Download as pdf or txt
Download as pdf or txt
You are on page 1of 13

Vaccine 31 (2012) 96–108

Contents lists available at SciVerse ScienceDirect

Vaccine
journal homepage: www.elsevier.com/locate/vaccine

Cost-effectiveness and economic benefits of vaccines in low- and middle-income


countries: A systematic review
Sachiko Ozawa a,∗ , Andrew Mirelman a , Meghan L. Stack a , Damian G. Walker b , Orin S. Levine a
a
Department of International Health, Johns Hopkins Bloomberg School of Public Health, 615N. Wolfe St, Baltimore, MD 21205, United States
b
Bill and Melinda Gates Foundation, PO Box 23350, Seattle, WA 98102, United States

a r t i c l e i n f o a b s t r a c t

Article history: Background: Public health interventions that prevent mortality and morbidity have greatly increased over
Received 14 April 2012 the past decade. Immunization is one of these preventive interventions, with a potential to bring economic
Received in revised form 19 October 2012 benefits beyond just health benefits. While vaccines are considered to be a cost-effective public health
Accepted 26 October 2012
intervention, implementation has become increasingly challenging. As vaccine costs rise and competing
Available online 8 November 2012
priorities increase, economic evidence is likely to play an increasingly important role in vaccination
decisions.
Keywords:
Methods: To assist policy decisions today and potential investments in the future, we provide a sys-
Vaccine
Cost-effectiveness
tematic review of the literature on the cost-effectiveness and economic benefits of vaccines in low- and
Economic evaluation middle-income countries from 2000 to 2010. The review identified 108 relevant articles from 51 countries
DALY spanning 23 vaccines from three major electronic databases (Pubmed, Embase and Econlit).
Benefits Results: Among the 44 articles that reported costs per disability-adjusted life year (DALY) averted, vac-
Systematic review cines cost less than or equal to $100 per DALY averted in 23 articles (52%). Vaccines cost less than $500
per DALY averted in 34 articles (77%), and less than $1000 per DALY averted in 38 articles (86%) in one
of the scenarios. 24 articles (22%) examined broad level economic benefits of vaccines such as greater
future wage-earning capacity and cost savings from averting disease outbreaks. 60 articles (56%) gath-
ered data from a primary source. There were little data on long-term and societal economic benefits
such as morbidity-related productivity gains, averting catastrophic health expenditures, growth in gross
domestic product (GDP), and economic implications of demographic changes resulting from vaccination.
Conclusions: This review documents the available evidence and shows that vaccination in low- and
middle-income countries brings important economic benefits. The cost-effectiveness studies reviewed
suggest to policy makers that vaccines are an efficient investment. This review further highlights key gaps
in the available literature that would benefit from additional research, especially in the area of evaluating
the broader economic benefits of vaccination in the developing world.
© 2012 Elsevier Ltd. All rights reserved.

1. Introduction Vaccines may bring economic benefits beyond just health gains
and there may be various pathways for these benefits to accrue.
While vaccines are considered to be a cost-effective pub- Unlike other health interventions, studies find that vaccines avert
lic health intervention, introduction and scale-up have become illness both directly through immunization and indirectly through
increasingly challenging. Governments in low- and middle-income herd immunity [1]. Both types of prevention can lead to a healthier,
countries and the international donor community face growing more productive population that can contribute more toward a
pressures on how to allocate their scarce resources and choose country’s economic development [2]. For example, by averting
among many competing priorities. As the scope and costs of new illness directly, households with vaccinated children can save
vaccines continue to grow, economic evidence is likely to play an medical costs and parents may take fewer days off of work to care
increasingly important role in decisions to introduce and sustain for sick children [3]. By averting disabilities, some vaccines may
vaccination. prevent delays in cognitive development and may also improve
school enrollment and attainment [4]. By averting deaths, vaccines
may even alter fertility decisions due to greater child survival [3,5].
While all such changes can have an immense impact on a country’s
∗ Corresponding author at: 615N. Wolfe St E8003, Baltimore, MD 21205, United
economy, it is difficult to get a full picture of the economic impact
States. Tel.: +1 410 955 3928; fax: +1 410 614 1419.
resulting from immunization. Understanding the full economic
E-mail address: sozawa@jhsph.edu (S. Ozawa). benefits of vaccines is vital to policy makers whose decisions to

0264-410X/$ – see front matter © 2012 Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.vaccine.2012.10.103
S. Ozawa et al. / Vaccine 31 (2012) 96–108 97

introduce new vaccines not only impact the health of a society, but of the economic evidence, we classified data used in the arti-
also its economy. Evidence on such economic benefits is therefore cles as primary data collected from surveys or a demographic
critical in assessing the full return on investment in vaccines. surveillance site, secondary data using data from other studies
For example, with the US$10 billion commitment and call to or publicly available databases, or both. Results from cost-
action by the Bill and Melinda Gates Foundation to increase access effectiveness/cost-utility analyses were converted to 2010 US
to life-saving vaccines during the “Decade of Vaccines” [6], there dollars.
is greater need for evidence on vaccines’ return on investment, To classify the types of economic benefits, we adapted a frame-
particularly at the country level. To assist both future investment work developed by Barnighausen et al. [7,8]. The framework
and policy decisions today, we provide a review of the literature classifies the benefits into seven categories: health gains, health
on the economic benefits of adult and childhood vaccines in low- care cost savings, care-related productivity gains, willingness to
and middle-income countries from 2000 to 2010. This systematic pay and value of statistical life, outcome-related productivity gains,
review addresses four research questions: How cost-effective are behavior-related productivity gains, and outbreak prevention sav-
vaccines? How much are people willing to pay for vaccines? How ings (see description in Fig. 1). While health gains are presented
frequently do economic benefit models use primary data? What in natural units of health (e.g. deaths and illnesses prevented),
narrow and broad economic benefits from vaccination have been all other categories provide economic benefits in dollar units.
reported? The first three categories, health gains, health care cost savings
and care-related productivity gains, take a narrow perspective
where the benefits primarily accrue among households of vac-
2. Materials and methods cinated children at the time of averted illness. The latter four
types of economic benefits are considered to take a broad per-
We conducted a systematic search in three major electronic spective as they capture long-term economic gains experienced by
databases [Pubmed (MEDLINE), Embase and Econlit (EBSCOhost)] those who are vaccinated and society as a whole, including non-
to locate peer-reviewed articles on the economic benefit of vaccines vaccinated community members. Articles on willingness to pay
in low- and middle-income countries. Specifically, we searched for and value of statistical life were also considered to take a broad
articles that tried to quantify this benefit. The search, performed perspective, as they capture the value that both households and
in February 2011, used variations of the following three keywords: society place on the lifetime benefits resulting from immuniza-
“economic benefit” AND “vaccine” AND “low- and middle-income tion. This review focused on articles that went beyond health gains
country”. Relevant MESH terms were selected and a full listing of to capture at least one of the six economic benefits in the frame-
all low- and middle-income countries based on the World Bank work.
country classifications was used in the search. Our search was lim- We quantified the number of articles that measured each type
ited to articles published between 2000 and 2010, since much of economic benefit and summarized our results by year, coun-
of the literature was published during this time and recent lit- try, vaccine analyzed, and kinds of data used in the analyses. We
erature is most relevant to current vaccine policies. The search examined the key results from each type of study, and identi-
was limited to English articles and published literature due to fied the gaps in evidence. PRISMA guidelines were followed for
resource constraints. A few articles were added through expert reporting [9].
consultation, search of the database of Journal of Developmental
Economics and from checking the reference lists of review arti-
cles. 3. Results
From the search results, we examined the titles and abstracts for
inclusion in this review. We included articles that focus on vaccines Pubmed search yielded 1225 articles. The search in Econlit
or vaccine preventable disease and discuss the economic benefits yielded 44 articles where two unique articles were included. The
with a focus on low- and middle-income countries. Articles were Embase search produced 537 articles with nine unique studies. 14
excluded if they did not quantify the economic benefit of vaccines additional articles were identified through reference list review
or discussed only the cost of vaccines, vaccine financing, delivery and expert consultation. The initial screening resulted in 205 arti-
or cold chain issues. The review included articles on both child cles, of which 39 were duplicates. We read full-length versions
and adult vaccines, but excluded studies on animal vaccines, travel of the 166 articles of which 58 articles were further excluded
vaccines, and rabies prophylactic vaccination. We also excluded based on our criteria. This resulted in 108 articles, which were
articles that presented investments in vaccines as an output, rather included in the final review (see Fig. 2 for our search strategy)
than input for economic development. Articles that measured the [10–117].
willingness to pay for vaccines, considered as a valuation of the ben- The articles presented results from 51 different countries or
efit received by households and individuals, were included in the country groupings. 90 articles (83%) presented results for individ-
review. We also included articles that measured the value of statis- ual countries, of which 36 unique countries were represented. The
tical life, which estimate the value of the mortality risk reduction remaining 18 articles (17%) presented results for country group-
resulting from vaccines at the population level. ings such as countries supported by the GAVI Alliance, lower- and
For the selected articles, we extracted both qualitative and quan- middle-income countries, Asian countries, and Latin American and
titative data on authors, title, country, region (classified by the Caribbean countries. All regions were well represented, with 9%
World Health Organization), year of study, vaccine analyzed, type each on Eastern Mediterranean and European regions, 16–20% on
of study, discounting rates, whether primary or secondary data Western Pacific and African regions, and 23% each on Americas
were used, types of costs quantified, types of economic benefits and South-East Asian regions. 26 articles (24%) were published
quantified, and primary results from each article. Studies were between 2000 and 2005, compared to 82 articles (76%) from 2006
categorized into the following types: (1) cost-effectiveness/cost- to 2010.
utility analyses, (2) cost-benefit analyses, (3) studies focusing on The search found articles on 23 individual vaccines. The most
costs of illnesses averted due to vaccines, (4) willingness to pay frequently analyzed vaccine was the rotavirus vaccine with 26 stud-
studies and (5) studies modeling broad economic impacts of vac- ies (24%), followed by ten articles (9%) which examined human
cines. Articles with multiple components could be included in papillomavirus (HPV). Vaccines against cholera, hepatitis B, human
more than one category. In addition, to capture the strengths immunodeficiency virus (HIV), polio, measles, hepatitis A and
98 S. Ozawa et al. / Vaccine 31 (2012) 96–108

Perspecve Type of Benefit Definion

Reducon in mortality or morbidity through vaccinaon


Health gains
presented in natural units of healtha

Narrow Savings of medical expenditures, health care system


Health care cost
savings, and household savings because vaccinaon
savings
prevents illness episodes

Care-related Savings of parents' producve me because vaccinaon


producvity gains avoids the need for taking care of a sick child

Individuals or society's economic valuaon of the long-


Willingness to pay
term benefits from vaccinaon, including producvity
& Value of
Broad gains and benefits of averng pain and suffering from
stascal life
vaccine-preventable diseases

Increased producvity from averted mortality and


Outcome-related morbidity, including the producvity benefits from
producvity gains improved cognion and physical strength, as well as
school enrollment, aendance and aainment

Benefits accruing because vaccinaon improves child


Behavior-related
health and survival and thereby changes household
producvity gains
choices, such as ferlity and consumpon choices

Outbreak Benefits accruing to society from saved costs of


prevenon savings outbreak invesgaons and prevenon

Fig. 1. Economic benefits of vaccine framework. a Natural units of health include numbers of deaths or disability, years of life saved, cases of illness, quality adjusted life
years (QALY) or disability adjusted life years (DALY), which are not presented in dollar units. All other rows in the above framework are presented in dollar units. This review
focused on articles that went beyond health gains to include at least one of the economic benefits in the rows below.
Source: Adapted from Barnighausen et al. [8].

pneumococcal disease each had between seven and nine articles individuals [35,52,64,65,71,74,87,106,108]. Table 1 displays the
that examined their economic benefits. main findings from the 44 cost-effectiveness/cost-utility studies
where all results are presented in cost per DALY averted in 2010
3.1. Cost-effectiveness and cost-benefit US dollars.
We also looked at cost-benefit analysis studies that reported
Our search identified 81 cost-effectiveness/cost-utility or results with a benefit cost ratio or net benefit. Of the 11 cost-benefit
cost-benefit articles. Among these, 74 were cost-effectiveness/cost- studies identified, eight (73%) reported a net benefit suggesting that
utility analyses, of which 44 presented the incremental the benefits outweighed the costs [14,22,44,85,104,110,115,116].
cost-effectiveness ratios in units of cost per disability- Discounting rates were consistent among the majority of cost-
adjusted life year (DALY) averted. 10 articles reported effectiveness/cost-utility and cost-benefit articles, where 70 out
cost-effectiveness ratios in units of cost per quality-adjusted of 81 articles (86%) discounted at 3%. A few studies applied
life year (QALY) gained [10,12,31,47,48,60,61,94,107,117]. 2% [104], 6% [41,106] or 10% discounting [85] or did not need
There were 11 articles carrying out cost-benefit analysis, to discount a 1-year analysis [115]. The discounting rate was
4 of which were also cost-effectiveness/cost-utility studies unclear in some papers. In terms of costs captured by these
[14,22,27,44,80,85,97,104,110,115,116]. studies, all of them (100%) modeled procurement costs (e.g.
Although each article analyzed distinct vaccines for different costs for vaccines, syringes, supplies and equipment). However,
countries using varying assumptions on costs and effectiveness, delivery costs (e.g. costs for personnel, training, surveillance,
21 of the 74 cost-effectiveness/cost-utility articles (28%) concluded monitoring and evaluation, marketing, social mobilization, trans-
that the vaccines they studied were cost-saving in at least one port) were included in 79% of articles (64 out of 81) and cold
of the base case scenarios. Among the 10 articles with QALY chain costs were only incorporated in 27% of articles (22 out of
results, half found vaccines to be cost-saving in at least one 81).
base case scenario [31,47,60,107,117]. Among the 44 articles with
DALY results, we found that 23 studies (52%) reported a cost 3.2. Willingness to pay
per DALY averted less than or equal to $100 in at least one of
their scenarios. At higher cutoffs, 34 (77%) and 38 (86%) arti- The search identified 13 willingness to pay studies esti-
cles reported results of less than or equal to $500/DALY averted mating the private demand for new and future vaccines
and $1000/DALY averted, respectively. Only nine of the cost- [35,38,58,63,66,68,75,81,92,103,111–113]. The willingness to
effectiveness/cost-utility articles (12%) modeled herd immunity to pay studies found that people were willing to pay $0.85–$5.20 per
capture health gains by the community, including unvaccinated person or $8.45–$50 per household for a cholera or typhoid vaccine
S. Ozawa et al. / Vaccine 31 (2012) 96–108 99

Table 1
Cost per DALY averted results from cost-effectiveness/cost-utility studies.

Vaccine Country/region Primary results converted Vaccine price Doses Efficacy Author, year
to 2010 US dollars per dose

Cholera Bangladesh $2315–$3682/DALY


India $1459–$3450/DALY
$0.60 2 60% Jeuland, 2009 [64]
Indonesia $12,933–$28,482/DALY
Mozambique $1056–$1708/DALY

Hepatitis B Gambia $34–$58/DALY $0.32 3 95% Kim, 2007 [72]


India $58/DALY $0.75 3 95% Prakash, 2003 [86]
Mozambique $23–$29/DALY $0.29
3 95% Griffiths, 2005 [57]
$55–$72/DALY $1.08

Haemophilus Indonesia Cost savingb $0.37


3 95% Broughton, 2007 [25]
influenzae type b $104/DALY $2.23
$44–$124/DALY $3.36
3 NR Gessner, 2008 [51]
$32–$90/DALY $3.79
Kenya $36–$75/DALY $3.65 3 NR Akumu, 2007 [13]
Russia $13,813/DALY $2.50
$27,873/DALY $5.00 4 95% Platonov, 2006 [83]
$55,990/DALY $10.00

HIV Thailand $108–$1308/DALY $0.84


$123–$1350/DALY $1.68 1 30% Ono, 2006 [79]
$393–$2108/DALY $16.80
Countries where <$28/DALY $14.00c NR 60% Berndt, 2007 [19]d
GNI < $1000

HPV Cost saving (10)b


<$152/DALY (49) $2.00
<$304/DALY (61)
GAVI (72)a <$304/DALY (15) 3 100% Goldie, 2008 [54]
$5.00
<$759/DALY (55)
<$759/DALY (16)
$12.25
<$1214/DALY (37)
GAVI (72) <GDP/capita (72) $2.00
3 NR Goldie, 2008 [55]
LAC (33) <$438/DALY (33) $5.00

Japanese encephalitis Cambodia $22–$64/DALY $0.30 1 96% Touch, 2010 [102]


China Cost-savingb $0.60 2–5 50–98% Ding, 2003 [43]

Malaria Tanzania $10–$15/DALY $1.00


$16–$27/DALY $2.00
$31–$49/DALY $4.00
$44–$72/DALY $6.00 3 52% Tediosi, 2006 [100]
$58–$95/DALY $8.00
$72–$118/DALY $10.00
$141–$233/DALY $20.00
Countries where <$25/DALY $5.00 3 60% Berndt, 2007 [19]d
GNI < $1000

Measles Bangladesh SIA $19.2/DALY


Ethiopia SIA $2.5/DALY $0.02 1–2 85–95% Bishai, 2010 [21]d
Uganda SIA $1.5/DALY
Afr-E region $82–$164/DALY
$0.12 1 85% Edejer, 2005 [45]
Sear-D region $240/DALY

Measles eradication Brazil Cost savingb


Colombia Cost savingb $0.02 1–2 85–95% Bishai, 2010 [21]d
Tajikistan Cost savingb

Pneumococcal Brazil $1702–$2111/DALY $15.00


3 97% Vespa, 2009 [108]
$3034–$3473/DALY $26.35
$165/DALY $5.00
$302/DALY $10.00
$576/DALY $20.00
$851/DALY $30.00
$1128/DALY $40.00
$1483/DALY $53.00
Chile $344/DALY $5.00
$632/DALY $10.00
$1207/DALY $20.00
3 97% Constenla, 2008 [33]
$1782/DALY $30.00
$2357/DALY $40.00
$3105/DALY $53.00
Uruguay $365/DALY $5.00
$669/DALY $10.00
$1276/DALY $20.00
$1884/DALY $30.00
$2493/DALY $40.00
$3283/DALY $53.00
100 S. Ozawa et al. / Vaccine 31 (2012) 96–108

Table 1 (Continued)

Vaccine Country/region Primary results converted Vaccine price Doses Efficacy Author, year
to 2010 US dollars per dose

Gambia $717–$1145/DALY $3.50 3 26–41% Kim, 2010 [71]


pneumonia
16–26% menin-
gitis/sepsis
GAVI <5 mortality $286/DALY 7.3% all causes
rate >150/1000
(25) $5.00 3 Sinha, 2007 [96]
GAVI <5 mortality $179/DALY 13.1%
rate 100–149 (20)
GAVI <5 mortality $290/DALY 10.9%
rate 25–99 (23)
GAVI <5 mortality $13,756/DALY 3.2%
rate <25 (4)
GAVI (72) $290/DALY 3–13%
$211–$874/DALY $5.00
$939–$1602/DALY $10.00
$2396–$3058/DALY $20.00
LAC (45) 3 97% Sinha, 2008 [95]
$3852–$4515/DALY $30.00
$5309–$5971/DALY $40.00
$7203–$7865/DALY $53.00

Polio eradication Low income $158–$237/DALY OPV $0.11


Duintjer Tebbens, 2010
countries IPV $1.20 3 NR
[44]
Lower middle $134–$1204/DALY OPV $0.11
income countries IPV $2.09
Upper middle Cost savingb OPV $0.11
income countries IPV $3.00

Polio IPV Countries using $2866/DALY $1.00–$9.00 NR NR Khan, 2008 [67]


OPV (148)
South Africa $92,792–$263,593/DALY $1.00 2–4 doses
$240,293–$346,394/DALY $2.00 3–4 doses
$281,757/DALY $6.00 3 doses
NR Griffiths, 2006 [56]
$387,858/DALY $8.00 3 $6 doses + 1
$2 dose
$792,201/DALY $10.00 3 doses
$898,302/DALY $12.00 3 $10 doses + 1
$2 dose

Rotavirus Brazil $854/DALY $5.00


2 85% Constenla, 2008 [34]
$1611/DALY $7.00–$8.00
Colombia $1403/DALY 2 85%
$7.50 De la Hoz, 2010[40]
$2944/DALY 3 95%
Egypt $646/DALY $9.16 2 65% Ortega, 2009 [80]
GAVI AMR (5) $32/DALY
GAVI EUR (8) $56/DALY
GAVI AFR (31) $18/DALY
GAVI EMR (5) $92/DALY $1.25
GAVI SEAR (8) $35/DALY
GAVI WPR (7) $38/DALY
GAVI (64) $27/DALY
2 78–85% Atherly, 2009 [16]
GAVI AMR (5) $353/DALY
GAVI EUR (8) $269/DALY
GAVI AFR (31) $99/DALY
GAVI EMR (5) $584/DALY $$7.00
GAVI SEAR (8) $185/DALY
GAVI WPR (7) $275/DALY
GAVI (64) $152/DALY
GAVI (72) Cost saving (10)b
<$152/DALY (60) $1.50
<$304/DALY (65)
3 72–85% Kim, 2010 [71]
<$152/DALY (23)
<$304/DALY (47) $5.00
$/DALY < GDP/capita (68)
Indonesia $146/DALY $7.00 2 70–84% Wilopo, 2009 [114]
Kenya $33/DALY $1.50 2 78–85% Tate, 2009 [99]
Kyrgyzstan Cost savingb $0.15
Cost savingb $0.30
Cost savingb $0.50
Cost saving – $18/DALY $1.00
2 63–85% Flem, 2009 [50]
$20–$44/DALY $1.50
$72–$95/DALY $2.50
$123–$147/DALY $3.50
$200–$223/DALY $5.00
S. Ozawa et al. / Vaccine 31 (2012) 96–108 101

Table 1 (Continued)

Vaccine Country/region Primary results converted Vaccine price Doses Efficacy Author, year
to 2010 US dollars per dose

Low income $36/DALY $1.00


countries in Asia
$197/DALY $5.00
$397/DALY $10.00
$796/DALY $20.00
$1195/DALY $30.00
Middle income $22/DALY $1.00
countries in Asia 2 75–93% Podewils, 2005 [84]
$296/DALY $5.00
$648/DALY $10.00
$1323/DALY $20.00
$2007/DALY $30.00
High income Cost savingb $1.00
countries in Asia
Cost savingb $5.00
$1863/DALY $10.00
$9624/DALY $20.00
$17,385/DALY $30.00
Low income $23/DALY $1.00
countries
$46/DALY $2.00
$68/DALY $3.00
$113/DALY $5.00
$169/DALY $7.50
Lower middle $36/DALY $1.00
income countries 2 78–85% Rheingans, 2009 [89]
$116/DALY $2.00
$195/DALY $3.00
$353/DALY $5.00
$550/DALY $7.50
Upper middle Cost savingb $1.00
income countries
Cost savingb $2.00
$133/DALY $3.00
$398/DALY $5.00
$730/DALY $7.50
Argentina $3990/DALY $8.00
$7126/DALY $12.00
$10,263/DALY $16.00
Brazil $1783/DALY $8.00
$2996/DALY $12.00
$4206/DALY $16.00
Chile $7821/DALY $8.00
$18,783/DALY $12.00
$29,746/DALY $16.00
Dominican $520/DALY $8.00
Republic $804/DALY $12.00
$1090/DALY $16.00
2 85% Rheingans, 2007 [90]
Honduras $242/DALY $8.00
$404/DALY $12.00
$566/DALY $16.00
Mexico $1425/DALY $8.00
$2390/DALY $12.00
$3355/DALY $16.00
Panama $854/DALY $8.00
$1661/DALY $12.00
$2467/DALY $16.00
Venezuela $1810/DALY $8.00
$3144/DALY $12.00
$4478/DALY $16.00
Malawi $5/DALY $0.15
2 50% Berry, 2010 [20]
$82/DALY $5.50
Mexico $1136/DALY $8.00 2 78–85% Constenla, 2009 [32]
Peru $758–$810/DALY $7.50 minus 5% 2 65–85% Clark, 2009 [30]
annually
Thailand $218–$893/DALY $6.20–$10.50 Chotivitayatarakorn,
2 85–90%
$435/DALY $7.00 2010 [29]
Uzbekistan $109/DALY $1.00
$279/DALY $2.50
2 93% Isakbaeva, 2007 [62]
$565/DALY $5.00
102 S. Ozawa et al. / Vaccine 31 (2012) 96–108

Table 1 (Continued)

Vaccine Country/region Primary results converted Vaccine price Doses Efficacy Author, year
to 2010 US dollars per dose

$1136/DALY $10.00
Vietnam Cost savingb $0.50
$61/DALY $2.50
$139/DALY $5.00 2 78–93% Fischer, 2005 [49]
$216/DALY $7.50
$293/DALY $10.00
$153/DALY $1.00
$825–$841/DALY $5.00
2 41–77% Kim, 2009 [70]
$1154/DALY $7.00
$1651/DALY $10.00

Tuberculosis Countries where $51/DALY $13.00c NR 60% Berndt, 2007 [19]d


GNI < $1000

Typhoid India $179–$579/DALY


Indonesia $639–$1494/DALY
$0.57 1 65% Cook, 2008 [36]
Pakistan $233–$256/DALY
Vietnam $4692–$4863/DALY

Notations, in alphabetical order: Afr-E, countries in the WHO Africa region with high child mortality and very high adult mortality; AFR, countries in the WHO Africa region;
AMR, countries in the WHO Americas region; DALY, disability-adjusted life year; EMR, countries in the WHO Eastern Mediterranean region; EUR, countries in the WHO
Europe region; GAVI, GAVI Alliance eligible countries; GNI, gross national income; IPV, inactivated polio vaccine; LAC, Latin American countries; NR, not reported; OPV,
oral polio vaccine; SEAR, countries in the WHO South-East Asia region; Sear-D, countries in the WHO South-East Asia region with high child and high adult mortality; SIA,
supplemental immunization activities; WPR, countries in the WHO Western Pacific region.
a
Numbers in parenthesis denote the number of countries the article analyzed.
b
Cost-saving indicates that using the vaccine as described results in net savings to the health system or society.
c
Price per person immunized.
d
Paper sited multiple times in the table under different diseases.

Fig. 2. Flow chart for study selection. Key search terms: Vaccines [vaccination, immunization, immunize]; Economics [efficiency, organizational, health expenditures, costs and
cost analysis, cost–benefit analysis, cost of illness, models, economic, health care costs, economic development, economics/pharmaceutical, economics/medical, catastrophic
illness, trade, gross national product, gross domestic product, household consumption, health expenditure, direct expenditure, indirect expenditure, commerce, personal
expenditure, cost analysis, productivity, employment, disability adjusted life year, quality adjusted life year, life year saved, opportunity cost, out of pocket, cost saving,
benefit]; Developing country [developing countries, less developed countries, third world countries, under developed countries poor countries, less developed nations, third
world nations, under developed nations, developing nations, poor nations, poor economies, third world economies, developing economies, under developed economies,
less developed economies, low-income countries, low- and middle-income countries, middle-income countries, low-income nations, low- and middle-income nations,
middle-income nations].
S. Ozawa et al. / Vaccine 31 (2012) 96–108 103

Table 2
Studies of willingness to pay for vaccines.

Vaccine/s Country Primary results Vaccine effectiveness Methodologya Currency Author, year

Cholera Bangladesh $1.05–$2.40/person 50% effective for 3 Dichotomous choice 2008 US$ Islam, 2008 [63]
years
$9.50/household
(5.8)b
Mozambique $8.45/household “Excellent” Dichotomous 2005 US$ Lucas, 2007
(6) effectiveness in 1st choice, [75]
year. “Diminishing” Payment card
effectiveness for next 2
years.
$0.85/person Unknown at time of Dichotomous 2005 US$ Jeuland, 2010
study choice, [66]
Payment card
Vietnam $40/household 50% effective for 3 Dichotomous choice 2003 US$ Kim, 2008 [68]
(5.4) years
$40/household 70% for 3 years
(5.4)
$46/household 70% for 20 years
(5.4)
$50/household 99% for 20 years
(5.4)

Cholera and typhoid India $15–$27/household Cholera 50% effective Dichotomous choice, 2004 US$ Whittington, 2009
(5) for 3 years Payment card [113]
$14–$23/household Typhoid 70% effective
(5) for 3 years

Typhoid India $2.2–$5.2/person 65% effective for 3 Dichotomous 2007 US$ Cook, 2009 [35]
years choice

Pneumococcal Bangladesh $2.38–$18.01/person 16% reduction in Open-ended, 2008 US$ Heinzen, 2008
overall child mortality Dichotomous [58]
choice,
Bidding,
Payment card

Malaria Burkina Faso $1.91–$2.80/person Not reported Bidding 2001 US$c Sauerborn,
2005 [92]
Ethiopia $36/household 100% effective for 1 Dichotomous 1997 US$ Cropper, 2004
(5) year choice [38]
Nigeria $6.77/person 75% effective for 3 Payment card 2010 US$ Udezi, 2010 [103]
years with side effect
of slight fever
$6.70/person 85% effective for 6
years, side effect of
severe headaches/fever
$5.06/person 95% effective for 12
years, 10% probability
of leukemia death

Dengue Philippines $32.3/person 1 year efficacy Dichotomous 2006 US$ Palanca-Tan,


choice 2008 [81]
$68.6/person 10 year efficacy

HIV Thailand $220/person, 50% effective for 10 Dichotomous choice 2000 US$ Whittington, 2008
$610/household years [112]
(varied)
$242/person, 95% effective for 10
$671/household years
(varied)
Mexico $669/person 100% effective over Payment card 1999 US$ Whittington,
lifetime 2002 [111]
a
Methodologies used to elicit willingness to pay include: open-ended questions, dichotomous choice (yes/no), bidding, and use of payment card. See article by Heinzen
[58] for detailed descriptions.
b
Numbers in parentheses denote average numbers of people in households.
c
US$ converted from CFAfr (1 US$ = 750 Cafr).

[35,63,66,68,75,113]. For a malaria vaccine, the results ranged 3.3. Use of primary data
from $1.91 to $6.77 per person or $36 per household [38,92,103].
For pneumococcal and dengue vaccines, people were willing 29 of the 108 studies (27%) collected primary data for all of the
to pay $2.38–$18.01 and $32.3–$68.6 per person, respectively benefits included in their analysis, while 48 articles (44%) only used
[58,81]. The results were highest for a HIV vaccine, where people’s secondary data to model the benefits. 31 articles (29%) used a mix
willingness-to-pay ranged from $220 to $669 per person or $610 of primary and secondary data in analyzing the benefits. Primary
to $671 per household [111,112]. These results are shown in data were used in 46% of the cost-effectiveness/cost-utility articles,
Table 2. 55% of cost-benefit studies and 56% overall.
104 S. Ozawa et al. / Vaccine 31 (2012) 96–108

Narrow Broad
Perspecve Perspecve
100
90
80

No. of Arcles
70
60
50
40 Legend (Data source):
30
20 Secondary data
10
0 Both

cost savings

Outbreak prevenon
producvity gains

producvity gains

producvity gains
Value of stascal life
Health care

Outcome-related

Behavior-related
Primary data

Willingness to pay &


Care-related

savings
Fig. 3. Type of economic benefit by data source.

Fig. 3 shows the number of articles that used only primary data, broad monetary benefits that result from a reduction of mortal-
secondary data or a mixed approach by type of economic benefit we ity [35,37,65], including one study that presented both value of
outlined in the framework. We find that primary data or a mixed statistical life and willingness to pay results [37].
approach were used in 49% of articles that analyzed health care Among articles that captured outcome-related productivity
cost savings compared with 55% in care-related productivity gains. gains were those that focused on increased earning capacity due
While 12 out of 13 willingness to pay studies gathered primary data to improved cognition and physical strength [23,24], as well
[38,58,63,66,68,75,81,92,103,111–113], all three values of statisti- as school enrollment, attendance and attainment [93]. Other
cal life analyses used secondary sources [35,37,65]. Three out of outcome-related productivity articles measured the effect of HIV
five articles on outcome-related productivity gains used primary mortality on a country’s GDP loss [78], and examined the impact
sources [18,23,93]. One out of two behavior-related productivity of immunization on poverty reduction [18]. There were two arti-
article collected primary data [77], while two out of three articles cles that presented behavior-related productivity gains, which
that examined outbreak prevention savings used primary sources looked at the epidemiologic transition or the increase in life
[15,82]. expectancy that result from the introduction of vaccines [24,77].
Three articles captured the benefit of saving costs of outbreak
3.4. Narrow economic benefits investigations or comparing the benefits of preventative vaccina-
tion with reactive vaccination after an outbreak [15,67,82]. Table 3
Out of the 108 articles, 93 articles (86%) reported some narrow highlights some of these broad benefits identified from the litera-
economic benefits of vaccines, where 84 articles (78%) reported ture.
only the narrow benefits. 91 articles (84%) quantified health care
cost savings, while 47 articles (44%) reported care-related produc- 4. Discussion
tivity gains.
Many articles that examined treatment costs pre- This review documents the available evidence showing that vac-
sented primary data on health care cost savings for cination in low- and middle-income countries brings economic
inpatient and outpatient services [Examples include: benefits beyond just health gains. The majority of studies illus-
17,26–28,46,48,59,78,93,102,110,115,116]. Some articles used trate that vaccines are cost-effective at less than $1000 per DALY
surveys to measure vaccine cost savings specific to medications averted, and many less than $100 per DALY averted. This suggests
and diagnostics [15,99]. A few articles measured the transportation to policy makers that vaccines tend to be an efficient investment.
and lodging cost savings for caregivers and patients due to vac- Just as importantly, this review highlights key gaps in the avail-
cines [25,35,36,48,50,64]. Other articles bundled these cost savings able literature that need additional research, especially in the area
to households by measuring out-of-pocket treatment savings of fully measuring the broader economic benefits of vaccination in
[17,26,30,32,36,50,57,62,78,91,93,94,102,106,110,115]. Where the developing world.
primary data were not available, the medication, diagnostics, Our review illustrates that, while more than 70 papers eval-
transport and lodging costs were modeled according to a specified uate the cost-effectiveness of vaccination, many take a narrow
percentage of total treatment costs [29,89]. A number of studies view without capturing societal benefits such as herd immunity.
gathered primary data on care-related productivity gains, such as Only a small fraction of papers we identified quantified the broad
vaccine’s ability to avert caretaker lost wages [25,28]. economic benefit of vaccinations such as increased GDP, value
of statistical life, and the economic implications of extended life
3.5. Broad economic benefits expectancy and reduced disease outbreaks. These benefits can be
significant as illustrated by a recent article from Ozawa et al., where
Less than a quarter of the articles (24 articles, 22%) quantified authors found that $231 billion (uncertainty range: $116–614 bil-
broad level benefit of vaccines. 15 articles presented willingness to lion) in value of statistical lives could be saved by six childhood
pay and/or value of statistical life results for vaccines, five articles vaccines in 72 of the world’s poorest countries over 10 years [118].
captured outcome-related productivity gains [18,23,24,78,93], two There are other broader economic benefits that have received
articles studied behavior-related productivity gains [24,77], and little attention in the literature. For example, the effect of vaccines
three articles considered outbreak prevention savings [15,67,82]. on long-term morbidity-related productivity gains and employ-
Three studies used the value of a statistical life approach to capture ment in society has not been studied. No articles have linked
Table 3
Select studies with broad economic benefits.

Type of benefit Primary results Vaccine Country Author, year Description

Value of statistical life VSL + avoided private COI US$67,000 Cholera India Cook et al., 2009 [35] Total societal benefit includes VSL, public and private cost
Total societal benefit US$672,000 of illness avoided, private benefits to the vaccinated and
value of mortality risk reduction to the unvaccinated
Value of statistical life VSL + avoided public and private COI minus Typhoid India Cook et al., 2009 [37] Presents VSL plus avoided public and private COI net
costs US$117,204–$277,531 benefits, for school children, all children, and adults
[Range: $55,513–$835,950]
Value of statistical life Mortality related benefits US$0.03–$0.75 per Cholera LMIC Jeuland et al., 2009 [65] Presents mortality related benefits for community and
household-month school-based vaccination
Cognitive development Mean test score difference for vaccinated vs. DTP, polio, TB, Philippines Bloom et al., 2010 [23] Presents the effect of vaccination on child test scores in
control groups: verbal reasoning test measles verbal reasoning, math and language
0.43–0.55; math test 0.42–0.63; language test
0.42–0.57. Increased cognitive ability linked to
higher productivity and earnings as an adult
School days missed 1,709,207–1,822,335 lost school days. Influenza Thailand Simmerman et al., 2006 [93] Includes absenteeism due to both outpatient and inpatient

S. Ozawa et al. / Vaccine 31 (2012) 96–108


US$23.4–62.9 million in economic loss, lost visits
productivity accounts for 56% of costs
Poverty reduction, health equity Reduction in childhood mortality hazard ratios BCG, polio, DPT, Ghana Bawah et al., 2009 [18] Presents change in childhood mortality hazard ratios by
by 0.14–0.18 [range 0.13–0.20]. Impact of measles wealth quintile and by immunization status (none, partial,
immunization is greater among poor, showing full)
poverty alleviation effects on child survival
Future productivity Increased annual earnings per vaccinated child Hib, hepatitis B, GAVI Bloom et al., 2005 [24]a Presents increased earnings for vaccinated cohort and IRR
$4.61–$14.10. Internal rate of return (IRR) yellow fever, for years 2005–2020 due to the expanded GAVI
12.4%–18.0%. pneumococcal, immunization program
rotavirus,
meningococcal
GDP loss GDP loss per year Intl$3,035,000,000 HIV Brazil Novaes et al., 2002 [78] Presents economic loss per year from premature AIDS
death in Brazil based on GDP per working age population
a
Life expectancy Increased life expectancy per year 0.58–1.78. Hib, hepatitis B, GAVI Bloom et al., 2005 [24] Presents increases in life expectancy, due to the expanded
yellow fever, GAVI immunization program
pneumococcal,
rotavirus,
meningococcal
Life expectancy and Life expectancy of 59.4 [range 57.3–61.5] Polio, measles, DTP, Ghana Meij et al., 2009 [77] Authors hypothesize that the introduction of mass
epidemiologic transition compared to 47 for a reference population, BCG vaccination programs may be an important driver of the
higher than predicted with regional GDP of improved life expectancy
US$100
Outbreak prevention $24,000 total or $0.20 per habitant in savings; Meningococcal Senegal Parent du Chatelet et al., Benefits of performing preventative vaccination vs.
$59 per case with preventive vaccination vs. 2001 [82] outbreak reactive vaccination
$133 per case with reactive vaccination
Outbreak investigation $2710 in costs per outbreak investigation Influenza Thailand Apisarnthanarak et al., 2008 Benefit of saving costs of outbreak investigations
compared to $256 for cost of vaccination [15]
Outbreak containment Outbreak prevention savings per year with Polio 148 countries using Khan, 2008 [67] Benefit of preventing polio outbreaks by introducing
OPV US$163,000,000 oral polio vaccine inactivated polio vaccine (IPV) in countries using OPV,
(OPV) annualized over a 10 year horizon
a
Paper sited multiple times in the table under different benefits.

105
106 S. Ozawa et al. / Vaccine 31 (2012) 96–108

vaccines with other broad benefits such as economic implications studies should also consider prioritizing the evidence and identify-
of demographic changes and investment in human capital, which ing the most appropriate study designs to examine these benefits.
can accelerate development. While one study examined the effect Further development of these types of measurements would allow
of vaccines on poverty reduction [18], no study has focused on country decision makers and donors to look at the wider and long-
the effect of vaccines in providing financial protection to house- term societal level return on investment that could be expected
holds from threats such as catastrophic health expenditure due from investing in vaccines.
to chronic illness and/or long-term disability. Identifying the most
appropriate study designs to examine these benefits, assessing the
value of additional information, and prioritizing the evidence based Acknowledgements
on rankings by decision-makers are all valuable areas for future
studies. We thank Rohan Deogaonkar, Raymond Hutubessy and Mark Jit
In addition to weak areas of evidence, a further gap was identi- for their valuable comments. This study was performed with finan-
fied related to the type of data used for analyses. Currently, much cial support from the Bill & Melinda Gates Foundation. The views
of the benefits are modeled using secondary data rather than mea- expressed herein are those of the authors and do not necessarily
sured as primary data. While some outcomes are easier to measure reflect the official policy or position of the Bill & Melinda Gates
than others, the large representation of modeled rather than mea- Foundation.
sured data signifies a weak evidence base. Future studies should
consider collecting primary data where broad assumptions are cur-
References
rently made or where secondary data from other countries are
currently applied. [1] John TJ, Samuel R. Herd immunity and herd effect: new insights and defini-
By focusing solely on the narrow benefits of vaccines, decision tions. Eur J Epidemiol 2000;16(7):601–6.
makers may be under-estimating the level of benefits and thereby [2] Evans D, Edejer T, Chisholm D, Stanciole A. WHO guide to identifying the
economic consequences of disease and injury. Geneva: Department of Health
undervaluing vaccines [3]. For example, Stack et al. found that of the Systems Financing, Health Systems and Services, World Health Organization;
potential $151 billion (uncertainty range: $130–175 billion) in eco- 2009.
nomic benefits that vaccines can bring to low- and middle-income [3] Ehreth J. The value of vaccination: a global perspective. Vaccine
2003;21(27–30):4105–17.
countries during the Decade of Vaccines, 94% are broad benefits
[4] Bloom D, Cannning D, Jamison D. Health, wealth and welfare. Finance Dev
[119]. By measuring and disseminating broader economic benefits, 2004;March:10–5.
it will be possible to more accurately evaluate whether vaccines [5] Shearley AE. The societal value of vaccination in developing countries. Vaccine
1999;17(October (Suppl. 3)):S109–12.
are a valuable investment. Such evidence is especially important
[6] Elias C. The Decade of Vaccines Collaboration: developing a global
in specific scenarios where vaccines may not be as cost-effective roadmap for saving lives. Expert Rev Vaccines 2011;10(November (11)):
without taking herd immunity benefits into consideration [64] or 1493–5.
appear too costly to eradicate a disease [56]. [7] Barnighausen T, Bloom DE, Canning D, Friedman A, Levine OS, O’Brien J,
et al. Rethinking the benefits and costs of childhood vaccination: the exam-
This work is important because of its emphasis on low- and ple of the Haemophilus influenzae type b vaccine. Vaccine 2011;29(March
middle-income countries. Historically, it has taken 15–20 years (13)):2371–80.
after first licensure in rich countries for new vaccines to reach [8] Barnighausen T, Bloom DE, Canning D, O’Brien J. Accounting for the full ben-
efits of childhood vaccination in South Africa. S Afr Med J 2008;98(November
developing countries where they are often needed the most. With (11)), 842, 4–6.
greater economic evidence, policy makers in developing countries [9] Moher D, Liberati A, Tetzlaff J, Altman DG. Preferred reporting items for
could incorporate better information in evidence-based decision systematic reviews and meta-analyses: the PRISMA statement. PLoS Med
2009;6(July (7)):e1000097.
making to introduce and expand vaccines in their health systems. [10] Aballea S, Chancellor J, Martin M, Wutzler P, Carrat F, Gasparini R, et al. The
It is essential to note that our results are limited by our search cost-effectiveness of influenza vaccination for people aged 50–64 years: an
strategies including the databases searched, keywords used, inclu- international model. Value Health 2007;10(March–April (2)):98–116.
[11] Acharya A, Diaz-Ortega JL, Tambini G, de Quadros C, Arita I. Cost-effectiveness
sion/exclusion criteria adopted and the time period (2000–2010)
of measles elimination in Latin America and the Caribbean: a prospective
of the search. Our search focused primarily on the English pub- analysis. Vaccine 2002;20(27–28):3332–41.
lished literature and does not include gray literature which is [12] Aggarwal R. Assessment of cost-effectiveness of universal hepatitis B immu-
nization in a low-income country with intermediate endemicity using a
not-peer-reviewed and varies significantly in quality. Even among
Markov model. J Hepatol 2003;38(2):215–22.
the published literature, the effect size of the economic benefits [13] Akumu AO, English M, Scott JA, Griffiths UK. Economic evaluation of delivering
may differ according to the methodological quality of the stud- Haemophilus influenzae type b vaccine in routine immunization services in
ies which we have not adjusted for in the results. Publication bias Kenya. Bull World Health Organ 2007;85(July (7)):511–8.
[14] Amirfar S, Hollenberg JP, Abdool Karim SS. Modeling the impact of a partially
toward more cost-effective results may have also affected our find- effective HIV vaccine on HIV infection and death among women and infants
ings. Since we focused on the economic benefits rather than costs, in South Africa. J Acquir Immune Defic Syndr 2006;43(October (2)):219–25.
our search was restricted to articles with some discussion of eco- [15] Apisarnthanarak A, Puthavathana P, Kitphati R, Auewarakul P, Mundy
L. Outbreaks of Influenza A among nonvaccinated healthcare workers:
nomic benefits. Despite these limitations, however, we believe we implications for resource-limited settings. Infect Control Hosp Epidemiol
have identified and synthesized articles in a systematic manner. 2008;29(8):777–80.
[16] Atherly D, Dreibelbis R, Parashar Umesh D, Levin C, Wecker J, Rheingans
Richard D. Rotavirus vaccination: cost effectiveness and impact on child mor-
tality in developing countries. J Infect Dis 2009;200(s1):S28–38.
5. Conclusions [17] Bahl R, Sinha A, Poulos C, Whittington D, Sazawal S, Kumar R, et al. Costs of
illness due to typhoid fever in an Indian urban slum community: implications
for vaccination policy. J Health Popul Nutr 2004;22(September (3)):304–10.
This review identified more than 100 papers that illustrate the
[18] Bawah AA, Phillips JF, Adjuik M, Vaughan-Smith M, Macleod B, Binka FN.
cost-effectiveness and economic benefits of vaccination in low- and The impact of immunization on the association between poverty and child
middle-income countries. However, it also shows that most studies survival: evidence from Kassena-Nankana District of northern Ghana. Scand
J Public Health 2010;38(February (1)):95–103.
take a narrow perspective of the economic benefits of vaccination,
[19] Berndt ER, Glennerster R, Kremer MR, Lee J, Levine R, Weizsäcker G, et al.
and that a number of key gaps in evidence remain unfilled. To bet- Advance market commitments for vaccines against neglected diseases: esti-
ter represent the full economic benefits of vaccines in low- and mating costs and effectiveness. Health Econ 2007;16(5):491–511.
middle-income country settings, the published literature would [20] Berry SA, Johns B, Shih C, Berry AA, Walker DG. The cost-effectiveness of
rotavirus vaccination in Malawi. J Infect Dis 2010;202(Suppl.):S108–15.
greatly benefit from approaches that measure the broad benefits of [21] Bishai D, Johns B, Lefevre A, Nair D. Cost effectiveness of measles eradication.
vaccination on individuals, households, and communities. Future Baltimore: Johns Hopkins Bloomberg School of Public Health; 2010.
S. Ozawa et al. / Vaccine 31 (2012) 96–108 107

[22] Bishai D, Lin MK, Kiyonga CW. Modeling the economic benefits of an AIDS [52] Giglio ND, Cane AD, Micone P, Gentile A. Cost-effectiveness of the CRM-based
vaccine. Vaccine 2001;20(November (3–4)):526–31. 7-valent pneumococcal conjugated vaccine (PCV7) in Argentina. Vaccine
[23] Bloom D, Canning D, Seiguer E. The effect of vaccination on children’s physical 2010;28(March (11)):2302–10.
and cognitive development in the Phillipines. Program on the global demog- [53] Goldie SJ, Kim JJ, Kobus K, Goldhaber-Fiebert JD, Salomon J, O’Shea
raphy of aging. Boston: Harvard School of Public Health; 2010. p. 1–16. MK, et al. Cost-effectiveness of HPV 16,18 vaccination in Brazil. Vaccine
[24] Bloom D, Canning D, Weston M. The value of vaccination. World Econ 2007;25(August (33)):6257–70.
2005;6(3):15–39. [54] Goldie SJ, O’Shea M, Campos NG, Diaz M, Sweet S, Kim S-Y. Health and eco-
[25] Broughton EI. Economic evaluation of Haemophilus influenzae type B nomic outcomes of HPV 16,18 vaccination in 72 GAVI-eligible countries.
vaccination in Indonesia: a cost-effectiveness analysis. J Public Health Vaccine 2008;26(32):4080–93.
2007;29(4):441–8. [55] Goldie SJ, O’Shea M, Diaz M, Kim S-Y. Benefits, cost requirements and
[26] Centenari C, Gurgel RQ, Bohland AK, Oliveira DM, Faragher B, Cuevas LE. cost-effectiveness of the HPV16,18 vaccine for cervical cancer preven-
Rotavirus vaccination in northeast Brazil: a laudable intervention, but can tion in developing countries: policy implications. Reprod Health Matters
it lead to cost-savings? Vaccine 2010;28(June (25)):4162–8. 2008;16(32):86–96.
[27] Chan PW, Abdel-Latif ME. Cost of hospitalization for respiratory syncytial [56] Griffiths UK, Botham L, Schoub BD. The cost-effectiveness of alterna-
virus chest infection and implications for passive immunization strategies tive polio immunization policies in South Africa. Vaccine 2006;24(July
in a developing nation. Acta Paediatr 2003;92(April (4)):481–5. (29–30)):5670–8.
[28] Chandrasena N, Rajindrajith S, Ahmed K, Pathmeswaran A, Nakagomi O. [57] Griffiths UK, Hutton G, Das Dores Pascoal E. The cost-effectiveness of introduc-
Hospital-based study of the severity and economic burden associated with ing hepatitis B vaccine into infant immunization services in Mozambique.
rotavirus diarrhea in Sri Lanka. J Pediatr Infect Dis 2009;4(4):379–86. Health Policy Plan 2005;20(January (1)):50–9.
[29] Chotivitayatarakorn P, Poovorawan Y. Cost-effectiveness of rotavirus vaccina- [58] Heinzen RR, Bridges JF. Comparison of four contingent valuation methods to
tion as part of the national immunization program for Thai children. Southeast estimate the economic value of a pneumococcal vaccine in Bangladesh. Int J
Asian J Trop Med Public Health 2010;41(January (1)):114–25. Technol Assess Health Care 2008;24(Fall (4)):481–7.
[30] Clark AD, Walker DG, Mosqueira NR, Penny ME, Lanata CF, Fox-Rushby [59] Hussain H, Waters H, Omer SB, Khan A, Baig IY, Mistry R, et al. The cost of treat-
J, et al. Cost-effectiveness of rotavirus vaccination in Peru. J Infect Dis ment for child pneumonias and meningitis in the Northern Areas of Pakistan.
2009;200(Suppl. 1):S114–24. Int J Health Plann Manage 2006;21(July–September (3)):38–229.
[31] Colantonio L, Gomez JA, Demarteau N, Standaert B, Pichon-Riviere A, Augus- [60] Hutton DW, So SK, Brandeau ML. Cost-effectiveness of nationwide hepatitis
tovski F. Cost-effectiveness analysis of a cervical cancer vaccine in five Latin B catch-up vaccination among children and adolescents in China. Hepatology
American countries. Vaccine 2009;27(September (40)):5519–29. 2010;51(February (2)):405–14.
[32] Constenla D, Velázquez FR, Rheingans RD, Antil L, Cervantes Y. Economic [61] Insinga RP, Dasbach EJ, Elbasha EH, Puig A, Reynales-Shigematsu LM.
impact of a rotavirus vaccination program in Mexico. Rev Panam Salud Pública Cost-effectiveness of quadrivalent human papillomavirus (HPV) vaccina-
2009;25(6):481–90. tion in Mexico: a transmission dynamic model-based evaluation. Vaccine
[33] Constenla DO. Economic impact of pneumococcal conjugate vaccination 2007;26(December (1)):128–39.
in Brazil, Chile, and Uruguay. Rev Panam Salud Pública 2008;24(2): [62] Isakbaeva ET, Musabaev E, Antil L, Rheingans R, Juraev R, Glass RI, et al.
101–12. Rotavirus disease in Uzbekistan: cost-effectiveness of a new vaccine. Vaccine
[34] Constenla DO, Linhares AC, Rheingans RD, Antil LR, Waldman EA, da Silva 2007;25(January (2)):373–80.
LJ. Economic impact of a rotavirus vaccine in Brazil. J Health Popul Nutr [63] Islam Z, Maskery B, Nyamete A, Horowitz MS, Yunus M, Whittington D. Pri-
2008;26(4):388–96. vate demand for cholera vaccines in rural Matlab, Bangladesh. Health Policy
[35] Cook J, Jeuland M, Maskery B, Lauria D, Sur D, Clemens J, et al. Using private 2008;85(February (2)):184–95.
demand studies to calculate socially optimal vaccine subsidies in developing [64] Jeuland M, Cook J, Poulos C, Clemens J, Whittington D. Cost-effectiveness
countries. J Policy Anal Manage 2009;28(1):6–28. of new-generation oral cholera vaccines: a multisite analysis. Value Health
[36] Cook J, Jeuland M, Whittington D, Poulos C, Clemens J, Sur D, et al. The cost- 2009;12(6):899–908.
effectiveness of typhoid Vi vaccination programs: calculations for four urban [65] Jeuland M, Whittington D. Cost–benefit comparisons of investments
sites in four Asian countries. Vaccine 2008;26(November (50)):6305–16. in improved water supply and cholera vaccination programs. Vaccine
[37] Cook J, Sur D, Clemens J, Whittington D. Evaluating investments in 2009;27(23):3109–20.
typhoid vaccines in two slums in Kolkata, India. J Health Popul Nutr [66] Jeuland M, Lucas M, Clemens J, Whittington D. Estimating the private benefits
2009;27(December (6)):711–24. of vaccination against cholera in Beira, Mozambique: a travel cost approach.
[38] Cropper M, Haile M, Lampietti J, Poulos C, Whittington D. The demand for a J Dev Econ 2010;91:310–22.
malaria vaccine: evidence from Ethiopia. J Dev Econ 2004;75:303–18. [67] Khan MM. Economics of polio vaccination in the post-eradication era: should
[39] Dayan GH, Cairns L, Sangrujee N, Mtonga A, Nguyen V, Strebel P. Cost- OPV-using countries adopt IPV? Vaccine 2008;26(16):2034–40.
effectiveness of three different vaccination strategies against measles in [68] Kim D, Canh do G, Poulos C, Thoa le TK, Cook J, Hoa NT, et al. Private demand for
Zambian children. Vaccine 2004;22(3–4):475–84. cholera vaccines in Hue, Vietnam. Value Health 2008;11(January–February
[40] De la Hoz F, Alvis N, Narváez J, Cediel N, Gamboa O, Velandia M. Potential epi- (1)):28–119.
demiological and economical impact of two rotavirus vaccines in Colombia. [69] Kim JJ, Kobus KE, Diaz M, O’Shea M, Van Minh H, Goldie SJ. Exploring the
Vaccine 2010;28(22):3856–64. cost-effectiveness of HPV vaccination in Vietnam: insights for evidence-
[41] de Soarez PC, Valentim J, Sartori AM, Novaes HM. Cost-effectiveness anal- based cervical cancer prevention policy. Vaccine 2008;26(July (32)):
ysis of routine rotavirus vaccination in Brazil. Rev Panam Salud Publica 4015–24.
2008;23(April (4)):221–30. [70] Kim S-Y, Goldie SJ, Salomon JA. Cost-effectiveness of rotavirus vaccination in
[42] Diaz M, Kim JJ, Albero G, de Sanjosé S, Clifford G, Bosch FX, et al. Health and Vietnam. BMC Public Health 2009;9(1):29.
economic impact of HPV 16 and 18 vaccination and cervical cancer screening [71] Kim S-Y, Lee G, Goldie SJ. Economic evaluation of pneumococcal conjugate
in India. Br J Cancer 2008;99(2):230–8. vaccination in The Gambia. BMC Infect Dis 2010;10:260.
[43] Ding D, Kilgore P, Clemens J, Wei L, Zhi-Yi X. Cost-effectiveness of routine [72] Kim S-Y, Salomon J, Goldie S. Economic evaluation of hepatitis B vaccination
immunization to control Japanese encephalitis in Shanghai, China. Bull World in low-income countries: using cost-effectiveness affordability curves. Bull
Health Organ 2003;81(5):334–42. World Health Organ 2007;85(11):833–42.
[44] Duintjer Tebbens RJ, Pallansch MA, Cochi SL, Wassilak SGF, Linkins J, Sutter [73] Kim S-Y, Sweet S, Slichter D, Goldie SJ. Health and economic impact
RW, et al. Economic analysis of the global polio eradication initiative. Vaccine of rotavirus vaccination in GAVI-eligible countries. BMC Public Health
2010;29(2):43–334. 2010;10:253.
[45] Edejer TTT. Cost effectiveness analysis of strategies for child health in devel- [74] Lopez E, Debbag R, Coudeville L, Baron-Papillon F, Armoni J. The cost-
oping countries. Br Med J 2005;331(7526):1177–80. effectiveness of universal vaccination of children against hepatitis A in
[46] Ehrenkranz P, Lanata CF, Penny ME, Salazar-Lindo E, Glass RI. Rotavirus diar- Argentina: results of a dynamic health-economic analysis. J Gastroenterol
rhea disease burden in Peru: the need for a rotavirus vaccine and its potential 2007;42(February (2)):152–60.
cost savings. Rev Panam Salud Publica 2001;10(October (4)):240–8. [75] Lucas ME, Jeuland M, Deen J, Lazaro N, MacMahon M, Nyamete A, et al. Private
[47] Ellis A, Ruttimann RW, Jacobs RJ, Meyerhoff AS, Innis BL. Cost-effectiveness of demand for cholera vaccines in Beira, Mozambique. Vaccine 2007;25(March
childhood hepatitis A vaccination in Argentina: a second dose is warranted. (14)):2599–609.
Rev Panam Salud Publica 2007;21(June (6)):345–56. [76] Massad E, Coutinho FA, Chaib E, Burattini MN. Cost-effectiveness analysis of
[48] Ezat WP, Aljunid S. Cost-effectiveness of HPV vaccination in the prevention a hypothetical hepatitis C vaccine compared to antiviral therapy. Epidemiol
of cervical cancer in Malaysia. Asian Pac J Cancer Prev 2010;11(1):79–90. Infect 2009;137(February (2)):241–9.
[49] Fischer TK, Anh DD, Antil L, Cat NDL, Kilgore PE, Thiem VD, et al. Health care [77] Meij JJ, de Craen AJ, Agana J, Plug D, Westendorp RG. Low-cost interventions
costs of diarrheal disease and estimates of the cost-effectiveness of rotavirus accelerate epidemiological transition in Upper East Ghana. Trans R Soc Trop
vaccination in Vietnam. J Infect Dis 2005;192(10):1720–6. Med Hyg 2009;103(February (2)):173–8.
[50] Flem ET, Latipov R, Nurmatov ZS, Xue Y, Kasymbekova KT, Rheingans RD. Costs [78] Novaes H, Luna E, Goldbaum M, Kilsztajn S, Rossbach A, de la Rocha Carval-
of diarrheal disease and the cost-effectiveness of a rotavirus vaccination pro- heiro J. The potential demand for an HIV/AIDS vaccine in Brazil. World Bank
gram in Kyrgyzstan. J Infect Dis 2009;200(November (Suppl. 1)):S195–202. policy research working paper 2940. Washington, DC: The World Bank; 2002.
[51] Gessner BD, Sedyaningsih ER, Griffiths UK, Sutanto A, Linehan M, Mercer p. 1–30.
D, et al. Vaccine-preventable haemophilus influenza type B disease burden [79] Ono S, Kurotaki T, Nakasone T, Honda M, Boon-Long J, Sawanpanyalert P,
and cost-effectiveness of infant vaccination in Indonesia. Pediatr Infect Dis J et al. Cost-effectiveness analysis of antiretroviral drug treatment and HIV-1
2008;27(5):438–43. vaccination in Thailand. Jpn J Infect Dis 2006;59:168–73.
108 S. Ozawa et al. / Vaccine 31 (2012) 96–108

[80] Ortega O, El-Sayed N, Sanders JW, Abd-Rabou Z, Antil L, Bresee J, et al. [100] Tediosi F, Hutton G, Maire N, Smith TA, Ross A, Tanner M. Predicting the
Cost–benefit analysis of a rotavirus immunization program in the Arab cost-effectiveness of introducing a pre-erythrocytic malaria vaccine into
Republic of Egypt. J Infect Dis 2009;200(November (Suppl. 1)):S92–8. the expanded program on immunization in Tanzania. Am J Trop Med Hyg
[81] Palanca-Tan R. The demand for a dengue vaccine: a contingent valuation 2006;75(2 Suppl.):131–43.
survey in Metro Manila. Vaccine 2008;26(February (7)):914–23. [101] Thompson KM, Tebbens RJD. Eradication versus control for poliomyelitis: an
[82] Parent du Châtelet I, Gessner BD, da Silva A. Comparison of cost-effectiveness economic analysis. Lancet 2007;369(9570):1363–71.
of preventive and reactive mass immunization campaigns against meningo- [102] Touch S, Suraratdecha C, Samnang C, Heng S, Gazley L, Huch C, et al. A cost-
coccal meningitis in West Africa: a theoretical modeling analysis. Vaccine effectiveness analysis of Japanese encephalitis vaccine in Cambodia. Vaccine
2001;19(25–26):3420–31. 2010;28(29):4593–9.
[83] Platonov AE, Griffiths UK, Voeykova MV, Platonova OV, Shakhanina IL, [103] Udezi WA, Usifoh CO, Ihimekpen OO. Willingness to pay for three hypothetical
Chistyakova GG, et al. Economic evaluation of Haemophilus influenzae malaria vaccines in Nigeria. Clin Ther 2010;32(August (8)):1533–44.
type b vaccination in Moscow, Russian Federation. Vaccine 2006;24(March [104] Uzicanin A, Zhou F, Eggers R, Webb E, Strebel P. Economic analysis of the
(13)):2367–76. 1996–1997 mass measles immunization campaigns in South Africa. Vaccine
[84] Podewils LJ, Antil L, Hummelman E, Bresee J, Parashar UD, Rheingans R. Pro- 2004;22(September (25–26)):3419–26.
jected cost-effectiveness of rotavirus vaccination for children in Asia. J Infect [105] Valencia-Mendoza A, Bertozzi SM, Gutierrez J-P, Itzler R. Cost-effectiveness of
Dis 2005;192(Suppl. 1):S133–45. introducing a rotavirus vaccine in developing countries: the case of Mexico.
[85] Poulos C, Bahl R, Whittington D, Bhan MK, Clemens JD, Acosta CJ. A BMC Infect Dis 2008;8(1):103.
cost–benefit analysis of typhoid fever immunization programmes in an Indian [106] Valentim J, Sartori AM, de Soarez PC, Amaku M, Azevedo RS, Novaes HM. Cost-
urban slum community. J Health Popul Nutr 2004;22(3):311–21. effectiveness analysis of universal childhood vaccination against varicella in
[86] Prakash C. Crucial factors that influence cost-effectiveness of universal hepati- Brazil. Vaccine 2008;26(November (49)):6281–91.
tis B immunization in India. Int J Technol Assess Health Care 2003;19(Winter [107] Valenzuela MT, Jacobs RJ, Arteaga O, Navarrete MS, Meyerhoff AS, Innis BL.
(1)):28–40. Cost-effectiveness of universal childhood hepatitis A vaccination in Chile.
[87] Quezada A, Baron-Papillon F, Coudeville L, Maggi L. Universal vaccination of Vaccine 2005;23(July (32)):4110–9.
children against hepatitis A in Chile: a cost-effectiveness study. Rev Panam [108] Vespa G, Constenla DO, Pepe C, Safadi MA, Berezin E, de Moraes JC, et al.
Salud Publica 2008;23(May (5)):303–12. Estimating the cost-effectiveness of pneumococcal conjugate vaccination in
[88] Reynales-Shigematsu LM, Rodrigues ER, Lazcano-Ponce E. Cost-effectiveness Brazil. Rev Panam Salud Pública 2009;26(6):518–28.
analysis of a quadrivalent human papilloma virus vaccine in Mexico. Arch [109] Vimolket T, Poovorawan Y. An economic evaluation of universal infant
Med Res 2009;40(6):503–13. vaccination strategies against hepatitis B in Thailand: an analytic decision
[89] Rheingans Richard D, Antil L, Dreibelbis R, Podewils Laura J, Bresee approach to cost-effectiveness. Southeast Asian J Trop Med Public Health
Joseph S, Parashar Umesh D. Economic costs of rotavirus gastroenteritis 2005;36(May (3)):693–9.
and cost effectiveness of vaccination in developing countries. J Infect Dis [110] Wang XY, Riewpaiboon A, von Seidlein L, Chen XB, Kilgore PE, Ma JC, et al.
2009;200(s1):S16–27. Potential cost-effectiveness of a rotavirus immunization program in rural
[90] Rheingans RD, Constenla D, Antil L, Innis BL, Breuer T. Potential cost- China. Clin Infect Dis 2009;49(October (8)):1202–10.
effectiveness of vaccination for rotavirus gastroenteritis in eight Latin [111] Whittington D, Matsui-Santana O, Freiberger JJ, Van Houtven G, Pattanayak S.
American and Caribbean countries. Rev Panam Salud Publica 2007;21(April Private demand for a HIV/AIDS vaccine: evidence from Guadalajara, Mexico.
(4)):205–16. Vaccine 2002;20(June (19–20)):2585–91.
[91] Rose J, Hawthorn RL, Watts B, Singer ME. Public health impact and cost effec- [112] Whittington D, Suraratdecha C, Poulos C, Ainsworth M, Prabhu V,
tiveness of mass vaccination with live attenuated human rotavirus vaccine Tangcharoensathien V. Household demand for preventive HIV/AIDS vac-
(RIX4414) in India: model based analysis. Br Med J 2009;339:b3653. cines in Thailand: do husbands’ and wives’ preferences differ? Value Health
[92] Sauerborn R, Gbangou A, Dong H, Przyborski JM, Lanzer M. Willingness to pay 2008;11(September–October (5)):965–74.
for hypothetical malaria vaccines in rural Burkina Faso. Scand J Public Health [113] Whittington D, Sur D, Cook J, Chatterjee S, Maskery B, Lahiri M, et al. Rethink-
2005;33(2):146–50. ing cholera and typhoid vaccination policies for the poor: private demand in
[93] Simmerman JM, Lertiendumrong J, Dowell SF, Uyeki T, Olsen SJ, Chitta- Kolkata, India. World Dev 2009;37(2):399–409.
ganpitch M, et al. The cost of influenza in Thailand. Vaccine 2006;24(May [114] Wilopo SA, Kilgore P, Kosen S, Soenarto Y, Aminah S, Cahyono A, et al. Eco-
(20)):4417–26. nomic evaluation of a routine rotavirus vaccination programme in Indonesia.
[94] Sinanovic E, Moodley J, Barone MA, Mall S, Cleary S, Harries J. The potential Vaccine 2009;27(November (Suppl. 5)):F67–74.
cost-effectiveness of adding a human papillomavirus vaccine to the cervi- [115] Wongsurakiat P, Lertakyamanee J, Maranetra KN, Jongriratanakul S,
cal cancer screening programme in South Africa. Vaccine 2009;27(October Sangkaew S. Economic evaluation of influenza vaccination in Thai chronic
(44)):6196–202. obstructive pulmonary disease patients. J Med Assoc Thai 2003;86(June
[95] Sinha A, Constenla D, Valencia JE, O’Loughlin R, Gomez E, de la Hoz F, (6)):497–508.
et al. Cost-effectiveness of pneumococcal conjugate vaccination in Latin [116] Zahdi MR, Maluf Jr I, Maluf EM. Hepatitis A: the costs and benefits of the
America and the Caribbean: a regional analysis. Rev Panam Salud Pública disease prevention by vaccine, Parana, Brazil. Braz J Infect Dis 2009;13(August
2008;24(5):304–13. (4)):257–61.
[96] Sinha A, Levine O, Knoll MD, Muhib F, Lieu TA. Cost-effectiveness of pneu- [117] Zhuang GH, Pan XJ, Wang XL. A cost-effectiveness analysis of univer-
mococcal conjugate vaccination in the prevention of child mortality: an sal childhood hepatitis A vaccination in China. Vaccine 2008;26(August
international economic analysis. Lancet 2007;369(9559):389–96. (35)):4608–16.
[97] Soogarun S, Wiwanitkit V. Vaccinating Thai adolescents against hepatitis A: [118] Ozawa S, Stack ML, Bishai DM, Mirelman A, Friberg IK, Niessen L, et al.
is it cost-effective? Southeast Asian J Trop Med Public Health 2002;33(Suppl. During the ‘Decade of Vaccines,’ the lives of 6.4 million children valued
3):8–145. at $231 billion could be saved. Health Aff (Millwood) 2011;30(June (6)):
[98] Taal MW, van Zyl-Smit R. Cost-effectiveness of hepatitis B vaccination in 1010–20.
haemodialysis patients. S Afr Med J 2001;91(April (4)):340–4. [119] Stack ML, Ozawa S, Bishai DM, Mirelman A, Tam Y, Niessen L, et al. Estimated
[99] Tate JE, Rheingans RD, O’Reilly CE, Obonyo B, Burton DC, Tornheim JA, et al. economic benefits during the ‘Decade of Vaccines’ include treatment sav-
Rotavirus disease burden and impact and cost-effectiveness of a rotavirus ings, gains in labor productivity. Health Aff (Millwood) 2011;30(June (6)):
vaccination program in Kenya. J Infect Dis 2009;200(Suppl. 1):S76–84. 1021–8.

You might also like