Simões et al. Parasites & Vectors 2014, 7:100
http://www.parasitesandvectors.com/content/7/1/100
RESEARCH
Open Access
A longitudinal study of Angiostrongylus cantonensis
in an urban population of Rattus norvegicus in
Brazil: the influences of seasonality and host
features on the pattern of infection
Raquel O Simões1,2, Arnaldo Maldonado Júnior2*, Natalie Olifiers2, Juberlan S Garcia2, Ana Valéria FA Bertolino3
and José L Luque4
Abstract
Background: The nematode Angiostrongylus cantonensis is a zoonotic parasite and the most important cause of
eosinophilic meningitis worldwide in humans. In Brazil, this disease has been reported in the states of Espírito Santo
and Pernambuco. The parasite has been detected in the naturally infected intermediate host, in the states of Rio de
Janeiro, Pernambuco and Santa Catarina. The murid Rattus norvegicus R. rattus were recently reported to be naturally
infected in Brazil. In this study, we conducted a two-year investigation of the dissemination pattern of A. cantonensis in
R. norvegicus in an urban area of Rio de Janeiro state, Brazil, and examined the influence of seasonality, year, host weight
and host gender on parasitological parameters of A. cantonensis in rats.
Methods: The study was conducted in an area of Trindade, São Gonçalo municipality, Rio de Janeiro, Brazil. Prevalence
of infected rats, intensity and abundance of A. cantonensis were calculated, and generalized linear models were
created and compared to verify the contribution of host gender, host weight, year and seasonality to the variations
in A. cantonensis abundance and prevalence in rats.
Results: The prevalence of A. cantonensis infection was stable during the rainy (71%, CI 58.9- 81.6) and dry seasons
(71%, CI 57.9-80.8) and was higher in older rats and in females. Seasonality, host weight (used as a proxy of animal
age) and gender were all contributing factors to variation in parasite abundance, with females and heavier (older)
animals showing larger abundance of parasites, and extreme values of parasite abundance being more frequent in
the dry season.
Conclusions: The high prevalence of this parasite throughout the study suggests that its transmission is stable and
that conditions are adequate for the spread of the parasite to previously unaffected areas. Dispersion of the parasite
to new areas may be mediated by males that tend to have larger dispersal ability, while females may be more
important for maintaining the parasite on a local scale due to their higher prevalence and abundance of infection.
A multidisciplinary approach considering the ecological distribution of the rats and intermediate hosts, as well as
environmental features is required to further understand the dynamics of angiostrongyliasis.
Keywords: Rattus norvegicus, Angiostrongylus cantonensis, pattern of infection, Brazil
* Correspondence: maldonad@ioc.fiocruz.br
2
Laboratório de Biologia e Parasitologia de Mamíferos Silvestres
Reservatórios, Instituto Oswaldo Cruz, Av. Brasil 4365 Manguinhos, 21040-360
Rio de Janeiro, RJ, Brazil
Full list of author information is available at the end of the article
© 2014 Simões et al.; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative
Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and
reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain
Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article,
unless otherwise stated.
Simões et al. Parasites & Vectors 2014, 7:100
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Background
The rat lungworm Angiostrongylus cantonensis is a
nematode that, in its adult stage, parasitizes the pulmonary
arteries of the synanthropic rodent Rattus norvegicus, the
definitive host [1]. Mollusc species act as intermediate
hosts and are infected by the first larval stage (L1) eliminated in rodent feces. Three weeks after mollusc infection,
the larvae molt to the infective third stage (L3), becoming
adult worms after being ingested by rats [2]. Humans become infected mainly by ingesting infected intermediate
host or parts of the intermediate host consumed inadvertently when contaminating food is ingested, but may also
be infected by consuming paratenic hosts (shrimps, crabs,
frogs, planarians, and lizards) [3].
The recent introduction of A. cantonensis to the
Americas [4] has resulted in human cases of eosinophilic
meningitis throughout the continents [5-10]. In Brazil,
this disease has been reported in the states of Espirito
Santo, Pernambuco and São Paulo [7,11,12], and the natural intermediate host A. fulica has been observed in the
states of Rio de Janeiro, Pernambuco and Santa Catarina
[13,14]. Recently, R. norvegicus and R. rattus have been
reported to be naturally infected in Brazil [15,16].
Although A. cantonensis is currently spreading rapidly
throughout the Americas [4], there have not been any
studies that have focused on the role of R. norvegicus in
parasite transmission; instead, most studies have focused
only on the intermediate host [17,18]. Horizontal studies
are important because they allow us to characterize the
profile of parasite transmission. In this study, we conducted a two-year investigation of A. cantonensis dissemination pattern in R. norvegicus in an urban area of
Rio de Janeiro state, Brazil, and examined the influence
of seasonality, year, host weight (used as a proxy for host
age), and host gender on the prevalence and abundance
of A. cantonensis in rats.
Methods
Study area
The study was conducted in an urban area of Trindade,
São Gonçalo municipality (22°48’26.7”S, 43°00’49.1”W),
the second most populous city (~1 million habitants) in
the state of Rio de Janeiro, Brazil (Figure 1). The climate
is tropical with recognizable seasons: a rainy season
from October to May and a dry season from April to
November. The annual average temperature of the region
is 25°C, with maximum and minimum temperatures ranging from 38°C to 17°C, respectively. The annual rainfall
is 1200 mm (data obtained from Urban Climatological
Station from Geosciences lab-LABGEO).
Rodent capture
We established three transects spaced approximately
50 meters apart with 20 trapping stations each along
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polluted watercourse banks close to human habitats. A
trapping station was established every 5 meters and included both a Tomahawk® trap (16 × 5 × 5 inches) and
Sherman® trap (3 × 3.75 × 12 inches). The study was conducted every three months from March 2010 to December
2011 and each capture session lasted 4 consecutive days.
Captured rodents were transported to a field laboratory, where they were euthanized in a CO2 chamber,
sexed, weighed and necropsied. All animal procedures
followed the guidelines for capture, handling and care of
mammals of the American Society of Mammalogists
[19]. The collection permits for rodents were obtained
from the Oswaldo Cruz Foundation (FIOCRUZ) Ethical
Committee on Animal Use (Permit Number: LW 24/10)
and the Brazilian government’s Institute for Wildlife and
Natural Resources (Permit Number: 24353–1). Biosafety
techniques were used during all procedures involving
biological samples [20].
Parasitological procedures
Helminths were collected from the pulmonary arteries
and subarachnoid spaces. The organs were separated in
Petri dishes and dissected under a stereomicroscope to
remove the parasites. The collected worms were washed
twice in physiological (0.9%) saline to remove tissue debris and were stored in 70% ethanol. Nematodes were
clarified in lactophenol (40% lactophenol, 20% lactic
acid, 20% phenol, and water q.s.p. 100 mL) and identified using a Zeiss Standard 20 light microscope. The
morphology of the caudal bursa and size of the spicules
were used as taxonomic characteristics for species identification according to Maldonado et al. (2010) [13] and
Chen (1935) [21].
Data analyses
Prevalences with their Sterne’s exact 95% confidence intervals (CI) [22] and the k index of aggregation were calculated using the program Quantitative Parasitology 3.0
[22]. For that, animals were divided into three age classes according to their weight: juveniles (<100 g), subadults (100–200 g) and adults (>200 g) [23]. A binary
logistic regression was used to investigate the influence
of season, year, host gender and host weight (used as a
proxy of animal age) on the presence/absence of A. cantonensis in rats and a generalized linear model with a
negative binomial distribution and log link was performed to verify the contribution of those variables to
the observed variation in A. cantonensis abundance in
pulmonary arteries of rats. We created models consisting
of all combinations and interactions of predictors, as
well as additional models containing an interaction between gender and weight plus year and/or season as
additional variables. These additional models were included because a priori analyses pointed out the inclusion
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Figure 1 Map showing the study area.
of the interaction “host gender* host weight” on the pool
of best-fitting models (see below). All analyses were performed using PASW Statistics Version 18.0. Models were
compared using the Akaike Information Criterion corrected for small sample size (AICc). Models were ranked
based on the difference between the best approximating
model (model with the lowest AICc) and all others in the
set of candidate models (ΔAICc); models with differences
within two units of the top model were considered competitive (best-fitting) models with strong empirical support
[24]. The relative importance of each predictor (or interaction of predictors) was quantified by calculating relative
variable weights (var. weight), which consist on summing
the Akaike weights across all the models where the
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predictor occurs. To better investigate model fit, we
calculated the likelihood ratio chi-square test for the
best-fitting model of parasite abundance; we also calculated the Hosmer-Lemeshow statistic and computed the
Nagelkerke R2 for the top model of parasite presence/
absence. The wald Chi-Square test was used to check
parameter significance in the best-fitting model.
We used the Mann–Whitney U-test and Moses test of
extreme reaction in post-hoc analyses to test for differences in the parasite abundance and its range between
host gender and seasons, whenever these predictors
appeared amongst best-fitting models for parasite abundance. Spearman rank correlation was also used in posthoc analyses to verify how parasite abundance varied
with host weight in males and females. For all significance tests, α = 0.05.
Results
One hundred and fourteen R. norvegicus were captured
during the study. Fifty-six rats were collected during the
rainy season (4 rats were not weighed) and 58 during
the dry season (Table 1).
A total of 861 adult worms were recovered from pulmonary arteries and 82 young worms (L5) in the subarachnoid space found in all age class. The highest
parasite burden (42 adult helminths) occurred in an
adult female during the dry season. In addition, the distribution of the nematodes was aggregated (k = 2.04).
Four models were considered competing models in the
analysis of parasite presence/absence in R. norvergicus, but
their likelihoods were relatively low (from 0.12 to 0.19;
Table 2). Moreover, model fit for the best-fitting model
(model 1; Table 2) was also low (Nagelkerke R2 = 0.221;
Hosmer-Lemeshow statistic: Chi-squared test = 8.561;
df = 8; P = 0.381). Parasite presence/absence was best predicted by host weight (βmodel 1 = 0.006; var. weight = 0.54),
host gender (βfemale, model 1 = 1.191; var. weight = 0.50), and
year (β2010, model 1 = −0.693; var. weight = 0.50), although
“year” was not a significant variable in the top model (Wald
Chi-square = 2.20; df = 1; p = 0.138); All the other predictors in the best-fitting model were significant (P < 0.05).
The prevalence of A. cantonensis varied from 63% to 87%
Table 1 Number of Rattus norvegicus infected by
Angiostrongylus cantonensis organized by age, sex
and season
Age*
Juvenile
Rainy Season
Dry Season
Total
Male
Female
Male
Female
2 (7)
2 (3)
2 (4)
0
6 (14)
Subadults
1 (1)
7 (8)
2 (6)
6 (8)
16 (23)
Adults
12 (17)
13 (16)
18 (25)
13 (15)
56 (73)
Positive rats (total number of collected rats).
*n = 110.
Table 2 Ranking of best-fit models describing parasite
presence/absence in Rattus norvegicus captured at São
Gonçalo, Rio de Janeiro/Brazil from 2010 to 2011;
k = number of parameters in the models
Model
Log(l)
AICc
k ∆AICc
AICc
weight
1-Year + host gender + host weight −54.30 116.98 4
0.00
0.19
2-Host gender + host weight
0.08
0.18
−55.41 117.05 3
3-Year + host gender × host weight −54.35 117.08 4
0.10
0.18
4-Host gender × host weight
0.85
0.12
−55.80 117.82 3
(Table 3; Figure 2), and tended to be higher in females
(78%; CI 65.2-87.2) than in males (59%; CI 46.4-70.1), while
the prevalence in juveniles (43% CI 21.3-67.5) tended to be
lower than in sub-adults (70% CI 48.9-84.5) and adults
(77% CI 65.7-85.0). Prevalence was marginally larger in
2011, but confidence intervals overlapped considerably in
this case (79% CI 66.4-88.1 against 64% CI 51.4-74.9; see
also Table 3). The interaction between host weight and
gender appeared in the third and fourth the best-fitting
models for parasite presence/absence (Table 2), but its relative weight was lowest amongst predictors present in the
best-fitting models (var. weight =0.40). Prevalence increases with age in both host sexes, but the difference between males and females occurs mostly in juveniles and
subadults, with females showing larger prevalences than
males. The multivariate analyses using host gender, host
weight, year and season as independent variables and A.
cantonensis abundance as the dependent variable indicated
that two models were considered competitive (models 1
and 2; Table 4). Season, host weight and host gender
contributed to variation in parasite abundance (likelihood
ratio chi-square for model 1 = 16.03; df = 3; p = 0.001),
even though Akaike weights indicated that the likelihood
of the best-fitting models were relatively low (AICc
weights = 0.40 and 0.15; Table 4). The variable “season”
(var. weight = 0.87) appeared amongst the best-fitting
models because 90% of the animals with abundance
greater or equal than 20 worms (N = 11) were found in
the dry season (βdry season,,model 1 = 0.579). Indeed extreme
values of parasite abundance were more likely to occur in
the dry season (Moses test of extreme reaction: P < 0.001;
Figure 3B); parasite abundance, however, did not differ
between seasons (P = 0.221). The interaction between
host gender and host weight (var. weight = 0.57) appeared
amongst the best-fitting models because the relationship
between parasite abundance and host weight is stronger
in females (βfemales*weight, model 1 = 0.004) than in males
(βmales*weight, model 1 = 0.002), and the β value for males was
not significant (Wald Chi-Square = 2.971; df = 1; p = 0.085).
All the other parameters in the top model were significant (P < 0.05). Post-hoc correlations between parasite
abundance and host weight showed that A. cantonensis
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Table 3 Prevalence (95% confidence interval), median intensity, and mean abundance followed by the standard
deviation of Angiostrongylus cantonensis in Rattus norvegicus collected during 2010 and 2011
Season
Month/year
Number of host
Prevalence
Median intensity
Rainy
March/2010
15
67% (41.5-85.0)
8 ± 5.7
6.2 ± 6.6
Dry
June/2010
15
67% (41.5-85.0)
18 ± 12.6
12.7 ± 13.5
September/2010
19
63% (40.9-80.9)
11 ± 9.8
8.8 ±9.3
December/2010
12
67% (51.7-93.2)
8.5 ± 5.1
6.4 ± 5.9
March/2011
14
79% (38.6-83.8)
10 ± 7.7
6.6 ± 7.8
June/2011
15
87% (60.9-97.5)
10 ± 9.9
8.2 ± 9.9
September/2011
10
70% (39.2-89.7)
8 ± 4.4
5.2 ± 5.1
December/2011
14
79% (51.7-93.2)
7.5 ± 5
5.2 ± 5.5
Rainy
Dry
Rainy
abundance increases with host weight in both sexes
(Rfemales = 0.40, N = 50, P = 0.004; Rmales = 0.30, N = 60,
P = 0.002), which would explain why “host weight”
(var. weight = 0.37) appeared as a main effect in the second
best model (Model 2, Table 4).
Moreover, females had larger parasite abundance
(P = 0.044) and extreme values of parasite abundance
than males (P = 0.004; Figure 3A). Despite differences
in parasite abundance between males and females,
“host gender” as a main factor had the lowest relative
variable weight amongst predictors in the best-fitting
models (0.28).
Discussion
The prevalence of A. cantonensis in R. norvegicus in Rio
de Janeiro is relatively high compared to other localities
where infected rats have been found [3]. As reviewed by
Wang et al. (2008) [3], areas in Cuba and the Dominican
Republic (both in the Americas) had a high prevalence
of A. cantonensis at 60% (12 infected rodents of 20 collected) and 100% (5 infected rodents in 5 collected), respectively. However, the small sample sizes used in these
short-term studies do not allow conclusive results and
Figure 2 Prevalence followed by 95% confidence interval (CI)
of Angiostrongylus cantonensis in Rattus norvegicus collected
during rainy and dry season in an urban area from Rio de
Janeiro, Brazil.
Mean abundance
preclude inference from the helminth infrapopulation
structure. In our study, we observed a high and stable
prevalence of A. cantonensis over two years, which suggests that transmission is continuously high. Prevalences
were marginally larger in 2011, but confidence limits
overlapped considerably between years (see also Table 3).
It would be interesting, however, to investigate whether
A. cantonensis prevalence in R. norvegicus is gradually
increasing in the long-term.
The recent settlement of A. cantonensis in the study
area of São Gonçalo, Rio de Janeiro state could partially
explain the high prevalence of this parasite. Additionally,
the presence of the exotic intermediate host A. fulica in
the study area [14], and its recent dispersion to all the
27 federations in Brazil [14,25,26] may contribute to the
establishment and increase of A. cantonensis transmission to its vertebrate host. However, nothing is known
about the population dynamics of the mollusc species
present in the study area, although it has been demonstrated that variation in the structure of the intermediate
host population plays an important role in the seasonal
fluctuations in helminth community parameters in the
definitive host [27]. Stability in prevalence may also be
caused by the following: (1) a long parasite lifespan in
the definitive host and liberation of L1 larvae over long
periods of time, which may maintain parasite transmission to the intermediate host even in times of low snail
abundance in the environment; (2) the presence of more
than one mollusc species that is able to facilitate development to the infective larval stage L3 [28]; (3) the lack
of factors constraining rat abundance (e.g., constant and
high food availability and refuge); and (4) A. cantonensis
genetic heterogeneity [29,30], which may facilitate adaptation to new environments.
The positive relationship between A. cantonensis abundance and rat weight is at least partially associated with
higher parasite burdens in older (and heavier) rats. As
previously reported [31,32], this observation is likely due
to the longer period of exposure to infection, which is also
corroborated by the higher parasite prevalence found in
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Table 4 Ranking of best-fit models describing parasite abundance in Rattus norvegicus captured at São Gonçalo, Rio de
Janeiro/Brazil from 2010 to 2011; k = number of parameters in the models
Model
Log(l)
AICc
k
∆AICc
1-Season + weight × gender
−331.53
671.4
4
0.00
AICc weight
0.40
2-Season + weight + gender
−332.47
673.3
4
1.89
0.15
3-Season + gender × weight + year
−331.51
673.6
5
2.16
0.13
4-Season + gender + weight + year
−332.35
675.3
5
3.83
0.06
Models 3 and 4 are presented for comparison purposes only.
adult rats. Additionally, the relatively weak relationship
may also suggest the presence of a regulatory process for
parasite density. Indeed, experimental studies demonstrated that rats exposed to A. cantonensis are able to
modulate the parasite burden when re-infected [33].
Males have higher levels of testosterone and larger
home ranges than females [34,35], which would potentially increase the probability of acquiring/maintaining
an infection [36,37]. However, females had a higher
prevalence and abundance of A. cantonensis than males,
and the relationship between parasite abundance and
host weight was also stronger in females, which somewhat undermines the hypothesis that males are more
frequently exposed to infection because of their larger
home ranges and/or testosterone levels. Although male
mammals generally harbor more helminth parasites than
females [37], the hormonal response of each gender may
determine their distinct parasitic profiles [38]. Some
studies have demonstrated female-biased parasitism
[39-41], suggesting that sex-biased parasitism is a complex phenomenon influenced by hormones other than
testosterone [39] and that additional variables in the
host-parasite relationship can influence predisposition to
infection and parasite burdens. For example, female adolescents seem to locomote more and spend more time
exploring aversive areas than males of the same age [42];
if that implies that females explore their home ranges
better, then they may be more prone to infection than
males. This would explain why prevalences are particularly higher in juvenile and subadult females than males
(see Table 3). Notwithstanding, our findings indicate that
females may be particularly important for maintaining
the parasite at a local scale due to their higher prevalence and abundance of infection and their philopatric
behavior, whereas dispersion of the parasite to new areas
may be mediated mainly by males that tend to have larger
dispersion ability [43,44].
Although the prevalence of A. cantonensis did not vary
between seasons (Table 3), the range of parasite abundance was greater during the dry season. Because the
mollusc intermediate hosts are susceptible to desiccation
[45], we would expect a lower abundance of snails and a
consequently lower prevalence and abundance of A. cantonensis in rats during that season. The presence of a
larger number of rats with young larvae of A. cantonensis in the subarachnoid space during the rainy
season suggests that infection rates may actually be
higher during the wet season. In many natural populations, however, animals show seasonal changes in
stress hormones as a response to environmental changes
(e.g. food or water shortage) and/or biotic factors (e.g.
increased intraspecific competition) [46]. If stress hormones in rats were high during the dry season, then individuals may be less able to modulate parasite infection,
Figure 3 Median, quartiles, and minimum and maximum values of abundance of Angiostrongylus cantonensis in Rattus norvegicus
collected in an urban area from Rio de Janeiro, Brazil. Values are given for (A) host gender and (B) season of data collection.
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which would explain the rats with higher burdens in that
season. Nevertheless, there are no studies of seasonal
changes in glucocorticoids in tropical mammals to support this hypothesis.
In summary, our results demonstrated that mainly
host gender and host age (measured as host weight) contributed to variation in A. cantonensis prevalence, while
season, host gender and host weight influenced parasite
abundance. However, model fit for both parasite abundance and prevalence was low, which means that additional variables not investigated may be relatively more
important for determining parasite abundance/prevalence
in the definitive host. For instance, variables directly linked
to infection rates and the abundance of the intermediate
hosts might better predict R. norvegicus infection rates.
Likewise, the host immune system and concomitant infection with other parasites may also be important predictors
for the abundance of A. cantonensis in R. norvegicus. To
disentangle the influence of these variables on parasite
abundance and prevalence, field studies need to be associated with experimental studies.
Conclusions
The stability of A. cantonensis prevalence throughout
the duration of this study confirms that this parasite is
established in the urban region of São Gonçalo municipality in Rio de Janeiro State and is under adequate
conditions for spreading to other areas. We suggest
that a multidisciplinary approach that considers ecological aspects (e.g., variation in diet, dispersal ability
and home range) of the rats and intermediate hosts, as
well as environmental features is required to further
understand the dynamic of several zoonoses, including
angiostrongyliasis [47]. These studies are therefore essential for the implementation of surveillance and control strategies to reduce the risk of angiostrongyliasis
among local residents and to limit the occurrence of
new foci.
Competing interests
The authors declare that they have no competing interests.
Authors’ contributions
Conceived and designed the work: ROS, AMJ and JLL. Performed the work:
ROS and JSG. Analyzed the data: ROS, NO, AMJ and JLL. Revised the manuscript
for important intellectual content: AMJ, NO, JSG and JLL. Wrote the paper: ROS.
All authors read and approved the final version of the manuscript.
Acknowledgments
We would like to thank all that helped with the field work; the staff of CEADE
for making a space available for our field laboratory; Secretary of Health of
São Gonçalo; Heloisa Diniz of Imaging Service-FIOCRUZ and Geosciences Lab
from Geography department (UERJ/FFP).
Author details
1
Curso de Pós-Graduação em Ciências Veterinárias, Universidade Federal
Rural do Rio de Janeiro, Seropédica, RJ, Brazil. 2Laboratório de Biologia e
Parasitologia de Mamíferos Silvestres Reservatórios, Instituto Oswaldo Cruz,
Av. Brasil 4365 Manguinhos, 21040-360 Rio de Janeiro, RJ, Brazil.
Page 7 of 8
3
Departamento de Geografia, Universidade Estadual do Rio de Janeiro/
Faculdade de Formação de Professores, Rua Dr. Francisco Portela, 1470,
24435-005 São Gonçalo, RJ, Brazil. 4Departamento de Parasitologia Animal,
Universidade Federal Rural do Rio de Janeiro, Caixa Postal 74540, 23851-970
Seropédica, RJ, Brazil.
Received: 9 September 2013 Accepted: 11 February 2014
Published: 10 March 2014
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doi:10.1186/1756-3305-7-100
Cite this article as: Simões et al.: A longitudinal study of Angiostrongylus
cantonensis in an urban population of Rattus norvegicus in Brazil: the
influences of seasonality and host features on the pattern of infection.
Parasites & Vectors 2014 7:100.
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