 32:2150-9; PMID:24598724; http://dx. 11. World Health Organization Department of Mental Health and Substance Dependence. Behavioral Factors in Immunization, Geneva, 2000. health/media/en/28.pdf. Accessed 25 May 2014. 12. Nichter M. Vaccinations in the Third World: a consideration of community demand. Soc Sci Med 1995; 41:617-32; PMID:7502096; 10.1016/0277-9536(95)00034-5 13. Salmon DA, Moulton LH, Omer SB, DeHart MP, Stokley S, Halsey NA. Factors associated with refusal of childhood vaccines among parents of school-aged children: a case-control study. Arch Pediatr Adolesc Med 2005; 159:470-6; PMID:15867122; 10.1001/archpedi.159.5.470 14. Bovier PA, Chamot E, Bouvier Gallacchi M, Loutan L. Importance of patients’ perceptions and general practitioners’ recommendations in understanding missed opportunities for immunisations in Swiss adults. Vaccine 2001; 19:4760-7; PMID:11535327; http://dx. 15. Boyd CA, Gazmararian JA, Thompson WW. Knowledge, attitudes, and behaviors of low-income women considered high priority for receiving the novel influenza A (H1N1) vaccine. Matern Child Health J 2013; 17:852-61; PMID:22729697; 10.1007/s10995-012-1063-2 16. Cover JK, Nghi NQ, LaMontagne DS, Huyen DT, Hien NT, Nga T. Acceptance patterns and decisionmaking for human papillomavirus vaccination among parents in Vietnam: an in-depth qualitative study postvaccination. BMC Public Health 2012; 12:629; PMID:22877158; 17. Narayan PaP. Mahalingam. Panic in Chennai as child dies after polio vaccination. Times of India, January 24, 2011. 18. Manikandan K. Boy dies after polio vaccination. The Hindu, January 23, 2011. 19. Parrella A, Gold M, Marshall H, Braunack-Mayer A, Baghurst P. Parental perspectives of vaccine safety and experience of adverse events following immunisation. Vaccine 2013; 31:2067-74; PMID:23422146; http:// 20. Braka F, Asiimwe D, Soud F, Lewis RF, Makumbi I, Gust D. A qualitative analysis of vaccine safety perceptions and concerns among caretakers in Uganda. Matern Child Health J 2012; 16:1045-52; PMID:21660604;


24. Salmon DA, Moulton LH, Omer SB, Chace LM, Klassen A, Talebian P, Halsey NA. Knowledge, attitudes, and beliefs of school nurses and personnel and associations with nonmedical immunization exemptions. Pediatrics 2004; 113:e552-9; PMID:15173536; http://dx. 25. Salmon DA, Pan WK, Omer SB, Navar AM, Orenstein W, Marcuse EK, Taylor J, deHart MP, Stokley S, Carter T, et al. Vaccine knowledge and practices of primary care providers of exempt vs. vaccinated children. Hum Vaccin 2008; 4:286-91; PMID:18424918; 26. Ylitalo KR, Lee H, Mehta NK. Health care provider recommendation, human papillomavirus vaccination,

and race/ethnicity in the US National Immunization Survey. Am J Public Health 2013; 103:164-9; PMID:22698055; 2011.300600 27. Larson HJ, Cooper LZ, Eskola J, Katz SL, Ratzan S. Addressing the vaccine confidence gap. Lancet 2011; 378:526-35; PMID:21664679; 10.1016/S0140-6736(11)60678-8 28. Hussain RS, McGarvey ST, Shahab T, Fruzzetti LM. Fatigue and fear with shifting polio eradication strategies in India: a study of social resistance to vaccination. PLoS One 2012; 7:e46274; PMID:23050003; http://

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Human Vaccines & Immunotherapeutics

Volume 10 Issue 10

Sustaining motivation to immunize: exchanging lessons between India and the United States.

In our recent study on vaccine uptake and parental attitudes toward immunizations in urban South India, we found strong support for vaccination due to...
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