Tropical Medicine and International Health doi:10.1111/j.1365-3156.2008.02203.

volume 14 no 2 pp 237–246 february 2009

Disability adjusted life years lost to dengue in Brazil

P. M. Luz1, B. Grinsztejn2 and A. P. Galvani1

1 School of Public Health, Yale University, New Haven, CT, USA

2 Instituto de Pesquisa Clı́nica Evandro Chagas, Fundação Oswaldo Cruz, Rio de Janeiro, Brazil

Summary objectives To assess the dengue burden in Brazil, and to compare it over three spatial scales: in the city
of Rio de Janeiro, the state of Rio de Janeiro, and in Brazil overall.
methods We calculated disability adjusted life years (DALYs) lost to dengue per million individuals
annually from 1986 through 2006. To calculate DALYs, we compiled data on the number of dengue
cases by age, clinical syndrome and outcome. We evaluated the sensitivity of our results to multiplication
factors used to adjust for inaccuracies in reporting using a Monte Carlo method.
results From 1986 through 2006, a mean of 56, 47 and 22 DALYs per million individuals annually
were lost to dengue in the city of Rio de Janeiro, in the state of Rio de Janeiro and in Brazil, respectively.
Over 80% of the dengue burden derived from dengue fever cases. The dengue burden was highest at the
city-level with a maximum single-year estimate of 560 DALYs per million individuals for 2002.
conclusions Assessment of dengue burden requires consideration of all clinical syndromes over
multiple years. Our results indicate that the dengue burden is as high as the burden of other major
infectious diseases that afflict the Brazilian population, including malaria. These results may prompt
policy makers to elevate the prioritization of dengue control, and allocate resources needed to curtail the
increasing dengue burden.

keywords Brazil, dengue, disability adjusted life years, disease burden, Rio de Janeiro

ment and the use of oxygen can reduce the case-fatality

Introduction
Dengue is a growing public health concern throughout
much of the tropical world (Gubler 2002; Farrar et al.
2007). In the past decades, the primary vector of dengue,
Aedes aegypti, has expanded its geographical range,
disseminating the risk of disease (Gubler 2002; Guzman &
Kouri 2003). Today, several dengue viruses are endemic in
over 100 countries, also increasing the frequency and
severity of epidemics (Gubler 2002; Guzman & Kouri
2002).
Dengue viruses include four distinct serotypes that
produce a spectrum of clinical syndromes. The most
common clinical syndrome is dengue fever (DF), which is
generally characterized by fever, severe headaches, and
muscle and joint pains. Dengue hemorrhagic fever (DHF) is
a less common syndrome that occurs in <5% of cases.
However, DHF is a more severe clinical syndrome char-
acterized by excessive capillary permeability. The plasma
leakage that occurs with DHF can lead to circulatory
failure that causes dengue shock syndrome. The case-
fatality ratio for patients with this shock syndrome can
reach 40% (Meltzer et al. 1998), but early hospitalization
and treatment with liquid infusions, electrolyte manage-
ratio to less than 1% (Gubler & Meltzer 1999).
Quantification of disease burden allows a comparison of
disease burdens within and between countries, which is
essential for informed decisions regarding resource alloca-
tions. Disease burdens also serve as a baseline for analysis
of the impact of interventions, including cost-effectiveness
analysis. Evaluations of disease burdens are fundamental to
decisions about how much investment should be made to
control different diseases. Recently, the Dengue Scientific
Working Group recommended that the evaluation of
dengue burden is a priority in the global dengue research
agenda (Farrar et al. 2007). Despite the global expansion
and clinical importance of dengue, few studies have
assessed the burden of this disease (Suaya et al. 2006;
Torres & Castro 2007). The dengue burden within Latin
America has been neglected (Torres & Castro 2007), with
the exception of two studies (Meltzer et al. 1998; Gubler
& Meltzer 1999). In Latin America, Brazil accounts for
approximately 70% of the dengue cases (Siqueira et al.
2005), highlighting the need for a dengue burden analysis
in Brazil.
In this study, we used the non-monetary index Disability
Adjusted Life Years [(DALYs) Murray 1994; Murray &

ª 2009 Blackwell Publishing Ltd 237

Tropical Medicine and International Health
P. M. Luz et al. DALYs lost to dengue in Brazil
Lopez 1994)] to measure the dengue burden in Brazil.
DALYs accounts for the mortality, or the time lost due to
premature death, and the morbidity, or the time lived with
disability, imposed by a disease or health condition (Murray
1994; Murray & Lopez 1994). We calculated DALYs lost to
dengue in the city and the state of Rio de Janeiro, as well as in
Brazil overall, from 1986 through 2006.
Methods
Data
The mandatory reporting of dengue cases in Brazil was
instituted two decades ago (Siqueira et al. 2005). A
reported dengue case must fulfil a clinical classification or
be confirmed through laboratory tests. The clinical classi-
fication of a dengue case, given by the Surveillance
Secretariat of the Ministry of Health (http://portal.
saude.gov.br/portal/saude/area.cfm?id_area=974), includes
a fever lasting at least 7 days, as well as any two of the
following symptoms: migraine, retro-orbital pain, myal-
gias, arthralgias, prostration or a rash, with or without
hemorrhaging. Laboratory confirmation includes virus
isolation and ⁄ or antibody detection through IgM enzyme-
linked immunosorbent assay.
To calculate DALYs, we compiled data from the Health
Department of the City of Rio de Janeiro (http://www.
saude.rio.rj.gov.br/), the Health Department of the State of
Rio de Janeiro (http://www.saude.rj.gov.br/), and the
Information System for Disease Reporting (http://
dtr2004.saude.gov.br/sinanweb/novo/). We searched for
data on reported cases by age, clinical syndrome (DF, DHF),
and outcome (cure or death). We included data from
published epidemiological studies conducted in Rio de
Janeiro and in Brazil as a whole found through the electronic
databases: PubMed, Web of Science, and SciELO (Casali
et al. 2004; Da Cunha et al. 1995; Dietz et al. 1990;
Figueiredo et al. 1990; Miagostovich et al. 1993; Nogueira
et al. 1988, 1991, 1993, 1999, 2007, Nogueira et al.1988;
Oliveira et al. 2001; Siqueira et al. 2005; Teixeira et al.
2002; Toledo et al. 2006; Zagne et al. 1994). Data were
used to compile the time series of reported DF cases by age
group, DHF cases, and dengue deaths (Figures 1 and 2).
Analysis
DALYs measure the level of morbidity and mortality
imposed by a disease, that is, the amount of time lost by an
individual as a result of disease or death (Murray 1994;
Murray & Lopez 1994). The time lost due to disease is
adjusted by age of onset and severity of disability. To
adjust for the severity of disability, DALYs methodology
238
volume 14 no 2 pp 237–246 february 2009
uses ‘1’ to represent loss from premature death and ‘0’ to
indicate perfect health. The disability from a disease is
classified into six grades, which consider the loss of time or
ability to perform in recreation, education, procreation,
and occupation (Murray 1994). The lower the grade, the
lower the impact the disability has on a person’s life.
DALYs lost by each case of dengue were calculated using
the following formula (Murray 1994):
DCeba n ðb þ rÞL o
 2
e ½1 þ ðb þ rÞðL þ aÞ  ½1 þ ðb þ rÞa
ðb þ rÞ
where D is the disability grade (D = 1 for premature death,
D = 0 for perfect health); a is the age of onset; L is the
duration of the disability or years of life lost due to
premature death; and r is the social discount rate. In
addition, C and b are parameters from an age-weighting
function. The age weighting function captures the value of
life at different ages, reflecting the dependence of the young
and elderly on adults (Murray 1994). To facilitate
comparison between DALYs lost due to dengue relative to
other diseases, we used values for C, b and r derived from
the Global Burden of Disease study (Table 1) (Murray
et al. 1996). Published estimates of DALYs lost to dengue
from other locations have assumed these same values
(Meltzer et al. 1998; Gubler & Meltzer 1999; Clark et al.
2005; Anderson et al. 2007). The disability grade imposed
by dengue was obtained from previous studies (Table 1)
(Meltzer et al. 1998; Gubler & Meltzer 1999; Lum et al.
2008). To determine DALYs per million individuals
annually, we divided total DALYs per year by the
population size for that year at each geographical level and
multiplied the result by a million.
The biological parameters – age of onset (a) and
duration of disability or years of life lost (L) – are
parameters for individuals who experience dengue. Col-
lectively in a population, such parameters can be assumed
to vary within a range of values. Thus, we assigned a
probability distribution to each parameter (Table 1),
rather than using a single point estimate. We then used
the Monte Carlo method to calculate the corresponding
range for the output of the model: total DALYs per year.
Briefly, the Monte Carlo method constitutes the random
sampling from the distributions of the parameters of the
model, followed by the deterministic evaluation of the
model which generates a distribution for the model
output. From the distribution of the model output
summary measures are calculated for the output of the
model. We used uniform probability distributions for the
parameters and sampled 1000 values from these distri-
butions. Monte Carlo simulations were generated using
PopTools (Hood 2008).
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P. M. Luz et al. DALYs lost to dengue in Brazil

(a) × 105
8
City of Rio de Janeiro
6 State of Rio de Janeiro

DF cases
Brazil
4

0
1986 1988 1990 1992 1994 1996 1998 2000 2002 2004 2006

(b) 3000
City of Rio de Janeiro
State of Rio de Janeiro
DHF cases

2000
Brazil

1000

0
1986 1988 1990 1992 1994 1996 1998 2000 2002 2004 2006

(c) 400
City of Rio de Janeiro
300 State of Rio de Janeiro
Deaths

Brazil
Figure 1 Reported number of (a) dengue 200
fever cases (b) dengue hemorrhagic fever
cases and (c) dengue deaths in the city of 100
Rio de Janeiro, the state of Rio de Janeiro,
and across Brazil from 1986 through 2006 0
Please note: y-axis range varies by plot. 1986 1988 1990 1992 1994 1996 1998 2000 2002 2004 2006

<1 1–14 15–49 >50

1

0.8
Proportion

0.6

Figure 2 Age distribution of DF cases for 0.4

the years 1986 through 2006 Age distribu-
tion was derived from multiple sources:
0.2
1986–1987 (Miagostovich et al. 1993)
1988–2000 (http://www.saude.rio.rj.gov.
br/) and 2001–2006 (http://dtr2004.saude. 0
gov.br/sinanweb/novo/). 1986 1988 1990 1992 1994 1996 1998 2000 2002 2004 2006

not underreported equally for all years. Instead, case

Sensitivity analysis
reporting varies depending on epidemic to endemic years,
Although dengue notification is compulsory, cases are and on clinical syndrome. Under-reporting is particularly a
underreported (Oliveira et al. 2001). However, cases are problem during endemic years (Teixeira et al. 2002;

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P. M. Luz et al. DALYs lost to dengue in Brazil

Table 1 Point estimates and probability distributions [Uniform(Min,Max)] for the parameters of the calculation of disability-adjusted life
years (DALYs)

Parameter Value(s) Notes and references

Age-corrected constant C 0.16243 (Murray et al. 1996)

Age-weighting parameter b
Discount rate r
Disability weight D
Days lost due to DF case L
Days lost due to DHF case L
Average age (in years) of onset for DF case
<1 years
1–14 years
15–49 years
>50
Average age (in years) of onset
for DHF case
Average age (in years) of death
Years of life lost in death L
0.04 (Murray et al. 1996)
0.03 (Murray et al. 1996)
0.81 (Meltzer et al. 1998 Gubler & Meltzer 1999 Lum et al. 2008)
U(2,7) (Zagne et al. 1994 Valdes et al. 2002 Balmaseda et al. 2006a
Anderson et al. 2007 Lum et al. 2008)
U(10,18) (Zagne et al. 1994 Valdes et al. 2002 Balmaseda et al. 2006a
Anderson et al. 2007 Lum et al. 2008)
0.5 (Miagostovich et al. 1993)
7.5 Health Department of the city of Rio de Janeiro (http://www.saude.rio.rj.gov.br/)
32 Health Department of the state of Rio de Janeiro (http://www. saude rj gov br/)
55 Information System for Disease Reporting
(http://dtr2004.saude gov br/sinanweb/novo/)
U(31,44) (Zagne et al. 1994 Da Cunha et al. 1995 Casali et al. 2004)
U(31,44) (Zagne et al. 1994)
U(32,44) (Zagne et al. 1994)

DHF, dengue hemorrhagic fever cases; DF, dengue fever.

Siqueira et al. 2005; Duarte & Franca 2006), while over-

reporting might occur during epidemics (Dietz et al. 1990;
Nogueira et al. 1999). Moreover, DF cases are more often
under-reported than DHF cases (Siqueira et al. 2005).
To evaluate the impact of under- and over-reporting on our
estimates for DALYs lost to dengue, we defined multipli-
cation factors for the number of DF cases by
endemic ⁄ epidemic year. Others have used multiplication
factors of 10 and 27 (Meltzer et al. 1998; Gubler &
Meltzer 1999; Clark et al. 2005). A recently published
empirical study found that a multiplication factor of 10
may be an appropriate adjustment for under-reporting
(Anderson et al. 2007). Given the uncertainties regarding
the magnitude of the multiplication factor, we explore a
range of multiplication factors from 0.3 through 10. We
determined the effect of the adjustment for the inaccuracies
in reporting by comparing results with and without
multiplication factors. For endemic years, we used multi-
plication factors from 1 through 10, where 1 corresponds
to no under-reporting and 10 corresponds to a reporting of
10% of the DF cases. For epidemic years, we used
multiplication factors from 0.3 through 10, to account for
over- to under-reporting. The lower limit of 0.3 for the
multiplication factor reflects the approximate 30% labo-
ratorial confirmation of suspected DF cases (Nogueira
et al. 1993). We used the Monte Carlo method to evaluate
the impact on the DALYs per million individuals annually
of the multiplication factors within the ranges given above.
Results
For the period 1986 through 2006, a mean of 56.4 (range:
35.3–77.8), 46.8 (range: 28.4–65.0), and 22.1 (range:
14.4–30.1) DALYs per million individuals annually were
lost to dengue in the city of Rio de Janeiro, the state of Rio
de Janeiro, and the country of Brazil, respectively. How-
ever, there were significant differences in the dengue
burden for different years (Figure 3). In epidemic years, a
mean of 127.2 (range: 78.8–173.5), 103.4 (range: 62.1–
142.6), and 34.4 (range: 22.8–46.6) DALYs per million
individuals annually were lost to dengue in the city of Rio
de Janeiro, the state of Rio de Janeiro, and Brazil,
respectively. These values are respectively 30.4, 20.5 and
2.7 times higher than those estimated for endemic years in
the jurisdictions.
From 1986 until 1995, dengue burden was highest in
the city and the state of Rio de Janeiro (Figure 3). During
the late 1990s, dengue expanded throughout the country
(Nogueira et al. 2007). This expansion is reflected in the
DALYs estimates for Brazil as a whole, which increase
from the 1990s through the 2000s. Despite the growing
dengue burden, DALYs estimates for the epidemic years
2001 and 2002 were higher for the city and state of Rio
de Janeiro than for Brazil as a whole. For all locations,
the maximum estimate in a single year was for the year
2002 when 559.5 (range: 375.9–741.2), 402.7 (range:
259.4–552.8), and 102.6 (range: 70.9–143.1) DALYs

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P. M. Luz et al. DALYs lost to dengue in Brazil

(a) 800

DALYs per million

600

400

200

0
1986 1988 1990 1992 1994 1996 1998 2000 2002 2004 2006

(b) 600
DALYs per million

400

200

0
1986 1988 1990 1992 1994 1996 1998 2000 2002 2004 2006

(c) 150
DALYs per million

100

Figure 3 Disability adjusted life years

(DALYs) lost to dengue per million indi- 50
viduals annually in (a) the city of Rio de
Janeiro (b) the state of Rio de Janeiro and
(c) Brazil from 1986 through 2006 Please 0
note: y-axis range varies by plot. 1986 1988 1990 1992 1994 1996 1998 2000 2002 2004 2006

were lost to dengue in the city, state, and country,
respectively.
Proportionally, DF was responsible for most of the
dengue burden in all locations (Figure 4). Between 1986
and 2006, DF accounted for over 80% of the dengue
burden. Deaths caused by dengue accounted for almost the
entire remaining burden of 20%. Between 1986 and 2006,
an increasing proportion of the dengue burden was
accounted for by deaths (Figure 4).
The dengue burden was significantly greater when using
multiplication factors to correct for inaccuracies in
reporting (compare results of Figure 5 with Figure 3),
suggesting that the results presented thus far are conser-
vative. The analysis using multiplication factors produces
city, state and national means of 225.9 (range: 43.7–
504.6), 197.0 (range: 40.3–436.6) and 87.3 (range: 27.8–
174.1) DALYs per million individuals annually lost to
dengue. There was considerable variation in the DALYs
lost to dengue by year (Figure 5). The maximum single-
year estimate was for 2002, when 1938.1 (range: 358.1–
4435.3), 1532.0 (range: 267.5–3544.3) and 338.2 (range:
71.5–763.2) DALYs were lost to dengue in the city, state
and country, respectively.
Discussion
We calculated the burden imposed by dengue from 1986
through 2006 in the city of Rio de Janeiro, the state of Rio
de Janeiro, and the country of Brazil, using the DALYs
methodology. Our analysis shows that dengue imposes a
significant burden in these three geographical levels, with
the city of Rio de Janeiro suffering the greatest relative toll.
We found that the dengue burden is disproportionally
derived from DF cases. We also found a significant
difference in dengue burden between endemic and
epidemic years.

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P. M. Luz et al. DALYs lost to dengue in Brazil

(a) 1

DF
Proportion

0.5 DHF
Deaths

0
1986 1988 1990 1992 1994 1996 1998 2000 2002 2004 2006

(b) 1

DF
Proportion

0.5 DHF
Deaths

0
1986 1988 1990 1992 1994 1996 1998 2000 2002 2004 2006

(c) 1

DF
Proportion

0.5 DHF
Deaths

0
1986 1988 1990 1992 1994 1996 1998 2000 2002 2004 2006

Figure 4 Proportion of the dengue burden accounted for by dengue fever (DF) dengue hemorrhagic fever (DHF) and dengue deaths in
(a) the city of Rio de Janeiro (b) the state of Rio de Janeiro and (c) Brazil from 1986 through 2006.

We found that most of the dengue burden results from
mildly symptomatic cases that rarely require hospitaliza-
tions. Given the transmissibility of dengue, a significant
fraction of the population is affected each year (Nogueira
et al. 1993; Kochel et al. 2002; Balmaseda et al. 2006b).
The vast majority of infected individuals will present with
non-specific syndromes or with DF (Gubler 1998). Thus
DF is the strongest determinant of the disease burden.
A similar pattern has been identified in other settings
(Meltzer et al. 1998) such as Thailand, where non-hospi-
talized patients with dengue illness accounted for 73% of
the disease burden (Anderson et al. 2007). For a complete
account of the burden imposed by dengue, all clinical
syndromes must be considered.
We also found that dengue burden is almost always
lower at the state and country level than at the city-level,
although significant at all geographical levels. Moreover,
we analysed 21 years of dengue occurrence and found that
dengue burden varies annually, being most pronounced
during epidemic years. Due to the domestic behavior of
Aedes aegypti, dengue is a disease of the household. Within
the household, Aedes aegypti is capable of feeding on

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P. M. Luz et al. DALYs lost to dengue in Brazil

(a)
4000

DALYs per million

3000

2000

1000

0
1986 1988 1990 1992 1994 1996 1998 2000 2002 2004 2006

(b)
3000
DALYs per million
2000

1000

0
1986 1988 1990 1992 1994 1996 1998 2000 2002 2004 2006

(c) 800
DALYs per million

600
Figure 5 Disability adjusted life years
(DALYs) lost to dengue per million indi-
viduals annually in (a) the city of Rio de 400
Janeiro (b) the state of Rio de Janeiro and
(c) Brazil from 1986 through 2006 when 200
considering multiplication factors for inac-
curacies in reporting Please note: y-axis 0
range varies by plot. 1986 1988 1990 1992 1994 1996 1998 2000 2002 2004 2006

several individuals during one gonotrophic cycle (Gubler
& Meltzer 1999). Dengue transmission can be explosive,
affecting a significant proportion of individuals within a
short period of time. The magnitude of an outbreak is a
function of the population size and of the susceptible
fraction of the population. Crowded urban cities with poor
infrastructure and inadequate sanitary conditions facilitate
dengue transmission (Gubler & Meltzer 1999), as con-
firmed by our analysis of dengue burden in the city of Rio
de Janeiro. We expect a comparable toll to be inflicted on
other crowded urban centres of Latin American.
A significant dengue burden has been reported for other
settings. In Puerto Rico, dengue caused a mean loss of 658
DALYs per million individuals annually between 1984 and
1994 (Meltzer et al. 1998). In the south-east Asia region,
dengue causes a loss of 420 DALYs per million individuals
annually (Shepard et al. 2004). In Thailand, two studies
found similar results: a mean loss of 427 DALYs per
million individuals in 2001 (Clark et al. 2005), and a mean
loss of 465 DALYs per million individuals annually for the
period 1998 to 2002 (Anderson et al. 2007). For the Latin
American and Caribbean regions, 127 DALYs were esti-
mated to be lost due to dengue per year during the period
1988–1992 (Gubler & Meltzer 1999). Except for one study
(Anderson et al. 2007), the above-cited published estimates
have assumed a range of multiplication factors for
inaccuracies in reporting.
For our analysis, we estimated DALYs lost to dengue
both with and without multiplication factors for inac-
curacies in reporting. When we consider these factors,
our estimates of the dengue burden are similar to those
of the above cited studies although higher multiplication
factors have been used elsewhere (Meltzer et al. 1998;
Gubler & Meltzer 1999). For the years considered in our
study, a mean of 225 (maximum of 504) DALYs per
million individuals annually were lost to dengue in the
city of Rio de Janeiro. During epidemic years, dengue
burden reached a mean of 498 (maximum of 1144)
DALYs per million individuals annually. In Brazil,
during epidemic years, a mean of 125 (maximum of
288) DALYs per million individuals annually were
lost to dengue. Thus, it is clear that the dengue burden

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Tropical Medicine and International Health
P. M. Luz et al. DALYs lost to dengue in Brazil
in our setting is of the same order of magnitude as the
dengue burden in countries that have, for decades,
severely suffered from dengue, such as Puerto Rico and
Thailand.
To place dengue within the health priorities of Brazil,
we compared our results to the Global Burden of Disease
Study by WHO (2004) and to the Brazilian Disease
Burden Project developed by a research group from the
Sergio Arouca National School of Public Health at the
Oswaldo Cruz Foundation (Gadelha et al. 2002;
Schramm et al. 2004). With respect to the WHO study,
we found that the dengue burden is on the same order of
magnitude as the following diseases [DALYs estimate per
million individuals are given in parenthesis (WHO
2004)]: leishmaniasis (117), leprosy (58), hepatitis B
(144), hepatitis C (99), syphilis (129), and malaria (235).
With respect to the Brazilian study, we revealed that the
burden imposed by dengue is on the same order of
magnitude as the following diseases (DALYs estimate per
million individuals are given in parentheses) (Gadelha
et al. 2002): sexually transmitted diseases not including
HIV (321), childhood diseases cluster (82) and malaria
(156). Based on these numbers, dengue should receive
the same national priority as these other infectious
diseases.
Our analysis of the dengue burden is conservative
because the impact of dengue extends beyond the health
burden as measured using DALYs lost. The impact of
dengue reaches other sectors which have not been
accounted for in our analysis. There are substantial direct
economic costs related to clinical and therapeutic man-
agement, laboratory tests and vector control. There are
also indirect economic costs such as the cost resulting from
the sick individual’s loss of work, and both psychological
and societal costs (Von Allmen et al. 1979; Kouri et al.
1989; Torres 1997; Valdes et al. 2002; Shepard et al.
2004; Anez et al. 2006; Suaya et al. 2006, 2007; Halstead
et al. 2007).
In summary, we determined the health burden of dengue
in Brazil using the non-monetary index DALYs. Our
findings make evident the significant burden imposed by
dengue on the society and on the government and allow
health authorities to evaluate the importance of dengue
within the competing disease priorities of Brazil. Our
results show that for the assessment of the dengue burden
all clinical syndromes need to be taken into account. As a
consequence of the annual variability in dengue incidence,
our study extends over two decades in order to give an
accurate estimate of the dengue burden. Our estimates can
inform policy planners of Brazil and Latin America about
the allocation of resources for research, prevention and
control.
244
volume 14 no 2 pp 237–246 february 2009
Acknowledgements
We thank Claudia Torres Codeço for her interesting
discussions and insights. We also thank Iuri da Costa
Leite and Joaquim Gonçalves Valente for their advice on
the DALYs calculation, and for their enormous support
in providing us with the methods and results from the
Projeto Carga de Doença (The Burden of Disease study
conducted in Brazil). We thank Kristina Talbert-Slagle
and Angie Hofmann for editing revision, and the two
anonymous reviewers for suggestions which greatly
improved the manuscript. P. M. Luz was funded by
CAPES (Brazilian federal agency for post-graduate edu-
cation), Fulbright, and the Garfield Weston Foundation.
A. P. Galvani greatly acknowledges funding from
Notsew Orm Sands Foundation and the Garfield
Weston Foundation.
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Corresponding Author P. M. Luz, School of Public Health, Yale University, 60 College Street, New Haven, CT 06520, USA.
Tel.: +1 203 785 2642; Fax: +1 203 785 4782; E-mail: paula.luz@yale.edu

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