Infectious Diseases

ISSN: 2374-4235 (Print) 2374-4243 (Online) Journal homepage: http://www.tandfonline.com/loi/infd20

The financial crisis and the expected effects on vaccinations in Europe: a literature review Helena C. Maltezou & Christos Lionis To cite this article: Helena C. Maltezou & Christos Lionis (2015) The financial crisis and the expected effects on vaccinations in Europe: a literature review, Infectious Diseases, 47:7, 437-446 To link to this article: http://dx.doi.org/10.3109/23744235.2015.1018315

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Date: 12 October 2015, At: 04:55

Infectious Diseases, 2015; 47: 437–446

REVIEW ARTICLE

The financial crisis and the expected effects on vaccinations in Europe: a literature review

HELENA C. MALTEZOU1 & CHRISTOS LIONIS2

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From the 1Department for Interventions in Health Care Facilities, Hellenic Center for Disease Control and Prevention, Athens and 2Clinic of Social and Family Medicine, Faculty of Medicine, University of Crete, Heraklion, Greece

Abstract Starting in 2008 several European countries experienced a financial crisis. Historically, diseases whose prevention and treatment depend highly on the continuity of healthcare re-emerge during political and financial crises. Evidence suggests that the current financial crisis has had an impact on the health and welfare of Europeans and that population health status and morbidity as well as mortality patterns may change in the coming years. At the same time decisions about expenditure for health services may impact the ability of public health providers to respond. It is expected that the current crisis will further exacerbate socioeconomic and health inequalities and novel vulnerable groups will emerge in addition to existing ones.We review the available evidence and discuss how the current crisis may have an impact on vaccine-preventable diseases and influence vaccination coverage rates in Europe.

Keywords: Vulnerable populations, healthcare services, vaccine-preventable disease, public health

‘Άνευ αιτίου ουδέν εστίν.’ ‘Nothing is causeless.’ Aristotle, ancient Greek philosopher (384–322 BC)

Introduction During the second half of the twentieth century tremendous advances in vaccine development led to the prevention of millions of infections, deaths, and debilitating sequelae among children globally and the control or elimination of several infectious diseases [1–3]. Nowadays routine vaccination programs remain pivotal in public health and are widely implemented to protect human health at the host level and the population as a whole. Although economic evaluations of vaccinations have been used rarely for informing policy-makers, post-licensure studies indicate an expanding spectrum of benefits and even saving costs associated with the introduction of vaccines in national vaccination programs [1,4–8].

Starting in 2008, Europe experienced a financial crisis that substantially lowered economic growth rates. The gross domestic product (GDP) per capita in the European Union (EU) contracted by 4.8% in 2009, stabilized during 2010–2011 and dropped again by 0.6% in 2012 [9]. Unemployment rates rose from 7.2% in 2007 to 10.8% in 2013; however, there are countries with unemployment rates as high as 27.3% and 26.1% (Greece and Spain, respectively) [10]. Nowadays the financial crisis continues in several European countries, with limited signs of recovery. In an environment where the demand for financial cuts governs political decisions, many Europeans have been negatively influenced. Historically, diseases whose prevention and treatment depend highly on the continuity of healthcare and drug supply, such as tuberculosis and HIV/AIDS, re-emerge during political and financial crises [11–13]. There is growing evidence that the current financial crisis has had an impact on the health of Europeans and thus population needs may change in the coming years [14–16]. Overall, important decisions about

Correspondence: Helena Maltezou, Department for Interventions in Health Care Facilities, Hellenic Center for Disease Control and Prevention, 3-5 Agrafon Street, Athens, 15123 Greece. Tel: ⫹ 30 210 5212 175. Fax: 0 210 5212 177. E-mail: [email protected] (Received 15 September 2014 ; accepted 8 February 2015) ISSN 2374-4235 print/ISSN 2374-4243 online © 2015 Informa Healthcare DOI: 10.3109/23744235.2015.1018315

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expenditures for health services are made that may impact the ability of public health providers to respond [17]. However, inequalities in health existed in Europe before the current financial crisis as elsewhere [18–21]. From a vaccinations perspective, differences among and within European countries have been consistently reported, in terms of national vaccination programs, vaccination services, access to vaccination, attitudes toward vaccinations, and eventually vaccination coverage rates [21–29]. It is expected that the current crisis will further exacerbate socioeconomic and health inequalities and novel vulnerable groups will emerge in addition to the old ones [17]. The potential impact of the current financial crisis on vaccination coverage rates in Europe has been included in certain reports; however, it has not received the interest that this subject deserves. To the best of our knowledge, an analysis focusing on the potential impact of the financial crisis on vaccinepreventable diseases and vaccination coverage rates in Europe has not been conducted so far. In this article we systematically review the published evidence on how the current crisis may have an impact on health and healthcare services in terms of vaccine-preventable diseases and may influence vaccination coverage in Europe. Issues of policy-making, access to vaccination services, and vaccination costs are also discussed. It also aims to draw suggestions to strengthen healthcare services and meet vaccination needs.

‘adults,’ ‘Roma,’ ‘homeless,’ ‘unemployed,’ ‘intravenous drug users,’ and ‘immigrants.’ Review articles and websites of international organizations (World Health Organization (WHO), European Centre for Disease Prevention and Control (ECDC), European Commission) were also studied. Articles presenting original or aggregated data from upper-income and upper-middle-income economies ( ⫽ countries) in accordance with the World Bank classification, on vaccine-preventable diseases and vaccination coverage rates in relation to socioeconomic conditions were selected for inclusion [30]. Epidemics of vaccinepreventable diseases were also selected based on their relevance. No comprehensive reviews on the potential impact of financial crises on vaccine-preventable diseases were found. We added to the identified articles a couple of other articles that we have chosen by a selective hand search in relevant journals. In total 143 articles were studied and 90 were included in this review (27, 39, and 14 articles provided information about vaccination coverage rates, vulnerable populations with poor socioeconomic conditions, and/or epidemics, respectively) (Figure 1). Overall, the available data about socioeconomic variables were fragmentary in most cases and not nationwide or systematically collected. All articles were reviewed by both authors.

Vaccinations in Europe Childhood vaccinations

Review strategy We searched the PubMed database until May 7, 2014 using combinations of the words ‘financial crisis,’ ‘economic crisis,’ ‘Europe,’ ‘health,’ ‘healthcare services,’ ‘vaccine-preventable diseases,’ ‘vaccination,’ ‘socioeconomic,’ ‘risk factors,’ ‘children,’

Significant country-to-country variations among national childhood vaccination programs exist in Europe, in terms of included vaccines, doses, target ages, and legislative frame (mandatory or recommended vaccinations) [31]. The ‘old’ vaccines against diphtheria, tetanus, pertussis, Haemophilus

PubMed database (original articles & reviews)

Websites of international organizations

143 articles were studied

90 articles were included

Hand search in relevant journals 53 articles were excluded (out of scope, 42; overrepresentation of information, 10; insufficient data, 1)

Figure 1. Flow chart of the selected articles.

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Financial crisis and vaccinations influenzae, poliomyelitis, measles-mumps-rubella (MMR), and hepatitis B are recommended in all 31 EU/European Economc Area (EEA) countries. With the exception of the pneumococcal conjugate and human papillomavirus (HPV) vaccines (recommended in 25 countries each) and the meningococcus serotype C conjugate vaccine (recommended in 16 countries), the remaining ‘newer’ vaccines (varicella, hepatitis A, rotavirus) are recommended in less than half European countries each [31]. Differences in terms of vaccination services and funding policies also exist and may further affect access to vaccination services and thus coverage during the financial crisis. Although very good vaccination coverage rates are recorded among children in Europe as a whole, suboptimal vaccination rates are found in several countries and in population subgroups. Studies from Europe, the USA, and China carried out during 2005–2013 indicate that socioeconomic variables are strongly associated with lower uptake rates of several vaccines in childhood. Such variables include higher levels of poverty, unemployment of the father, large families, race, immigrant status, and lower adolescent educational level [32–35]. Factors that have been repeatedly linked with higher vaccine uptake in children include high socioeconomic status, higher income, residence area, parental educational level, use of healthcare by mothers, positive maternal attitudes about vaccines, and satisfaction with information provided by healthcare professionals about vaccines [28,33,36,37]. In terms of vaccination policies, school-based vaccination programs against HPV have been successfully implemented in recent years, and provide an opportunity to overcome issues of costs, access to healthcare services, and parental attitudes [36,38,39]. School entry mandates for vaccines have also increased meningococcal C vaccine uptake [34]. Adulthood vaccinations Adult vaccination programs lag well behind childhood programs. A 2010–2011 survey revealed that only 12 (38.7%) of 31 economically advanced countries had comprehensive vaccination programs for adults [23]. Influenza, pneumococcal, and hepatitis B vaccines were the prevalent recommended vaccines for adults and a funding mechanism existed for most of them. Higher GDP and health expenditure per capita were associated with a high likelihood of a recommendation for a vaccine [23]. Free-of-charge influenza vaccinations, personal reminding letters, and vaccination coverage monitoring systems have been consistently associated with increased vaccine uptake rates among adults

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[27,40]. A survey conducted with more than 90 000 household contacts in 11 European countries during 7 consecutive influenza seasons (2001/2002 through 2007/2008) showed that, in addition to the known risk factors of older age and chronic illness, socioeconomic variables, such as level of education, household income, household size, and population size of residence area, influence the likelihood to get vaccinated against influenza; however, with different expressions among countries [22]. We can assume that socioeconomic factors will increase in importance, as poverty has increased due to the financial crisis.

Specific vulnerable populations with poor socioeconomic conditions Roma populations Large-scale measles epidemics occurred in several European countries during the past decade. In 2010 alone, more than 30 000 measles cases were notified and Roma populations were disproportionally affected [41]. Roma is the most populous ethnic minority in Europe, with an estimated population of 11 million people [42]. Although there are no systematic studies on the health of Roma populations, recent studies indicate an excess of infection-related morbidity in young Roma children in terms of acute respiratory infections, influenza, otitis media, bronchitis, pneumonia, and tuberculosis, as well as infant mortality [21,43–45]. High incidence rates of hepatitis A and B are also detected in Roma children (82% seroprevalence against hepatitis A in Roma children compared with 9.3% in non-Roma children in Spain) [21], and a large hepatitis A outbreak among Roma populations occurred in Greece in 2007 [46]. Gaps in sanitary conditions, poverty, large households, low maternal education, limited access to healthcare, and ethnicity per se have been associated with these findings [21,25,43,45,46]. Recent studies have repeatedly found low vaccination rates against measles in Roma children (51% in Poland [25]; 7–8% in Greek Roma children compared with 83% in non-Roma Greek children [47]), which renders them at high risk for acquisition of measles. In Bulgaria, where most measles cases in Europe occurred, mainly in Roma settlements, very high case fatality rates and complication rates were noted [29]. In this setting, maternal education, immunization status of the child, and households declaring an income were associated with a decreased risk for developing severe complications such as pneumonia or encephalitis from measles [29]. The recent measles epidemics in Europe also affected young children and young adults whose

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parents had refused their routine vaccination against measles sometime in the past because of concerns about the safety of the MMR vaccine, religious or anthroposophic opinions, opposition to vaccinations or simply missed vaccination opportunities [41,48]. Despite proven efficacy and safety for more than 50 years, the MMR vaccine has been in the epicenter of an increasing anti-vaccination movement in Europe for the past two decades, with detrimental results. Pockets of unvaccinated persons in several European countries served as the ideal background for the sustainment and propagation of measles outbreaks [49–53]. This epidemic challenged public health authorities in Europe but also in measles-free countries like the USA, because of importation of measles cases and the onset of several generations of cases [41]. Analysis of 6-year data from 29 EU/EEA countries with vaccination coverage rates against measles ranging from 72.6% to 100% found that higher vaccination coverage rates against measles were associated with a lower burden of measles [6]. In England, a country where coverage with the MMR vaccine has declined since 2000, researchers have looked at socioeconomic factors in relation to MMR coverage and found that lower coverage rates strongly correlated with population density and deprivation [54]. This is of concern, because young children in deprived areas are more likely to have a poor health status and thus are at higher risk for complications compared with children in non-deprived areas [54]. In a similar vein, a 2003 study in north-west London found that uptake of the first MMR dose increased with higher socioeconomic status and among children with Asian background compared with Afro-Caribbean and white children (87.1%, 74.7%, and 57.5%, respectively) [24]. Outbreaks of rubella and mumps still occur in Europe as well [55,56]. Suboptimal vaccination coverage rates and late adoption of two MMR doses in several central European countries mainly explain these outbreaks [57]. Based on the above, it is also expected that the poor access of families to primary care services may lead to a decrease of vaccination rates in Roma and other vulnerable populations. Homeless persons and intravenous drug users Homeless persons and intravenous drug users (IDUs) are typical examples of vulnerable groups facing health inequalities because of financial issues, selfneglect behavior, poor mental health, and limited access to healthcare services. When healthcare is available, often it is complicated because of fragmentation of services. Because of their poor living conditions, homeless persons are highly vulnerable to specific infectious diseases, such as invasive

pneumococcal disease, tuberculosis, HIV, hepatitis A, B, C, and E, and scabies [58–60]. A prospective, population-based surveillance study for invasive pneumococcal disease in homeless adults in Toronto, Canada during a 5-year period revealed an incidence of 273 infections per 100 000 persons per year compared with 9 per 100 000 persons per year in the general adult population [59]. Compared with the general adult population, homeless persons with invasive pneumococcal disease were younger, were statistically more likely to have underlying conditions (smoking, alcohol abuse, intravenous drugs use, and underlying lung disease), and had a fivefold risk for recurrent disease [59]. Similarly, a 2012 cross-sectional study among 455 homeless persons in 27 homeless hostels in London, found that 4 in 10 homeless persons faced chronic health problems, which predisposed them to serious influenza-related morbidity [61]. Despite this, influenza vaccine uptake was 23.7% among 16–64-year-old homeless persons with a chronic underlying condition compared with 53.2% nationally. In homeless persons ⬎ 65 years old, vaccine uptake was 42.9% compared with 74% nationally [61]. Gaps in immunity against measles, diphtheria, and tetanus have been reported among homeless persons [62]. IDUs are also at high risk for a variety of parenterally transmitted infections and frequently have chronic conditions for which influenza and pneumococcal vaccinations are recommended [63]. Large outbreaks of hepatitis A have been recorded among homeless drug users in inner European cities, which have been successfully contained with mass vaccination [64,65]. In the past decade routine vaccination programs against hepatitis A and hepatitis B have been implemented successfully in shelters and clinics as part of routine healthcare services for homeless populations [66,67]. Gaps in knowledge about vaccinations and vaccine-preventable diseases have been revealed among homeless people [68]. Studies indicate that culturally sensitive counseling and education improve their knowledge and overall acceptance of vaccinations, achieving high vaccine uptake rates [66,67]. A 16-fold increase of notified HIV-1 infections among IDUs was noted in Greece in 2011 compared with 2010 [69]. Most cases (81.2%) were males of Greek origin and transmission was confined in the Athens metropolitan area; however, phylogenetic analyses revealed that most HIV-1 strains were geographically consistent with the recent migratory waves in Greece [69]. This study also demonstrated an inverse correlation between the recent GDP decline in this country, the annual HIV and hepatitis C virus prevalence rates, and the unemployment and homelessness rates in IDUs [69]. An alarming increase in

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Financial crisis and vaccinations the number of IDUs newly diagnosed with multiple viral hepatitis and HIV co-infections has been also noted in Romania during 2011–2012 and has been linked to financial constraints [70]. The recent IDUrelated outbreaks highlight the risk of silent epidemics of diseases with prolonged incubation periods in the context of social and economic deprivation. Homeless people and other vulnerable subpopulations with poor socioeconomic conditions are expected to increase significantly in the coming years in Europe. Efforts should be made to overcome barriers and to provide vaccination services to homeless persons and IDUs along with other healthcare interventions, such as chest-X-ray screening for tuberculosis. Vaccinations against seasonal influenza annually and complete vaccination against hepatitis A, hepatitis B, measles, diphtheria, tetanus, and pneumococcal infection are justified. Although decreased antibody responses are often detected in IDUs post-vaccination, there is no conclusive evidence linking these observations to a decreased clinical protection [71]. Hepatitis C vaccines are highly needed for IDUs and clinical vaccine trials in at-risk HCV-uninfected IDUs are under way [72]. Street- and shelter-based interventions are the most efficient ways to reach homeless people. Methadone substitution and needle exchange programs have been used successfully to reach IDUs with no consistent healthcare [63]. Migrants The enormous influx of migrants from developing countries to Europe during the past decade has also influenced the epidemiology of certain infectious diseases in their host countries, including vaccine-preventable diseases [20,73–75]. As of January 1, 2013 there were 33.5 million foreign-born people with a diverse background living in the EU, which represents 6.7% of the EU population [76]. Immigrant children, and especially those of newly arrived immigrants, tend to have significantly lower vaccination coverage rates and delayed vaccinations compared with indigenous European children, which is attributed to financial, health access, cultural, and linguistic difficulties [33,77]. Illegal immigrants residing under deprived conditions in several inner cities in Europe constitute an emerging public health problem. In a recent report Greek rural general practitioners (GPs) raised concerns about where resources should be allocated to address the healthcare needs of immigrants and other vulnerable population [78]. They reported that communicable diseases are associated with poverty and loss of individual control and they constitute a real threat in a period where limited resources are available for their management [78]. The poor access of migrant populations to healthcare

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services and the lack of monitoring data constitute an additional barrier in designing and implementing effective vaccination programs for this group. It should be kept in mind, however, that the susceptibility to vaccine-preventable diseases and vaccination coverage rates among migrants, homeless persons, and IDUs may differ among and within communities, because of different ethnic, socioeconomic, and educational backgrounds and duration of immigration, homelessness, and intravenous drug injection. Lessons from the past Evidence from the past indicates that disruption or sub-financing of healthcare services in light of financial, political, and humanitarian crises may impact vaccine uptake rates and trigger the onset of epidemics, even in countries with prior well-established vaccination programs. An excellent review of the US experience with child health and healthcare services in relation to changes in economic trends showed that between 1980 and 1982, when two economic recessions occurred successively, children were disproportionally affected [79]. Compared with nonpoor children, poor children had fewer per capita visits and fewer preventive visits [79]. Expenditure cuts were associated with more people seeking care in the public health sector who had a diminished capacity to respond. A 6% reduction of completely vaccinated 2-year-old children was reported in the State of Colorado between 1980 and 1982 [79]. After more than two decades during which diphtheria was controlled, the Russian Federation faced a large-scale diphtheria epidemic in the 1990s, with 115 088 reported cases and 3078 fatalities during 1990–1997 [80]. In contrast to the pre-vaccine era, most cases occurred among adult age cohorts. A large accumulation of susceptible hosts through the years provided the perfect background for the propagation of this epidemic; approximately 30% of adults had received a booster shot in the past 10 years while early childhood vaccination coverage rates below 80% were routinely recorded during 1989–1993 in a context of an increasing reluctance to vaccinate among pediatricians because of safety concerns [80]. Mass internal movement of people and migration to large urban centers, crowded living conditions, and increased homelessness traced to the collapse of the Soviet Union, contributed to the rapid spread of the epidemic across several former Soviet Union Democracies [80]. The Global Polio Eradication Initiative of WHO is currently challenged by the re-emergence of poliomyelitis in a few non-endemic countries in Africa and Asia, including Syria [81]. As of December 4, 2013, 17 laboratory-confirmed cases among young children

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have been notified from Syria. Syria had excellent early childhood vaccination coverage rates against poliomyelitis during 2002–2010 but as low as 52% vaccination rates in 2012, in the light of the disruption of healthcare services in many areas because of the current conflicts. The ECDC risk assessment concluded that there is a high risk of importation and re-establishment of circulation of wild poliomyelitis virus and a moderate risk of disease in the EU, especially in low or unvaccinated groups [81]. Currently there are 12 million people ⬍ 30 years old in the EU who are unvaccinated against poliomyelitis and herd immunity is problematic. As of December 2013, there were more than 2 million registered Syrian refugees, representing an increase of 700 000 since July 2013 [81]. First signs There is limited evidence of the impact of the financial crisis on vaccination coverage rates, based on published literature. A recent technical report issued by ECDC [17] presented evidence that health inequalities play a strong role in transmission of infectious diseases. In addition, the recent large outbreaks, such as measles in Bulgaria, indicate that large population groups have had poor access to vaccinations and to the healthcare system [17]. In Greece a 22% rise in visits to public healthcare services was recorded in recent years because people cannot afford private healthcare, along with a rise of out-of-pocket costs for healthcare. More importantly, the financial crisis in Greece left many people without a personal doctor. In this setting street clinics have been operated by non-governmental and charitable organizations to run health checks and immunization programs, but without a comprehensive approach and coordination. As Stuckler et al. pointed out [82], prevention services were deemed particularly susceptible to budget cuts as a result of financial crisis compared with primary care. Especially in countries where integrated primary care was not a key issue before the onset of the current financial crisis [83], the impact of the financial crisis on both the quality of primary care services and health promotion/diseases preventionrelated services is anticipated to be high [84]. Although published evidence is limited, the immunization programs in children in Greece seem to be affected, despite the high vaccination coverage rates noted before the austerity [47]. Data from an academic capacity that operates jointly with the municipality services in Heraklion, Greece revealed incomplete vaccination schemes in children of uninsured families either of Greek origin or migrants. According to this study, 8.6% of the children aged 23 months and more from migrants have completed

two doses of hepatitis A vaccination. In the same direction the MMR coverage in children 6 years old (two doses) was 28.9%, while the corresponding rate against varicella was 5.3% (C. Lionis, unpublished report). A low vaccination rate against pneumococcus among elderly primary care visitors has also been reported recently in rural Crete and it is unknown to what extent the financial crisis and the burden allocated to primary care accounts for this situation [85]. However, we need more observational and prospective data to reflect clearly the current situation in countries affected by the financial crisis.

Considerations regarding healthcare services A recently published report from rural primary care on the island of Crete, Greece underlines the problems that the financial crisis introduced in primary care. GPs reported that the financial crisis resulted in primary care services having limited time for engaging in health promotion and disease prevention activities [78]. The financial crisis could damage the immunization programs in two ways: restricted budget as a result of the health reforms may affect the introduction of new vaccines or the reimbursement of old vaccines, while limited access to vaccines and medicines of people without health care insurance seems to be the most important barrier for families to follow a previously established vaccination program. The lack of continuity and personalized and patient-centered care may enhance reluctance of families to vaccinate their children and it may decrease their compliance to participate in vaccination programs for adults. It should be kept in mind, however, that examples and experiences from one country may not be applicable for other countries, given the differences in healthcare and the available capacity to respond. Austerity also may have an impact on the burden of multimorbidity and frailty, two illness conditions that make the need for vaccination more apparent.

Strengthening primary healthcare services: the stake of public health Despite the profound impact of vaccinations in population and public health, it does not seem to be the first priority for healthcare services in countries affected by the financial crisis. However, a high interest in strengthening primary care in these countries that have been affected by the economic crisis has been stressed. There are many reasons to believe that by strengthening primary care and improving the quality of a healthcare system, the vaccination insufficiencies and health inequalities can be addressed.

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Financial crisis and vaccinations Primary care physicians have a key role in addressing comprehensively and holistically the care of patients and especially the care of vulnerable people. Vulnerable people usually are multimorbid and frail and the need for vaccination coverage is more apparent to them; while the interest in seeing primary care physicians being more involved in the management of frailty by using the appropriate approach has been reflected in the current literature [86,87]. Also, interest in a definition of a frame of reference in relation to primary care with a special emphasis on financing systems and referral systems has been raised recently [88]. The financial crisis has also led the affected countries to rethink the need for introducing primary care in their healthcare reforms. An article by Kousoulis et al. discussed the axes that a healthcare system can reshape to overcome the financial crisis and they focus on equity, quality, value framework, medical professionalism, information technology, and decentralization of healthcare services [89]. However, there is still a lack of evidence on the effectiveness of primary care-based programs to reduce healthcare inequalities introduced by the financial crisis. For that reason primary healthcare services and social protection nets need to be expanded and integrated rather than contracted in times of economic recession. Vaccination services should focus on vulnerable subgroups, for example, Roma, homeless people, children living in poverty, recent migrants. Further, there is a need to move from a childhoodbased vaccination conception to lifespan vaccination for all people and subgroups. Electronic, patientbased monitoring systems for real-time measurement of vaccination coverage are of outmost importance and should be implemented across Europe to assess vaccination services. More flexible vaccine delivery platforms should be evaluated in real life to increase vaccination opportunities among adults with poor socioeconomic conditions, and the role of local and regional administrative bodies needs to be studied. In a recent survey conducted in a US hospital during the implementation of a pertussis vaccination cocooning strategy predominantly among Hispanics, under-insured and medically under-served parents and relatives, 50.5–73.3% of the latter expressed willingness to get vaccinated against influenza, meningitis, and pneumonia during hospital visits or clinic appointments for mothers or infants [90]. School-based vaccinations and on-site vaccinations for specific groups (e.g. IDUs, homeless people) may be expanded and offer an opportunity to vaccinate vulnerable groups and this is also a target for a coordinated and integrated primary healthcare. The effectiveness of educational and training programs to increase the capacity of pri-

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mary care practitioners in settings affected by the economic crisis needs to be explored.

Conclusions In real life vaccination efficacy depends on vaccination programs that work well and on high vaccination rates, which in turn rely on well-functioning primary care services. It is expected that socioeconomic and health inequalities will be further exacerbated in the coming years in Europe and will challenge response and healthcare capacity. Strengthening and expanding primary healthcare services represents the stake to ensure the continuity of vaccinations paying attention to vulnerable subgroups including the homeless and IDUs, which are expected to be affected most by the crisis, and communities with limited access and use of healthcare services (people in poverty, Roma, migrants). It is also crucial to invest in establishing vaccination monitoring systems to provide real-time data; however, in periods of austerity this may not be affordable. Flexible vaccine delivery platforms are expected to facilitate vaccine delivery to vulnerable people and thus reduce vaccination inequalities and should be implemented within an integrated primary healthcare system. Declaration of interest: The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the paper. No funds were received for this study. References [1] Zhou F, Shefer A, Wenger J, Messonnier M, Wang LY, Lopez A. Economic evaluation of the routine childhood immunization program in the United States, 2009. Pediatr 2014;133:577–85. [2] World Health Organization and United Nations Children’s Fund. Global Immunization Vision and Strategy 2006-2015. World Health Organization and United Nations Children’s Fund; 2005. Available at: http://whqlibdoc.who.int/hq/2005/ WHO_IVB_05.05.pdf [accessed May 7, 2014]. [3] Peltola H, Jokinen S, Paunio M, Hovi T, Davidkin I. Measles, mumps, and rubella in Finland: 25 years of a nationwide elimination programme. Lancet Infect Dis 2008;8: 796–803. [4] Barnighausen T, Bloom DE, Canning D, Friedman A, Levine OS, O’Brien J, et al. Rethinking the benefits and the costs of childhood vaccination: the example of the Haemophilus influenzae type b vaccine. Vaccine 2011;29:2371–80. [5] Fesenfeld M, Hutubessy R, Jit M. Cost-effectiveness of human papillomavirus vaccination in low and middle income countries: a systematic review. Vaccine 2013;31:3786–804. [6] Colzani E, McDonald SA, Carrillo-Santisteve P, Busana MC, Lopalco P, Cassini A. Impact of measles national vaccination coverage on burden of measles across 29 Member States of the European Union and European Economic Area, 2006–2011. Vaccine 2014;32:1814–19.

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