Abstracts

Introduction

Influenza is a viral respiratory disease that places a heavy burden on health systems, particularly in low- and middle-income countries ¹1. Demicheli V, Jefferson T, Ferroni E, Rivetti A, Di Pietrantonj C. Vaccines for preventing influenza in healthy adults. Cochrane Database Syst Rev 2018; (2):CD001269.^,22. World Health Organization. Global influenza strategy 2019-2030. https://apps.who.int/iris/bitstream/handle/10665/311184/9789241515320-eng.pdf?sequence=18&isAllowed=y (accessed on 20/Nov/2020).
https://apps.who.int/iris/bitstream/hand... . Vaccination is one of the most effective interventions to prevent diseases ³3. World Health Organization. Influenza (seasonal), 2018. https://www.who.int/news-room/fact-sheets/detail/influenza-(seasonal) (accessed on 10/Nov/2020).
https://www.who.int/news-room/fact-sheet... . Vaccines show an efficacy above 60% and a mortality reduction of up to 80% ⁴4. Dawood FS, Chung JR, Kim SS, Zimmerman RK, Nowalk MP, Jackson ML, et al. Interim estimates of 2019-20 seasonal influenza vaccine effectiveness - United States, February 2020. MMWR Morb Mortal Wkly Rep 2020; 69:177-82.. Yet, influenza still exerts a heavy toll on health, with three to five million severe cases of the disease and between 290,000 to 650,000 influenza-related deaths, mainly affecting the risk groups that have been prioritized for vaccination: pregnant women, infants, older adults, and adults with risk factors ³3. World Health Organization. Influenza (seasonal), 2018. https://www.who.int/news-room/fact-sheets/detail/influenza-(seasonal) (accessed on 10/Nov/2020).
https://www.who.int/news-room/fact-sheet... .

Latin American countries have made significant advances in introducing and scaling up seasonal influenza vaccines, giving increasing priority to immunization strategies as an integral part of the national immunization programs (NIP). Most South American countries have a seasonal influenza policy of freely providing vaccination to children aged under six years, people with chronic comorbidities, adults aged over 60 years, pregnant women within 20 weeks of gestation or puerperal women ⁵5. Gentile A, Paget J, Bellei N, Torres JP, Vasquez C, Laguna-Torres A, et al. Influenza in Latin America: a report from the Global Influenza Initiative (GII). Vaccine 2019; 37:2670-8.. However, coverage levels achieved vary from one country to another, ranging across older adults, pregnant women, and children aged under five years from 29% in Paraguay to 89% in Brazil. Among the countries in the Andean Region (Peru, Bolivia, Ecuador, Colombia, and Venezuela) and the South Cone (Argentina, Chile, Paraguay, and Uruguay), and Brazil, NIP covered, in 2018 (or the most recent year), 61.6% of adults aged 60 years and older, 58.4% of children aged under six years, 56.7% of pregnant women, and 76.7% of adults with chronic conditions ⁶6. Pan American Health Organization. Influenza vaccination coverage map: influenza vaccine coverage in countries and territories of the Americas, 2005-2017. http://ais.paho.org/imm/InfluenzaCoverageMap.asp (accessed on 06/Oct/2020).
http://ais.paho.org/imm/InfluenzaCoverag... . Vaccination coverage across all risk groups in Argentina, Bolivia, Brazil, Chile, Colombia, and Ecuador perform above the regional average, whereas Paraguay, Peru, Uruguay, and Venezuela perform below the average ⁶6. Pan American Health Organization. Influenza vaccination coverage map: influenza vaccine coverage in countries and territories of the Americas, 2005-2017. http://ais.paho.org/imm/InfluenzaCoverageMap.asp (accessed on 06/Oct/2020).
http://ais.paho.org/imm/InfluenzaCoverag... .

Supply- and demand-side factors influence influenza vaccine coverage ⁷7. Palache A, Oriol-Mathieu V, Fino M, Xydia-Charmanta M. Seasonal influenza vaccine dose distribution in 195 countries (2004-2013): little progress in estimated global vaccination coverage. Vaccine 2015; 33:5598-605.. On the demand side, vaccine hesitancy has been defined as the delay in accepting or rejecting vaccines despite their availability ⁸8. Cobos Muñoz D, Monzón Llamas L, Bosch-Capblanch X. Exposing concerns about vaccination in low- and middle-income countries: a systematic review. Int J Public Health 2015; 60:767-80.^,99. SAGE Working Group. Report of the SAGE working group on vaccine hesitancy. Thousand Oaks: SAGE Publications; 2014.. Vaccine hesitancy is the result of a complex interaction of behavioral and societal factors whose intervention requires leadership from vaccination programs. Among several models that have been proposed to analyze vaccine hesitance, the “3Cs” model considers the role played by confidence, complacency, and convenience ¹⁰10. MacDonald NE, Eskola J, Liang X, Chaudhuri M, Dube E, Gellin B, et al. Vaccine hesitancy: definition, scope and determinants. Vaccine 2015; 33:4161-4.. Confidence is the degree of trust in the effectiveness and safety of the vaccine, in its delivery system - including the reliability and competence of health services and professionals -, and in the motivations of the decision-makers to achieve effective access to vaccines ⁹9. SAGE Working Group. Report of the SAGE working group on vaccine hesitancy. Thousand Oaks: SAGE Publications; 2014.. Lack of confidence stems from strong negative attitudes towards vaccination, which can be influenced by misinformation about vaccination risks, affiliation to anti-vaccine groups or by legitimate concerns regarding vaccine safety and efficacy. Complacency refers to the degree to which people consider vaccination necessary to prevent a vaccine-preventable disease, as a result of the combination of risk perception, knowledge of the disease and the vaccine, prejudices regarding side effects and other reactions, and the need for vaccination. Vaccine convenience is defined by availability, affordability, willingness to pay, geographical accessibility, ability to understand and to accept vaccine-related information, the appeal of immunization services, and quality of care ¹⁰10. MacDonald NE, Eskola J, Liang X, Chaudhuri M, Dube E, Gellin B, et al. Vaccine hesitancy: definition, scope and determinants. Vaccine 2015; 33:4161-4.^,1111. Betsch C, Böhm R, Chapman GB. Using behavioral insights to increase vaccination policy effectiveness. Policy Insights Behav Brain Sci 2015; 2:61-73..

NIP can address vaccines hesitancy by increasing confidence on their effectiveness and safety; reduce complacency by clearly and convincingly communicating influenza risks and immunization benefits, and improve the perception of convenience derived from vaccine availability and accessibility. It can be hypothesized that the factor most directly addressed by NIP is convenience via their focus on vaccine supply, relegating strategies to bolster vaccine confidence and to tackle influenza complacency.

This study aims to explore, based on the perspective of officials interviewed in each country, the balance between facilitators and barriers to address vaccine confidence, complacency, and convenience in the chosen South American countries (Brazil, Chile, Paraguay, Peru, and Uruguay) which show contrasting influenza vaccination coverage.

Methods

A qualitative study was conducted based on national immunization program documentation and semi-structured interviews with program officials at the strategic planning and operational levels. Five South American countries were selected based on judgement of their vaccination rates. Our choice aimed to include countries with contrasting vaccination coverages. Brazil and Chile were selected as high performers and Paraguay, Peru, and Uruguay as low performers ⁶6. Pan American Health Organization. Influenza vaccination coverage map: influenza vaccine coverage in countries and territories of the Americas, 2005-2017. http://ais.paho.org/imm/InfluenzaCoverageMap.asp (accessed on 06/Oct/2020).
http://ais.paho.org/imm/InfluenzaCoverag... . Informant selection was based on convenience. Officials were identified based on their profiles of responsibility and participation in decision-making for the national (strategic level) management of NIPs, as well as those who participate in the programming and operational implementation processes, particularly with relation to influenza, in the states, regions or municipalities (operational level).

Informants were contacted by phone call or email and informed of the objectives of our investigation. Then, we requested appointments for face-to-face interviews. In total, 57 officials were contacted (27 at the strategic level and 30 at the operational level). Out of these, 38 agreed to be interviewed, 17 being at the strategic level and 21 at the operational level (Box 1). All interviews were conducted in Spanish (or Portuguese in the case of Brazil). A total of 61 documents were analyzed for the five countries, covering the guidelines of the national vaccination programs and their legal support, as well as national health plans, technical operational guidelines, manuals, bulletins from the epidemiology and statistics departments, and Pan American Health Organization (PAHO) country reports and evaluations.

Interview and documentary content analyses were carried out by researchers specializing in Public Health or Social Sciences and Health in each of the studied countries. Interview guides for each country were designed specifically for this investigation (Supplementary Material I: http://cadernos.ensp.fiocruz.br/static//arquivo/supl-e00045721-i_8686.pdf. Supplementary Material II: http://cadernos.ensp.fiocruz.br/static//arquivo/supl-e00045721-ii_3005.pdf). Interview and content analysis guides aimed to explore influenza program barriers and facilitators such as policy formulation, program planning, implementation, monitoring, and evaluation.

Each interview was carried out in the interviewee’s own work environment at a previously agreed time, lasting for 55 minutes on average. In all cases, before the interviews, permission was requested to record them and confidentiality consents were provided. Interview transcriptions and document content were coded in ATLAS.ti version 7 (http://atlasti.com/) via the directed content analysis technique ¹²12. Hsieh H-F, Shannon SE. Three approaches to qualitative content analysis. Qual Health Res 2005; 15:1277-88., based on predetermined codes, themes, and sub-themes that were developed from the literature, documents on the planning and operational implementation of health programs, and the 3Cs model. Also, during the coding process, pop-up codes were identified and linked to related themes and sub-themes via an iterative deductive/inductive approach. This process allowed us to identify program facilitators and barriers in relation to the 3Cs model of vaccine confidence, convenience, and influenza risk complacency at each country.

Our research protocol was approved in each country by their National Ethics Researches Committee as follows: Brazil (National Ethics Reserach Commision, 05215918.6.0000.5347); Chile (Ethics Research Committee on Beings, Faculty of Medicine, University of Chile, 191-2018); Paraguay (Ethics Research Committee, Central Public Health Laboratory, 106/2019); Peru (Prisma Ethics Research Committee, CE1651.18); and Uruguay (Ethics Research Committee, Uruguayan National Institute of Public Health, 1580).

Results

The national influenza vaccination programs of the five studied countries are similar regarding their coverage policies, targeted risk groups, and vaccination schedules (Table 1). Programs aim to cover, free of charge, all children aged under five years, pregnant women, adults older than 60 years, and persons living with chronic illnesses. Main program differences lie in age group definitions, inclusion of other risk groups, such as Indigenous peoples and institutionalized persons (except in Uruguay), and in the reported coverage of each risk group. Immunization coverage of people with chronic diseases is problematic as information is out of date or missing, whereas coverage rates, when reported, ranges from 99% to 97%. For other risk groups, high-coverage countries as Brazil and Chile report 81% to 95% and 65% to 90% coverage across risk groups, respectively. For low-coverage countries, figures range from 24% to 54% for Paraguay, 38% to 55% for Peru, and 24% to 57% for Uruguay. Health personnel is always the group best covered across countries, except for Brazil, in which older adults occupy that position.

Below, we show barriers and facilitators to vaccination coverage, contrasting program officers’ perceptions on supply- and demand-side components. Supply-side components include legal and financial bases; programming, purchase and distribution; personnel; access; collaboration arrangements; and monitoring, research, and evaluation. Demand-side components focus on vaccine promotion and communication; confidence on the vaccine; and complacency with influenza. Results for confidence and complacency are followed by testimonies for further detail.

Supply-side components

Legal and financial bases

Influenza vaccines are part of NIPs under the responsibility of national governments’ Ministries of Health ¹³13. Portal de Legislación. Ley que redefine el Calendario Nacional de Vacunación, el Calendario Nacional de Vacunación de Pueblos Indígenas y las Campañas Nacionales de Vacunación, en el ámbito del Programa Nacional de Inmunizaciones (PNI), en todo el territorio nacional. https://www.diariodasleis.com.br/legislacao/federal/234113-campanhas-nacionais-de-vacinauuo-redefine-o-calendurio-nacional-de-vacinauuo-o-calendurio-nacional-de-vacinauuo-dos-povos-indugenas-e-as-campanhas-nacionais-de-vacinauuo-no-um.html (accessed on 18/Oct/2020).
https://www.diariodasleis.com.br/legisla... ^,1414. Ministerio de Salud Pública. Código Sanitario de Chile. Decreto nº 725, de 1968. Diario Oficial 1968; 31 jan.^,1515. Ministerio de Salud Pública y Bienestar Social. Normas nacionales de vacunación, técnico administrativas y de vigilancia del Programa Nacional de Enfermedades Inmunoprevenibles y PAI. Asunción: Ministerio de Salud Pública y Bienestar Social; 2016.^,1616. Ministerio de Salud del Perú. NTS 141-MINSA/2018/DGIESP. Norma Técnica de Salud que establece el esquema nacional de vacunación. Diario Oficial El Peruano 2018; 19 dic.^,1717. Ministerio de Salud Pública. Ordenanza 289 Plan Integral de Atención en Salud, Decreto 465/008 de 3 de octubre de 2008. Aprobar el documento "CATALOGO DE PRESTACIONES (Anexo II del Decreto n.465/008, Decreto n. 289/009, Decretos y Leyes posteriores)". https://docplayer.es/79159600-Atento-el-ministro-de-salud-publica-resuelve.html (accessed on 26/Dec/2020).
https://docplayer.es/79159600-Atento-el-... . According to program officers, NIPs are politically, legally, and financially well supported, which guarantees their sustainability. In all countries, documentation supports the legal and financial bases of program norms and guidelines, except in Paraguay, in which the National Vaccine Law lacks written regulations. Officers in the country are proposing a regulation to introduce administrative sanctions to officers failing to reach vaccination goals. Regulations for the Uruguayan program have been recently reformulated to strengthen its implementation.

The Peruvian program is perceived as facing financing problems stemming from the failure to identify at-risk groups and, hence, to request the budget required to serve them. In Paraguay, financial resource limitations are perceived specifically in the lack of local financial resources to fund vaccination campaigns. On the other hand, Chile recently increased its budget toward these campaigns and introduced incentives to health personnel performance to reduce lost vaccination opportunities and increase coverage.

Programming, purchase, and distribution

NIP planning across countries is conducted by the Ministreis of Health via immunization departments or directorates charged with defining national objectives and goals. Determining targets for influenza vaccination coverage faces limitations in all countries, according to NIP officers’ perceptions. All countries have nominal registers available for children, pregnant women, and older adults, although program officers perceive the need to expand and strengthen them via improved coordination with authorities responsible for providing local information. Generally, NIPs report the lack of registers of persons living with chronic diseases and find the information on local disease prevalence unreliable. As noted in Box 2, there is a lack of recent information regarding the coverage of the influenza vaccine for this risk group. In Brazil, interviewees perceive the administrative autonomy of municipal governments as a problem due to the voluntary adhesion of municipalities in the use of the national health information system - with only 50% of the municipalities using it. In spite of the availability of registers in Uruguay (except for chronic diseases), its NIP estimates the total population to be vaccinated, whereas risk groups are quantified and targeted only via local operational strategies. In Paraguay, reliance on nominal registers is also limited, and programming is based on census information, itself out of date since the last census is from 2002. Generally, NIPs report purchasing arrangements of influenza vaccine as satisfactory, based on the consolidated purchasing of PAHO via its revolving fund mechanism, except for Chile, which successfully relies on direct competitive bidding. Distribution is carried out according to established deadlines, although a threat of delays was perceived due to cumbersome bureaucratic purchasing processes (Peru), barriers with vaccine importation (Uruguay), deficiencies with distribution coordination (Paraguay), and the need to cover a vast geographic area (Brazil).

Personnel

Peru, Chile, and Brazil have specific guidelines for training health personnel for their vaccination programs. Officials from all countries claimed that Ministries of Health formulated training guidelines which were implemented top-down all the way to health facilities, but in Paraguay and Uruguay, respondents reported unpublished training guidelines. Except for Uruguay and Paraguay, interviewees reported specific problems with personnel availability or with the competencies needed for executing the influenza vaccination program. Difficulties were reported in hiring or retaining operational and health personnel (Brazil); personnel shortages and the lack of skills specific to vaccinating migrant populations (Chile), and problems with campaigns in remote areas (Peru). Regarding the latter, remedial innovative training strategies were reported to be under implementation.

Access to services

Respondents in all studied countries reported that the population face barriers to accessing vaccination health services, except in Uruguay. Participants reported that service centers for the Brazilian, Paraguayan, and Peruvian programs are often remote, and, also for Brazil and Uruguay, they highlight inflexible opening hours during vaccination campaigns. Respondents indicated economic and educational barriers in Paraguay, whereas, for Peru, they found cultural barriers affecting Indigenous populations. The only strategy mentioned to improve access was expanding infrastructure in remote areas of Paraguay and Peru.

Collaboration arrangements

Coordination across public health institutions is reported as successful in all programs, as well as with the private sector. For the latter, written coordination mechanisms or signed agreements are reported for all countries. In Brazil, program officers found difficulties in coordinating with the education sector for child vaccination. In Uruguay, agreements enable government influenza vaccine distribution and free delivery by both public and private health providers. Brazil, Paraguay, and Uruguay have reinforced vaccination programs via collaboration agreements with civil society organizations. Brazilian program officers perceived that collaboration had diminished after program goals were increased.

Monitoring, research, and evaluation

Brazil, Chile, and Peru have published guidelines for evaluating influenza vaccination campaigns. In Brazil and Chile, state or provincial coordinators conduct permanent monitoring to update registers, compile goals by priority groups, and permanently evaluate local program performance. In Chile, vaccination campaign supervision is carried out during planning, and organization, execution, and coverage evaluation stages. Peruvian guidelines stipulate that the program must convene national, macro-regional, and regional program authorities to monitoring meetings, whereas health establishments are to locally monitor a set of indicators. In Peru and Paraguay, monitoring is restricted to the number of doses applied according to risk groups. Officers in Uruguay reported monitoring vaccination organization and vaccination center performance.

The evaluation of influenza vaccination programs is the responsibility of the Ministry of Health, with PAHO reporting on program coverage internationally ¹⁸18. Corrdenação Geral do Programa Nacional de Imunizações, Ministério da Saúde. 21ª campanha nacional de vacinação contra influenza: informe técnico. Brasília: Ministério da Saúde; 2019.^,1919. Romero MI, Osvaldo Quiroz MP. Informe final programa nacional de inmunizaciones (PNI). Santiago: Dirección de Presupuestos, División de Control de Gestión, Ministerio de Hacienda de Chile; 2012.^,2020. Ministerio de Salud Pública y Bienestar Social. Consolidado nacional por grupo de riesgo. Reportes vacunación. https://pai.mspbs.gov.py/influenza-2019/ (accessed on 12/Nov/2020).
https://pai.mspbs.gov.py/influenza-2019/... ^,2121. División Epidemiología, Dirección General de la Salud, Ministerio de Salud Pública. Gráficos automáticos sobre IRAG en el Uruguay. Información consolidada a nivel país, en línea y actualizada en tiempo real. http://colo1.msp.gub.uy/epidemiologia/servlet/iraggrafmenu (accessed on 20/Oct/2020).
http://colo1.msp.gub.uy/epidemiologia/se... ^,2222. Pan American Health Organization. Influenza and other respiratory virus surveillance systems in the Americas, 2017. Washington DC: Pan American Health Organization; 2017.. Chile reported external impact evaluations, such as the one carried out by the Ministry of Finance, whereas in Brazil, the NIP carries out impact evaluations. Only Uruguayan NIP officers mentioned research on vaccination hesitancy. The absence of studies assessing vaccine confidence were mentioned as a barrier in Peru, particularly among Indigenous groups living in urban areas or those still uncontacted.

Demand-side components

Vaccine promotion and communication

The situation of influenza vaccine confidence and convenience by risk groups is not specifically addressed in published program documentation across countries, although all programs, except the Paraguayan one, publish communication and promotional guidelines. The Chilean program is the only one among the five countries to specify promotional guidelines targeting the risk groups that prove most difficult to cover in the previous campaign, with the most recent guideline focusing on children, older adults, and pregnant women. In Brazil and Uruguay, program officers also report focusing on the risk groups least covered in previous years.

Program officers across all countries report the implementation of communication strategies to promote the national influenza vaccination season based on television, radio, posters, and social networks. In Brazil, officers saw a problem in the exclusive use of traditional media, instead of using new social media, such as Facebook, WhatsApp, and Instagram to reach a larger population. In Chile, informants indicated the need for adaptation to the new realities of social media, whereas in Paraguay, they found the need for more integrated promotional efforts across all vaccines. In Peru, informants perceived these strategies as partially effective, with good coordination across communication channels and increased coverage of the vaccine, but with the need to increase media coverage. In Uruguay, program officers reported the recent intensification of promotional efforts for the influenza vaccination campaign via mass media, as well as via videos screened in waiting rooms. However, officers pointed to the reduced effectiveness of promotional efforts due to the delays with vaccine supply mentioned above.

Uruguay was the only country which published a diagnosis of its national immunization program and of influenza vaccine confidence and complacency. A study conducted in 2016 found high levels of confidence by parents of immunized children as a whole ²³23. Zunino C, Speranza N, González V, Silva P, Varela A, Giachetto G, et al. Evaluación de la confianza y satisfacción del Programa Nacional de Vacunaciones en Montevideo, Uruguay, entre mayo y octubre de 2016. Arch Pediatr Urug 2019; 90:69-77.. However, a study in 2017 evidenced high complacency with influenza, with 24% to 26% of mothers of preschool children, pregnant women, and older adults considering this a serious or very serious disease. Among persons in the same risk groups who were not vaccinated, 18% to 21% stated either lacking trust in the vaccine or fearing adverse effects ²⁴24. Unidad de Inmunizaciones, División Epidemiología, Ministerio de Salud. Evaluación de la confianza y satisfacción del programa nacional de vacunaciones en Montevideo, 2016. Montevideo: Ministerio de Salud; 2016..

Vaccine confidence

In Uruguay, distrust in the vaccine is manifested in the exaggeration of its adverse effects, unlike other vaccines with greater acceptance:

“Nobody questions vaccines or their adverse effects or anything, but in the case of the flu...” (Interviewee at strategic level - Uruguay).

“People get vaccinated, catch a cold, and think first that it was because of the vaccine (...) and since they got a cold, they say ‘the vaccine is useless’, then word of mouth begins to circulate” (Interviewee at strategic level - Uruguay).

Program officers in Chile, Paraguay, and Uruguay mention the population’s belief in myths about the vaccine, including that it will lead to the development of a more severe form of the disease:

“People generally believe in the myth that if they get vaccinated, they will get a more severe flu, more severe symptoms (...) A cold that would occasionally be a normal cold, they associate [it] with vaccination (...) that would lead to a more serious form [of the disease]” (Interviewee at strategic level - Paraguay).

In the Chilean, Paraguayan, and Uruguayan programs, anti-vaccine discourse is perceived as a threat to confidence in the influenza vaccine, as it is believed to generate fear of vaccination and resistance toward it. For the Peruvian program, mistrust is a problem among native, ethnic, and uncontacted groups. Program officers in Chile explicitly said that anti-vaccine misinformation is disseminated via social networks such as Facebook, WhatsApp, YouTube, Twitter, and Instagram, whereas for other countries, no specific sources of misinformation were mentioned, although the existence of anti-vaccine groups was mentioned in Uruguay.

A critical barrier mentioned by all programs, except the Brazilian one, is health personnel’s lack of confidence in the influenza vaccine:

“The same health personnel do not want to be vaccinated. The flu vaccine does not have much credibility regarding its effectiveness or its conviction. Health personnel are not convinced” (Interviewee at strategic level - Paraguay).

Complacency with influenza

Program officers in the five countries perceive complacency with influenza risks as a problem, finding that strategies to reduce it are insufficient. In Chile, complacency is perceived particularly among migrant populations. In Uruguay, complacency among health personnel is highlighted both in their reluctance to promote the vaccine across risk groups and to apply it to themselves:

“In medical groups, it is discussed whether to vaccinate or not, so (...) if that is installed, it is very difficult to reverse, that is, I know that risk groups are not reached as they would like to” (Interviewee at operational level - Uruguay).

In Chile, mass media spotlights regarding the flu are perceived as more influential than programs to reduce complacency:

“We campaign every year, but what influences the most is when people feel at risk. Last year, there was a lot of demand after what had happened in the Northern hemisphere” (Interviewee at strategic level - Chile).

In Brazil, barriers to reduce complacency are perceived specifically among pregnant women, a situation believed to be reinforced by the reluctance of health personnel to indicate the vaccine during the gestation period:

“There is this well-known fear regarding the vaccination of pregnant women (...) I think there are still many physicians who do not recommend vaccines and many pregnant women who, depending on the recommendation, are afraid and will not go” (Interviewee at operational level - Brazil).

Furthermore, program officers in Brazil perceive complacency with influenza risks as a paradoxical consequence of the success of the program, with reduced influenza morbidity and mortality minimizing exposure to the risk of becoming ill.

Discussion

To the best of our knowledge, this is the first study conducted across South American countries to assess how NIPs balance problem formulation and strategy implementation to address influenza vaccination hesitancy by high-priority risk groups. Our results suggest that NIPs are mostly concerned with addressing influenza vaccine convenience by identifying specific barriers (Box 2) and supporting the program on facilitators (Box 3) bearing on vaccine supply. In contrast, the identification of barriers and facilitators related to influenza vaccine confidence and to complacency with influenza are underdeveloped. Countries that report high vaccination coverage rates (Brazil and Chile) tend also to report fewer barriers and more facilitators across program components than low vaccination coverage countries (Paraguay, Peru, and Uruguay). However, program officers across all countries perceive difficulties in addressing vaccine confidence and complacency with influenza.

The legal support that NIPs receive guarantees the allocation of financial resources for vaccination campaigns, with resource restrictions related more to programming issues than to financial shortages. This support is likely to influence the free availability of the vaccine for the at risk populations. All NIPs perceive vaccine purchase and distribution as mostly satisfactory, except for Uruguay, thus, with specific distribution challenges thus ensuring that the vaccine is available prior to the flu season. Though Brazilian, Paraguayan, and Peruvian NIPs found problems of geographic access affecting vaccine convenience, these are focused mostly on rural and Indigenous populations.

Personnel shortages were mentioned mostly for the remote parts of the countries or with migrant populations. Participants mentioned the lack of competencies to address vaccine hesitancy only for Indigenous and migrant populations. Thus, the question arises if local health personnel possess the required competencies to build confidence and decrease complacency. Only Paraguay and Peru mention educational and cultural barriers on the part of beneficiary populations - the latter, only for Indigenous populations. However, respondents reported no specific strategies to tackle these problems. Collaboration with health service providers is perceived as satisfactory across NIPs, although they found opportunities to strengthen collaboration with civil society organizations. NIP monitoring is stronger in Brazil and Chile than in the other three studied countries, although this critical program component restricts itself to vaccine coverage surveillance and leaves out confidence and complacency indicators.

NIP officers perceive confidence and complacency as acute problems affecting coverage and consider the need to improve communication and information strategies. However, they observed no specific efforts to address them. Officers see influenza vaccine hesitancy as particularly influenced by culture and myths as compared to other vaccination programs. Furthermore, they found severe barriers and facilitators to address confidence and complacency, such as the reluctance of health personnel to recommend the vaccine to pregnant women and the influence of mass media.

Among the most prominent concern perceived is how incapable NIPs are to plan according to their needs, particularly in estimating target risk groups. Informants’ perceptions coincide with the situation reported by Ropero et al. ²⁵25. Ropero-Álvarez AM, Omeiri NE, Kurtis HJ, Danovaro-Holliday MC, Ruiz-Matus C. Influenza vaccination in the Americas: progress and challenges after the 2009 A(H1N1) influenza pandemic. Human Vaccines and Immunotherapeutics 2016; 12:2206-14. for adults with chronic conditions in Latin American and Caribbean countries. The absence of specific denominators has been indicated as a barrier to implementing influenza vaccination programs that affect the scheduling of immunization activities and their monitoring ⁷7. Palache A, Oriol-Mathieu V, Fino M, Xydia-Charmanta M. Seasonal influenza vaccine dose distribution in 195 countries (2004-2013): little progress in estimated global vaccination coverage. Vaccine 2015; 33:5598-605..

The need for training and motivating health personnel is critical to addressing confidence and complacency, individuals who often suffer from overload and receive few training opportunities ²⁶26. Bresee J, Fitzner J, Campbell H, Cohen C, Cozza V, Jara J, et al. Progress and remaining gaps in estimating the global disease burden of influenza. Emerg Infect Dis 2018; 24:1173-7.. Although training strategies were in place in all studied countries, informants perceived health personnel’s low acceptance and sensitivity to recommend the vaccine. In Nigeria, a study has found that NIPs focus on the technical components of the program at the expense of the development of communication skills ²⁷27. Oku A, Oyo-Ita A, Glenton C, Fretheim A, Ames H, Muloliwa A, et al. Perceptions and experiences of childhood vaccination communication strategies among caregivers and health workers in Nigeria: a qualitative study. PLoS One 2017; 12:e0186733., despite the importance of interactions between people and health professionals, particularly to provide trusted information about vaccines ²⁸28. Ames H, Glenton C, Lewin S. Parents' and informal caregivers' views and experiences of communication about routine childhood vaccination: a synthesis of qualitative evidence. Cochrane Database Syst Rev 2017; (2):CD011787..

Brazilian and Chilean officers’ perceptions of vaccination strategies are, in general, more favorable than those from the other three countries. However, Uruguay is the country in which program officers more sharply indicated complacency problems. Notably, this country also reports the lowest vaccination rate. In a health service exit survey of individuals across risk groups, conducted by the authors in the same countries, Uruguay showed the highest complacency, particularly regarding the perception of influenza as a serious risk as well as the knowledge of influenza and the vaccine. Uruguay was also the country with the lowest confidence in the vaccine. A logistic regression suggested that confidence most strongly predicts vaccination rates, thus placing Uruguay at a greater disadvantage ²⁹29. González-Block MA, Gutiérrez-Calderón E, Pelcastre-Villfuerte B, Arroyo-Laguna J, Comes Yamila, Crocco P, et al. Influenza vaccination hesitancy in five countries of South America. Confidence, complacency and convenience as determinants of immunization rates. PLoS One 2020; 15:e0243833..

The reported rise of anti-vaccine movements across several of the studied countries is a concern, suggesting the role that access to digital information and social networks can have in facilitating the dissemination of anti-vaccine messages and access to health information based on individual experiences (“experience-based”), rather than on scientific evidence (“evidence-based”) ³⁰30. Dubé E, Vivion M, MacDonald NE. Vaccine hesitancy, vaccine refusal and the anti-vaccine movement: influence, impact and implications. Expert Rev Vaccines 2015; 14:99-117.. A study conducted in 2019 by Avaaz, in partnership with the Brazilian Immunization Society (SBIm), indicated that 67% of the Brazilians interviewed believed in at least one inaccurate information about vaccines ³¹31. Avaaz; Sociedade Brasileira de Imunizações. As Fake News estão nos deixando doentes? Como a desinformação antivacinas pode estar reduzindo as taxas de cobertura vacinal no Brasil. https://sbim.org.br/images/files/po-avaaz-relatorio-antivacina.pdf (accessed on 14/Feb/2020).
https://sbim.org.br/images/files/po-avaa... . According to the survey, respondents who believe that vaccines are partially or completely unsafe (72% and 59%, respectively) received news about vaccines via social media or messaging services ³¹31. Avaaz; Sociedade Brasileira de Imunizações. As Fake News estão nos deixando doentes? Como a desinformação antivacinas pode estar reduzindo as taxas de cobertura vacinal no Brasil. https://sbim.org.br/images/files/po-avaaz-relatorio-antivacina.pdf (accessed on 14/Feb/2020).
https://sbim.org.br/images/files/po-avaa... . Evidence on childhood vaccination suggests that populations in low- and middle-income countries are increasingly exposed to information relating to real or supposed vaccine harm, and to trust issues with medicine, science, and the health system ⁸8. Cobos Muñoz D, Monzón Llamas L, Bosch-Capblanch X. Exposing concerns about vaccination in low- and middle-income countries: a systematic review. Int J Public Health 2015; 60:767-80.. Health personnel in high-income countries have been found to be motivated to accept vaccination as a measure to protect themselves and their patients, yet, they manifest beliefs that can pose barriers to vaccination, and particularly to the promotion of influenza vaccine among the population, including concerns about side-effects, skepticism about vaccine effectiveness, and the belief that influenza is not a serious illness ³²32. Lorenc T, Marshall D, Wright K, Sutcliffe K, Sowden A. Seasonal influenza vaccination of healthcare workers: systematic review of qualitative evidence. BMC Health Serv Res 2017; 17:732..

Our findings suggest the need for NIPs in the studied countries to be more engaged in developing communication strategies that go beyond the “information deficit” model and consider the social, cultural, and political context in which people live ³⁰30. Dubé E, Vivion M, MacDonald NE. Vaccine hesitancy, vaccine refusal and the anti-vaccine movement: influence, impact and implications. Expert Rev Vaccines 2015; 14:99-117.^,3333. Rossen I, Hurlstone M, Lawrence C. Going with the grain of cognition: applying insights from psychology to build support for childhood vaccination. Front Psychol 2016; 7:1483.^,3434. Dubé E, Gagnon D, Vivion M. Optimizing communication material to address vaccine hesitancy. Can Commun Dis Rep 2020; 46:48-52.. Communication strategies need to consider the specific media coverage and national experience with influenza vaccine hesitancy since the H1N1 pandemic ³⁵35. Yaqub O, Castle-Clarke S, Sevdalis N, Chataway J. Attitudes to vaccination: a critical review. Soc Sci Med 2014; 112:1-11..

Health programs in low- and middle-income countries are being innovated to enable health authorities and providers to address demand-side determinants by introducing financial incentives and subsidies and promoting community involvement ³⁶36. Elmusharaf K, Byrne E, O'Donovan D. Strategies to increase demand for maternal health services in resource-limited settings: challenges to be addressed. BMC Public Health 2015; 15:870.. Our study suggests that only Chile has introduced these incentives. Poverty reduction programs based on conditional cash transfers (CCT) have prioritized increasing demand for health promotion and prevention, including vaccination ³⁷37. Gopalan S, Mutasa R, Friedman J, Das A. Health sector demand-side financial incentives in low- and middle-income countries: a systematic review on demand- and supply-side effects. Soc Sci Med 2014; 100:72-83.. In Brazil and Colombia, CCTs have been put in force via the Bolsa Familia and Familias en Acción programs, respectively ³⁸38. Segura-Pérez S, Grajeda R, Pérez-Escamilla R. Conditional cash transfer programs and the health and nutrition of Latin American children. Rev Panam Salud Pública 2016; 40:124-37.. Evidence has shown the effectiveness of such programs in improving children’s health status and access to preventive services, although not directed to vaccination services ³⁸38. Segura-Pérez S, Grajeda R, Pérez-Escamilla R. Conditional cash transfer programs and the health and nutrition of Latin American children. Rev Panam Salud Pública 2016; 40:124-37.^,3939. Lopez-Arana S, Avendano M, van Lenthe FJ, Burdorf A. The impact of a conditional cash transfer programme on determinants of child health: evidence from Colombia. Public Health Nutr 2016; 19:2629-42.. These programs have mostly targeted children and pregnant women, and should be considered in addressing adults with chronic conditions and older adults’ health and vaccination needs. However, CCTs have relied on recipients’ cost-benefit analyses and do not necessarily address confidence and compliance with health interventions, which depend on perceptions of the health system, cultural values, and psychological realities ⁴⁰40. Brewer NT, Chapman GB, Rothman AJ, Leask J, Kempe A. Increasing vaccination: putting psychological science into action. Psychol Sci Public Interest 2017; 18:149-207..

The monitoring of vaccine hesitancy by immunization programs has been increasingly recommended as a key strategy for epidemiological surveillance. Larson et al. ⁴¹41. Larson HJ, Figueiredo A, Xiahong Z, Schulz WS, Verger P, Johnston IG, et al. The state of vaccine confidence 2016: global insights through a 67-country survey. EBioMedicine 2016; 12:295-301. propose the regular monitoring of vaccine attitudes, coupled with the monitoring of national and sub-national immunization rates, to identify populations with declining confidence and acceptance. Such recommendations are now being applied to monitor COVID-19 vaccine hesitancy, precisely indicating the groups that require special surveillance, as well as supporting health promotion and communication strategies targeting them ⁴²42. Hardy B. Surgo Ventures Projects U.S. COVID-19 vaccination rates will plateau in late april - before we reach herd immunity. https://static1.squarespace.com/static/5f7671d12c27e40b67ce4400/t/6075bc376125561b742e9ff5/1618328632135/final+press+release-surgo+ventures+gen+pop+followup+survey+%281%29.pdf (accessed on 16/Jun/2020).
https://static1.squarespace.com/static/5... ^,4343. Crowe D. Almost one-third of adult Australians say they're unlikely to get COVID vaccination: survey. The Age 2021; 19 may. https://www.theage.com.au/politics/federal/almost-one-third-of-adult-australians-say-they-re-unlikely-to-get-covid-vaccination-survey-20210518-p57szo.html
https://www.theage.com.au/politics/feder... ^,4444. Khan MS, Mohsin SA, Adelaine A, Karan A. Rethinking vaccine hesitancy among minority groups. Lancet 2021; 397:1863-5.^,4545. Office for National Statistics. Coronavirus and vaccine hesitancy, Great Britain - 13 January to 7 February 2021. London: Office for National Statistics; 2021..

A limitation of this study is the bias that could have been introduced by informants regarding the situation of barriers and facilitators of influenza vaccination programs. However, these perceptions reflect the knowledge and attitudes of key personnel in charge of the programs, thus influencing the programs operation.

Conclusions

NIPs, and specially influenza vaccination, have made significant progress in planning, purchasing, and distributing biologicals. NIPs in the studied South American countries show similar barriers and facilitators affecting their operation. These programs give most attention to the determinants of hesitancy related to improving the availability and access of biologicals among public and private providers and with the support of civil society organizations. While these strategies prioritize the convenience of vaccination, there are some opportunities to address confidence and complacency via specific strategies by integral approaches, including social, economic, and psychological incentives and tools. To this end, programs can strengthen training and incentives to improve competencies and interests of the health personnel on their role as the main promoters of vaccination. Furthermore, communication strategies must be developed to respond to the concerns of specific risk groups targeted for influenza vaccination.

Acknowledgments

This project was financially supported by Sanofi Pasteur.

References

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