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Temporal Variation of the Presence of Rhodnius prolixus (Hemiptera: Reduviidae) Into Rural Dwellings in the Department of Casanare, Eastern Colombia

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Rhodnius prolixus (Stål, 1859) is the major vector of Trypanosoma cruzi in Colombia and Venezuela. The species is strongly associated with high-altitude ecotopes, such as sylvatic palms (Attalea butyracea), where spatially and temporally stable infestations are established. We investigated temporal variation in regards to the presence of R. prolixus in rural dwellings in the department of Casanare (eastern Colombia) over a period of 12 mo. Thirty houses were sampled from January to December 2017 by installing Maria sensors, collecting triatomines through community entomological surveillance, and conducting a monthly search in each house. The collection of specimens from the houses varied significantly by month with the higher number of collections occurring in the low-rainfall season and the lower number of collections occurring in the months of increased precipitation. The proportions of males, females, and nymphs also varied significantly throughout the time period: nymphs (fifth instar only) were reported only during May, July, and September and significantly greater numbers of females than males were reported in the inspected dwellings in all months. Density, crowding, and colonization indices varied according to the season. A bloodmeal analysis revealed 17 different hosts. A total of 42 randomly selected R. prolixus specimens were subjected to molecular analyses for detection of T. cruzi DNA with 22 found positive (infection prevalence of 52%). In conclusion, we observed a high presence of R. prolixus (infected with T. cruzi) in dwellings close to native palm plantations. These findings indicate a high risk of vector transmission of T. cruzi for people in the study areas and challenges for the current vector control schemes in the region.
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Sampling, Distribution, Dispersal
Temporal Variation of the Presence of Rhodnius prolixus
(Hemiptera: Reduviidae) Into Rural Dwellings in the
Department of Casanare, Eastern Colombia
HelenJineth Rincón-Galvis,1 Plutarco Urbano,1,2 Carolina Hernández,2,3 and
JuanDavid Ramírez2,3,4,
1Grupo de Investigaciones Biológicas de la Orinoquia (GINBIO), Fundación Universitaria Internacional del Trópico Americano
(Unitrópico), Yopal, Colombia, 2Centro de Investigaciones en Microbiología y Parasitología Tropical (CIMPAT), Facultad de
Ciencias, Universidad de los Andes, Bogotá, Colombia, 3Grupo de Investigaciones Microbiológicas-UR (GIMUR), Departamento de
Biología, Facultad de Ciencias Naturales y Matemáticas, Universidad del Rosario, Bogotá, Colombia, and4Corresponding author,
e-mail: juand.ramirez@urosario.edu.co
Subject Editor: David Florin
Received 13 May 2019; Editorial decision 25 August 2019
Abstract
Rhodnius prolixus (Stål, 1859)is the major vector of Trypanosoma cruzi in Colombia and Venezuela. The spe-
cies is strongly associated with high-altitude ecotopes, such as sylvatic palms (Attalea butyracea), where spa-
tially and temporally stable infestations are established. We investigated temporal variation in regards to the
presence of R.prolixus in rural dwellings in the department of Casanare (eastern Colombia) over a period of
12 mo. Thirty houses were sampled from January to December 2017 by installing Maria sensors, collecting
triatomines through community entomological surveillance, and conducting a monthly search in each house.
The collection of specimens from the houses varied significantly by month with the higher number of col-
lections occurring in the low-rainfall season and the lower number of collections occurring in the months of
increased precipitation. The proportions of males, females, and nymphs also varied significantly throughout
the time period: nymphs (fifth instar only) were reported only during May, July, and September and signifi-
cantly greater numbers of females than males were reported in the inspected dwellings in all months. Density,
crowding, and colonization indices varied according to the season. Abloodmeal analysis revealed 17 different
hosts. Atotal of 42 randomly selected R.prolixus specimens were subjected to molecular analyses for detec-
tion of T.cruzi DNA with 22 found positive (infection prevalence of 52%). In conclusion, we observed a high
presence of R.prolixus (infected with T.cruzi) in dwellings close to native palm plantations. These findings in-
dicate a high risk of vector transmission of T.cruzi for people in the study areas and challenges for the current
vector control schemes in the region.
Key words: Colombia, temporal variation, Rhodnius prolixus, density, dispersion
American trypanosomiasis, Chagas disease, is a parasitic infection
caused by the protozoan Trypanosoma cruzi (Cortés and Suárez
2005, Montilla et al. 2011, Llano et al. 2014). This parasite is
transmitted by insects of the subfamily Triatominae, when mucous
membranes or wounded skin comes into contact with the parasite-
infected feces of the bug (Guhl etal. 2007, Becerril et al. 2010). In
Colombia, the department of Casanare (eastern Colombia) has the
second highest reported prevalence of T. cruzi infection in humans
(10%), after Arauca (21.1%) (Cortés and Suárez 2005, Guhl etal.
2007, Parra-Henao etal. 2009). Casanare is recognized as a focus of
vector and oral transmission of Chagas disease as well (Angulo etal.
2012, Zuleta etal. 2017, Hernández etal. 2016).
This disease is endemic on the American continent (Dias etal.
2002), where millions of people are affected. In Colombia, it has
been estimated that 5% of the population are infected and 23% live
in areas with high risk of transmission (Hoyos etal. 2007, Llano
etal. 2014). Vector transmission can occur through the domestic,
peri-domestic, and sylvatic cycles (Montilla etal. 2011, Angulo etal.
2012, Guhl and Ramírez 2013). In a process of domicilation that is
dened as sylvatic triatomines entering dwellings and then propa-
gating as evidenced by the presence of at least three developmental
stages (Guhl etal. 2007, Esteban etal. 2017) sylvatic triatomines
can enter dwellings where both shelter and blood of humans and/
or domestic animals can be obtained. This capacity of triatomines
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Journal of Medical Entomology, XX(X), 2019, 1–8
doi: 10.1093/jme/tjz162
Research
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2Journal of Medical Entomology, 2019, Vol. XX, No. XX
to disperse from sylvatic ecotopes to human habitations represents
a critical factor in the population dynamics of triatomines and the
epidemiology of Chagas disease as previously reported in Brazil and
Argentina (Zeledon and Rabinovich 1981, Pizarro and Romaña
1998, Canale etal. 1999, Dias-Lima and Sherlock 2000).
The distribution of the 149 known species of triatomines varies
according to their ecological requirements (Justi and Galvão 2017).
In Colombia, 27 species have been recorded, of which 17 have been
found infected with T. cruzi (Parra-Henao etal. 2015, Ayala etal.
2019, Velásquez-Ortiz etal. 2019). In the eastern plains of Colombia
(extending into Venezuela), Triatoma dimidiata (Latreille, 1811),
Triatoma. maculata (Erichson, 1848)and Rhodnius prolixus (Stål,
1859)have been recorded as the main vectors of T.cruzi. Of these,
R.prolixus is the most important in Colombia and Venezuela be-
cause of occurrence in sylvatic, domestic, and peri-domestic ecotopes
(Dias et al. 2002, Angulo and Esteban 2011, Angulo et al. 2012,
Urbano etal. 2015, Esteban etal. 2017, Urbano etal. 2018).
Forests of Attalea butyracea (wine palm) are considered the
main ecological entities for sustaining and establishing colonies
of triatomines, particularly R. prolixus in the eastern plains of
Colombia (Teixeira etal. 2001, Abad-Franch et al. 2005, Angulo
etal. 2012, Urbano etal. 2018). Rueda etal. (2014), observed higher
densities of triatomines in palms located near houses, banana plan-
tations, and fruit trees, than in palms located in secondary forests,
possibly because the former provide conditions (food resource in the
blood of humans and domestic animals) that facilitate domiciliation
of the vector (Guhl etal. 2007, Angulo et al. 2013, Urbano et al.
2015, Urbano etal. 2018). Consequently, humans play an important
role in altering the cycle of transmission of the trypanosome parasite
and the vector, increasing the probability of transmission of the par-
asite (Guhl etal., 2007). It is important to clarify the capacity of this
vector to adapt to different ecotopes and to intrude into homes under
different environmental conditions. Precipitation is one of the most
relevant factors involved in the presence of triatomines in human
dwellings; a higher population density was found in wild popula-
tions of R.prolixus (Urbano etal. 2018), Rhodnius neglectus (Lent,
1954), and Rhodnius robustus (Larouse, 1927)during periods of
low rainfall (Gurgel-Gonçalves etal. 2004, Longa and Scorza 2005).
Such information is required to dene rational surveillance
interventions and to implement control programs in areas where
sylvatic populations of triatomines are potentially involved in the
transmission of Chagas disease (Abad-Franch et al. 2005). Most
rural dwellings in the department of Casanare are immersed in land-
scape matrices whose main structural component consists of sylvatic
palms. This area provides biological, ecological, and environmental
conditions, which favor the eco-epidemiological cycles of the para-
site. The aim of this study was to determine the temporal variation
of R.prolixus in rural dwellings of the Casanare department over a
12-mo period. We also identied the T.cruzi infection and the blood
feeding sources of a random subsample of collected R.prolixus.
Materials and Methods
StudyArea
The study was carried out in the villages of Agualinda in the mu-
nicipality of Pore (5.66278°N, −71.9908°W) and Sabanetas in the
municipality of Paz de Ariporo (5.872663°N, −71.84714°W) of the
department of Casanare (Fig. 1). The area comprises forest matrices
composed of grazing and silvo-pastoral areas (trees, forage, and
the grazing of domesticated animals), in addition to natural and
introduced pastures currently used for extensive cattle ranching.
Plantain, cassava, corn, and cacao crops are the most important
economic activities in these municipalities (Bejarano 2012). These
areas have an average annual temperature of 28± 8°C and average
annual rainfall of 2,000–2,700mm. According to the climatic clas-
sication of Kӧppen (Köppen 1918), a tropical climate is repre-
sented with a marked unimodal seasonality having a period of high
rainfall that extends from May to November with average monthly
precipitation of 329mm, and a period of low rainfall during the re-
maining 5 mo with average monthly precipitation of 89mm, and an
altitude range of 280± 10 m above sea level. The dwellings selected
for monitoring were typically located in grazing areas surrounded
by small cultivated areas and scattered palms near riverine forests,
where the main structural component was sylvatic palms. Ahigh
index of infestation by R.prolixus (3.3%) and cases of infection
in humans (7.2%) had previously been reported for the area (Guhl
etal. 2007, Zuleta etal. 2017).
Sampling
Sampling and monitoring were carried out on a total of 30 houses,
12 selected from the village of Sabanetas (Paz de Ariporo) and 18
from the village of Agualinda (Pore). Maria sensors were installed in
these houses, according to the methodology proposed by Wisnivesky-
Colli etal. (1992) and triatomines were collected through commu-
nity entomological surveillance by families trained in recognition of,
searching for, and collection of the triatomine insects. The ‘María
Sensors’ (in-house made) are cardboard boxes with absorbent paper
folded inside that, xed to the walls of the house, can passively de-
tect the presence of triatomines. Direct collection of the insects from
the Maria Sensors occurred when periodic monitoring of the boxes
was carried out, or by evidence of the triatomines such as feces, eggs,
or exuvia. Visits were made monthly during 2017, when the num-
bers of triatomines recorded by the installed sensors was checked
and specimens captured by the families were collected. In addition,
an active-man-hour search was carried out inside each house, with
a sampling effort of 16h per month, and triatomines that were at-
tracted by light during 2 d per month from 1,800 to 2,200 were
collected (Jácome-Pinilla etal. 2015). Triatomines were placed in la-
beled plastic containers, with lter paper folded inside, covered with
a tulle cloth and fastened with rubber band, allowing movement and
absorbing excess moisture, for later identication and processing
in the laboratory. Specimens were identied using the keys of Lent
and Wygodzinsky (1979). In addition, a subsample (42 randomly
selected individuals) was selected to carry out molecular analysis
for identication of the infective agent; these specimens were placed
in absolute ethanol and labeled with the household and the month
sampled.
Statistical Analysis
Shapiro–Wilk tests were performed to analyze data normality as-
sumptions and Levene tests to determine the homoscedasticity of
the variables. Subsequently, Kruskal–Wallis nonparametric tests
were applied to determine signicant differences in the popula-
tion densities of R.prolixus among sampling months, and among
nymphs, females, and males. Trends in the density of individuals cap-
tured per month were analyzed using a multiple Dunn test (P > 0.05).
The relationships between the density of R.prolixus and the average
monthly precipitation and temperature in the inspected dwellings
were examined using the Spearman correlation coefcient (P<0.05).
Density (number of triatomines collected/number of houses exam-
ined), crowding (number of triatomines collected/number of positive
houses), infestation (number of positive houses/number of houses
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3Journal of Medical Entomology, 2019, Vol. XX, No. XX
examined × 100), and colonization (number of houses with nymphs/
number of positive houses × 100)were quantied using the meth-
odological parameters proposed by Suarez-Davalos et al. (2010).
Statistical analyses were performed using RStudio software and the
graphics were made with the Origin 5.0 program.
Detection of T.cruzi DNA, Parasite Genotyping, and
Determination of Feeding Sources
A total of 42 randomly selected R.prolixus were subjected to mo-
lecular analyses for detection of T.cruzi DNA, parasite genotyping,
and identication of feeding sources. All specimens were stored and
conserved in ethanol until processing. DNA extraction of the in-
sects’ guts was conducted using a Qiagen Dneasy Blood & Tissue
kit (Qiagen, Berlin, Germany). Detection of T.cruzi was conducted
by end-point quantitative polymerase chain reaction (qPCR) using
TaqMan Fast Advanced Master Mix 2× (Roche Diagnostics GmbH,
Mannheim, Germany), water and the primers cruzi1 (10µM) (5-
AST CGG CTG ATC GTT TTC-3), cruzi2 (10µM) (5-AAT TCC
TCC AAG CAG CGG ATA-3), and a cruzi3 probe (5µM) (FAM-
CAC ACA CTG GAC ACC AA-NFQ-MGB) to detect the satellite
tandem repeat DNA of the parasite (166bp), following the proce-
dure previously reported (Hernández etal. 2016). A Ct value <38
was considered as positive amplication. For insects with a positive
qPCR result, a conventional PCR for kinetoplast DNA amplication
was conducted using Buffer Taq 10×, MgCl2 50mM, dNTPs 25mM,
Taq Platinum 5 U/µl, water and the primers 121 (50 pmol/µl) (5-
AAA TAA TGT ACG GGK GAG ATG CAT GA-3) and 122 (50
Fig. 1. Geographic location of the villages of Agualinda and Sabanetas in the municipalities of Pore and Paz de Ariporo, respectively (Casanare). Symbols in
the form of houses represent the locations of the villages and stars indicate the urban centers of the two municipalities. Asterisks represent houses that were
monitored in each municipality.
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4Journal of Medical Entomology, 2019, Vol. XX, No. XX
pmol/µl) (5-GGT TCG ATT GGG GTT GGT GTA ATA TA-3) to
discriminate between T.cruzi (330bp) and T.rangeli (400–450bp),
as reported elsewhere (Ramírez etal. 2009). Parasite genotyping was
accomplished by amplication of the spliced leader intergenic region
of the miniexon gene (SL-IR), dividing discrete typing units into two
groups: TcI (350bp) and TcII–T cVI (300bp) as reported elsewhere
(Ramírez etal. 2010).
To determine the blood feeding sources, a 215-bp fragment of the
12S gene fragment was amplied using Go Taq Green Master Mix,
water and primers L1085 (10nM) (5-CCC AAA CTG GGA TTA
GAT ACC C-3) and H1259 (10nM) (5-GTT TGC TGA AGA TGG
CGG TA-3), as reported by Dumonteil et al. (2018). PCR prod-
ucts were cleaned using ExoSAP-IT Express PCR Product Cleanup
75001/75002 (Affymetrix, Thermo Fisher Scientic Inc., Waltham,
MA) and then submitted to Sanger sequencing. Resulting sequences
were edited in MEGA X software and submitted to BLASTn for
similarity search.
Results
A total of 2,240 specimens of R.prolixus were collected with density
variation recorded according to the month sampled. Despite the use
of Maria sensors to ensure the maximum collection of insects, these
sensors did not collect or detect any specimens. Triatomines were
detected only in each of the inspected homes by communitarian sur-
veillance and active-man-hour search. The months, organized from
lowest to highest with respect to the numbers of individuals col-
lected, were: 125 in July, 130 in September, 132 in August, 136 in
June, 141 in October, 149 in November, 185 in May, 205 in March,
210 in April, 223 in December, 289 in January, and 316 in February.
Presence
The population density of captured R.prolixus varied signicantly
among months (Kruskal–Wallis, χ2=51.12, P< 0.05). The highest
densities of presence of triatomines into homes were observed in
February, January, December, April, and March, and the lowest
densities were observed in May, November, October, June, August,
September, and July (Dunn test, P<0.05). The density of individuals
captured per dwelling was signicantly higher in the period of low
rainfall than during high rainfall (Dunn test, P< 0.05). However,
the period of transition from low to high rainfall (April and May)
also recorded high densities of individuals in the dwellings (Fig. 2).
In the case of temperature, this variable was homogenous across the
year with an average temperature of 26.4°C. Therefore, we were not
able to nd an association between insect’s density and temperature.
Statistically signicant differences were found among the monthly
samples in the densities of males, females, and nymphs (fth instar)
of R.prolixus (Kruskal–Wallis, χ2=9,573.12, P<0.05). The propor-
tion of females recorded in the inspected houses was higher than that
of males in all months. The highest presence densities of females rel-
ative to males were recorded in February, January, December, April,
and March. Nymphs were reported only in the months of May, July,
and September (Fig. 3).
Entomological Indexes
The months of low rainfall had higher density and crowding indexes.
The colonization index estimates the number of micro-habitats in
which immature stages of development are found with respect to the
number of habitats in which an individual is collected. There was ev-
idence of possible colonization only in the months of May, July, and
September (Table 1). In contrast, the index of infestation was rela-
tively high throughout the year; although the number of individuals
arriving per dwelling uctuated according to the season, there was
continuous presence of individuals throughout theyear.
Presence and Precipitation
As the average monthly precipitation levels increased, the number
of individuals arriving at the dwellings decreased (Spearman coef-
cient=−0.6643) indicating greater presence into dwellings during
the months of low rainfall (P= 0.0021) (Fig. 4). During the 7 mo
from May to November with the greatest precipitation, the detection
of triatomines was low as evidenced by only 998 specimens (44.5%
of the total for the year) collected, while the 5 mo of lower rainfall
from December to April recorded 1,243 insects (55.4%). In the case
of temperature, detections did not vary signicantly.
Detection of T.cruzi Infection, Parasite Genotyping,
and Determination of Blood Sources
We analyzed 20 R.prolixus individuals from Paz de Ariporo. Eight
(40%) were found infected with T.cruzi and subsequently four were
Fig. 2. Numbers of Rhodnius prolixus specimens (adults and nymphs) col-
lected per dwelling during the sampling months in the villages of Agualinda
(Pore) and Sabaneta (Paz de Ariporo) in the department of Casanare. Error
bars are shown during each month of sampling.
Fig. 3. Numbers of Rhodnius prolixus males (Green), females (Blue), and
nymphs (red) collected per dwellings of the villages of Agualinda (Pore) and
Sabaneta (Paz de Ariporo) in the department of Casanare. Error bars are
shown during each month of sampling.
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5Journal of Medical Entomology, 2019, Vol. XX, No. XX
typed as TcI, and two with mixed infections (TcI/TcII–T cVI). At
Pore, we analyzed 22 R. prolixus individuals of which 14 (64%)
were found infected with T.cruzi, of which six were typed as TcI and
four as mixed infections (TcI/T cII–TcVI). In terms of blood sources,
we identied the following BLAST hits: Coendou melanurus (por-
cupine) (seven hits), Homo sapiens (Human) (eight hits), Alouatta
caraya (Howler monkey) (seven hits), Ovis candensis (Sheep) (one
hit), Equus caballus (Horse) (seven hits), Sus scrofa (Pig) (seven
hits), Oryctolagus cuniculus (Rabbit) (two hits), Felis catus (Cat)
(ve hits), Rattus norvegicus (Rat) (one hit), Monodelphis domestica
(Opposum) (four hits), Canis lupus familiaris (Dog) (seven hits),
Didelphis marsupialis (Opposum) (seven hits), Mus musculus
(Mouse) (three hits), Ochotona koslowi (Kozlov’s Pika) (one hit),
Myrmecophaga tridactyla (Giant anteater) (six hits), Xenothrix
mcgregori (The Jamaican monkey) (four hits), and Talpa occidentalis
(Iberian Mole) (two hits). No individuals were positive for T.rangeli.
Discussion
Human habitations provide suitable environments for some
triatomines to easily establish infestations (Gurgel-Gonçalves etal.
2004). Once triatomines establish in dwellings, or in adjacent loca-
tions, they are able to feed on animals and/or people, increasing the
transmission risk of T.cruzi, which in turn would be reected in the
incidence of Chagas disease and the maintenance of triatomines in
the home and peri-domiciliary areas (Rueda etal. 2014, Hernández
etal. 2016). This could explain the high indexes of infestation and
crowding found in this investigation (Table 1). However, the colo-
nization index found was very low and in only a small proportion
of dwellings, which suggests that the species was not establishing
populations within the dwellings. Rather, there were continuous
events of presence throughout the year (Fig. 2), with an index of
home infestation higher than previously recorded for R. prolixus
in other areas of the department (Angulo etal. 2012, Zuleta etal.
2017), and also higher than reported for other species: Rhodnius
ecuadoriensis (Lent & León, 1958)in Ecuador (47.4%) (Grijalva
et al. 2017) and Triatoma infestans (Klug, 1834) in Argentina
(2.9–14.4%) (Espinoza et al. 2017, Cavallo et al. 2018). This is
consistent with the high prevalences of T. cruzi infection (40% in
Paz de Ariporo and 64% in Pore), which were higher than those re-
ported for intradomiciliary triatomines in Brazil (1.8–24.7%) (Ferro
e Silva etal. 2018), Venezuela (0.06%) (Carrasco etal. 2014), and
the Colombian Orinoco (15.78%) (Angulo etal. 2012).
The understanding regarding the feeding sources and T. cruzi
infection in triatomines found in human dwellings has relevance
in terms of transmission dynamics and vector control programs.
For example, in Mexico, the feeding sources conrmed a signi-
cant dispersal of T. dimidiata between habitats (domestic and syl-
vatic) (Torres-Montero 2012). In addition, this has been reported in
T.brasiliensis from Brazil where the authors could hypothesize with
the mammal feeding source information previous concerns about
the potential of several animals to link the sylvatic and domiciliary
T.cruzi cycles (Almeida etal. 2016). Recent work in the Colombian
Orinoco region concluded that A.butyracea palms found in altered
areas provide a similar quality habitat for R.prolixus populations in
terms of bloodmeal availability. Both habitats showed similarities in
vector infection prevalence and potential host species, representing a
single T.cruzi transmission scenario at the introduced oil palm plan-
tation and native Attalea palm interface (Erazo etal. 2019). These
studies augment our ndings of 17 feeding sources and high T.cruzi
infection indicating high risk for Chagas disease transmission in the
studyarea.
Although a high frequency of presence in houses was observed
throughout the year (12-mo period of sampling) (Fig. 2), there was
no evidence of colonization, because the presence of immature stages
was sporadic (Fig. 3, Table 1). This could perhaps be explained by
the rst to fourth instars not having the capacity to disperse the dis-
tance from the palms to the houses. Nevertheless, a study conducted
in Venezuela showed the presence of rst to fourth instar infesting
houses but in the absence of palm surroundings (Feliciangeli etal.
2004). Future studies should consider the sampling of the palms
and houses to unveil the true entomological indexes. In addition,
this highlights one limitation of our study as R.prolixus individuals
were removed from the environment each month, reducing the ef-
fective sample size of the population. In certain houses, the monthly
surveys may have reduced the presence of R.prolixus to near zero.
Thus the next month survey would have been new individuals that
moved in since the previous survey, representing a sample bias. As
we are aware of this possible limitation, the collection of new indi-
viduals each month supports our hypothesis of strong dispersion of
R.prolixus into the houses, which poses a challenge for the vector
control programs in the region.
Table 1. Monthly changes of density, crowding indexes, infestation, and colonization indexes of Rhodnius prolixus in dwellings in the
department of Casanare, during the year 2017
Index Jan. Feb. Mar. Apr. May June July Aug. Sep. Oct. Nov. Dec.
Density 9.6 10.6 6.8 7.0 6.2 4.5 4.2 4.4 4.3 4.7 5.0 7.4
Crowding 10.3 10.9 7.6 8.1 7.4 5.7 5.0 4.7 5.0 5.2 5.3 8.0
Infestation (%) 93.3 96.7 96.7 86.7 83.3 80.0 83.3 93.3 86.7 90.0 93.3 93.3
Colonization (%) 0.0 0.0 0.0 0.0 16.7 0.0 10.7 0.0 15.4 0.0 0.0 0.0
Fig. 4. Changes in the density of R. prolixus (adults and nymphs) in rural
dwellings in the municipalities of Pore and Paz de Ariporo Casanare, and in
the average monthly rainfall reported at the Paz de Ariporo meteorological
station (36011501 of 2017).
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6Journal of Medical Entomology, 2019, Vol. XX, No. XX
In the case of the adults collected, Ayala etal. (2019) recorded the
highest number of triatomine presences into houses in the months of
April and May, and lower densities in the months of higher rainfall.
These observations are consistent with ours, in which we recorded
the largest numbers of R.prolixus individuals reaching homes in the
months of lower average rainfall (Fig. 4), and higher frequency of
arrival at homes in the months of April and May (Fig. 2). This re-
inforces the importance of precipitation in terms of triatomine inva-
sion and entomological indexes. In our case, temperature was not an
important factor as this was constant during the year. In the present
study, an inverse relationship was noted between the number of indi-
viduals per dwelling and the average monthly rainfall (Fig. 4), corrob-
orating earlier studies (Pizarro and Romaña 1998, Longa and Scorza
2005, Vásquez etal. 2013, Esteban etal. 2017, Ayala etal. 2019).
These changes represent a response of the species to environmental
changes, habitat disturbances, and inter- and intraspecic competi-
tion. However, triatomines mitigate exposure of their populations
to these adverse conditions by developing adaptive physiological
and ethological responses to seasons, which may also be reected
in variations in the incidence of developmental stages (Schowalter
2006). The difference noted in the proportions of nymphs and adults
collected in the dwellings could be determined, in the rst instance,
by forced dispersion from wild and peri-domiciliary ecotopes and,
secondly, by physiological adaptations of Triatominae, consisting
of variations of nymphal periods, molting and hatching rates of
eggs, longevity of adults, and the numbers of instars and periods of
starvation (Zeledon and Rabinovich 1981, Arévalo etal. 2007). In
addition, R. prolixus tends to migrate from its original ecotope in
search of food or shelter in some seasons (Noireau and Dujardin
2001), and the immature stages have smaller dispersion distances
than adults (Zeledon and Rabinovich 1981). Likewise, other au-
thors have suggested that the density of triatomines captured in the
months of low rainfall is signicantly higher than during the high
rainfall season (Noireau and Dujardin 2001, Hernández etal. 2010,
Vásquez etal. 2013, Reyes et al. 2017), possibly because the dis-
persion of triatomines is related to their nutritional status during
the dry season. When their wild food sources are reduced, adult
triatomines may migrate toward articial ecotopes in search of alter-
natives sources of blood. This is consistent with our observations of
an inverse relationship between the density of triatomines that reach
dwellings and the average monthly precipitation in the study area,
giving rise to a higher density of triatomines in dwellings in the dry
season (Fig. 4). Similarly, higher population densities were found in
wild populations of R.prolixus (Urbano etal. 2018), R. neglectus,
and R. robustus during periods of low rainfall (Gurgel-Gonçalves
etal. 2004, Longa and Scorza 2005).
Rhodnius prolixus is a species with a wide climatic and alti-
tudinal range. It is frequently found in houses in localities where
the opportunity to colonize domestic structures is present (Noireau
et al. 1994, Esteban etal. 2017). However, according to Esteban
etal. (2017), adaptation of this vector to ecotopes such as palms
means that the presence of immature stages in dwellings could result
from displacement from nearby wild habitats rather than a coloniza-
tion event. The presence of the species in homes has been associated
with decrease in vegetation coverage, the distance to the forest, and
lights from houses at night (Angulo etal. 2012, Erazo and Cordovez
2016). This could explain the low colonization frequency, which was
observed in only three months (Table 1). These results differed from
those found for R.ecuadoriensis and Panstrongylus rufotuberculatus
(Latreille, 1811), which exhibited rates of intradomiciliary coloni-
zation up to 77% (Grijalva etal. 2017). Interestingly, the average
densities of males, females, and nymphs within dwellings showed
the opposite trend to those reported by Esteban etal. (2017) for the
department of Santander (eastern Colombia), where a greater pro-
portion of males were reported to reach homes. Asignicant differ-
ence between collections of females and males (Fig. 3) was detected,
suggesting the composition of populations that enter dwellings is
variable due to previous reports that demonstrate that the male/fe-
male ratio in sylvatic populations is similar (Grijalva et al. 2012,
Urbano etal. 2015).
The high dispersal capacity of R. prolixus is linked to a high
adaptability to invade and colonize different micro-habitats in par-
ticular areas (Heger etal. 2006, Feliciangeli etal. 2007). This was
evidenced in the present investigation by the observation that 100%
of the homes inspected contained triatomines in at least 1 mo, and
that the index of infestation throughout the hydrological period was
relatively constant (Table 1). Conversely, since 100% of the houses
contained triatomines, the presence of the triatomines may also have
been the result of propagation within the houses. Rhodnius prolixus
was recorded in houses of the municipalities of both Pore and Paz de
Ariporo, suggesting that the wide geographical distribution of this
species in Casanare results from its successful colonization of many
species of palm and types of housing. Dispersion of R.prolixus may
occur toward anthropogenic environments where some vertebrate
refuges are present or relict palm species occur (Urbano etal. 2015);
later they behave as intruders in homes in search of food. These fac-
tors have been evaluated for several species of triatomines in other
countries (Fitzpatrick etal. 2008, Grijalva etal. 2014, Ferro e Silva
etal. 2018). An understanding of the mammals that inhabit the palm
forests is important to unveil the blood sources for the triatomines.
However, we do not have information about the diversity of ani-
mals in these palms and therefore cannot formulate a hypothesis in
this regard. The only available information was the high diversity
of blood sources demonstrating that despite having food available,
R.prolixus is attracted to human dwellings, possibly due to light at-
traction (Jácome-Pinilla etal. 2015).
Finally, control strategies for vector transmission of Chagas di-
sease in the department of Casanare have been directed towards
housing interventions with insecticides (Palomino etal. 2007, Silva
etal. 2007, Rendón etal. 2015, Zuleta etal. 2017). However, our
data show that the months in which the probability of dispersion
and presence of insects into houses is greatest corresponds to the
low rainfall period. It is important to keep this in mind in the imple-
mentation of control strategies and epidemiological surveillance in
the department.
Conclusion
The high values of the indices and trends in the presence frequencies
of triatomines in rural dwellings in the department of Casanare indi-
cate a high risk of T.cruzi vectorial transmission in the study areas.
However, the low colonization indexes recorded for R.prolixus in-
dicate that this species is unlikely to exhibit domiciliation. This does
not rule out this process in the future, given that the largest propor-
tion of individuals entering the houses in an intrusive or sporadic
manner were females.
Acknowledgments
The authors wish to express their gratitude to the owners of the homes where the
samplings were made. We thank Harry Taylor, Ph.D., from Edanz Group (www.
edanzediting.com/ac) for editing a draft of this manuscript. This work was funded
by Dirección de Investigación e Innovación from Universidad del Rosario and by
Fundación Universitaria Internacional del Trópico Americano (Unitrópico).
Downloaded from https://academic.oup.com/jme/advance-article-abstract/doi/10.1093/jme/tjz162/5574699 by guest on 27 September 2019
7Journal of Medical Entomology, 2019, Vol. XX, No. XX
Competing Interests
The authors assert no conict of interest. All authors have read and
approved the manuscript and its analyses.
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... Likewise, abundant populations of sylvatic R. prolixus have been identified associated with native palms Attalea butyracea and palms introduced in agro-industrial crops such as Elaeis guineensis with high rates of natural infection by T. cruzi (24). A high presence of R. prolixus infected with T. cruzi has been shown in homes in rural areas, which increases in the low rainfall season and decreases in the months of higher rainfall (26,27). On the other hand, Casanare is the department of the country with the highest number of acute CD, both isolated cases and outbreaks; between 2012 and 2020, 8 outbreaks of presumed oral transmission were reported, and acute cases have been reported in 52.6% (10/19) of the municipalities. ...
... The most important economic activities are cattle ranching, agriculture, and mining (30); most rural dwellings are immersed in landscape matrices whose main structural component are wild palms. This area provides biological, ecological, and environmental conditions, which favor the ecoepidemiological cycles of the parasite T. cruzi (27). ...
... In Figure 4, the geographical distribution of DTUs in the different municipalities of the department can be observed (Figure 4). Studies carried out in triatomines have mainly identified the DTUs TcI, TcII, TcIII, TcIV, and TcVI in R. prolixus, T. maculata, P. geniculatus, and Psammolestes arthuri (27,(38)(39)(40)(41). In a study carried out in children with chronic Chagas disease from this region, DTU TcI was identified more frequently (42). ...
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Background: Chagas disease (CD), caused by the protozoan Trypanosoma cruzi , is considered a public health problem in Latin America. In Colombia, it affects more than 437,000 inhabitants, mainly in Casanare, an endemic region with eco-epidemiological characteristics that favor its transmission. The objective of this study was to describe the clinical and epidemiological characteristics of the cases of acute CD in Casanare, eastern Colombia, in the period 2012–2020. Methods: In the present study, 103 medical records of confirmed cases of acute CD were reviewed. The departmental/national incidence and fatality were compared by year; the climatological data of mean temperature, relative humidity, and precipitation per year were reviewed and plotted at IDEAM (Colombian Meteorology Institute) concerning the number of cases of acute CD per month, and it was compared with the frequency of triatomines collected in infested houses by community surveillance. Univariate, bivariate, and multivariate analyses were performed, comparing symptoms and signs according to transmission routes, complications, and age groups. Results: The incidence was 3.16 cases per 100,000 inhabitants, and the fatality rate was 20% in the study period. The most frequent symptoms included: fever 98.1%, myalgia 62.1%, arthralgia 60.2%, and headache 49.5%. There were significant differences in the frequency of myalgia, abdominal pain, and periorbital edema in oral transmission. The main complications were pericardial effusion, myocarditis, and heart failure in the group over 18 years of age. In Casanare, TcI Discrete Typing Unit (DTU) has mainly been identified in humans, triatomines, and reservoirs such as opossums and dogs and TcBat in bats. An increase in the number of acute CD cases was evidenced in March, a period when precipitation increases due to the beginning of the rainy season. Conclusions: The results corroborate the symptomatic heterogeneity of the acute phase of CD, which delays treatment, triggering possible clinical complications. In endemic regions, clinical suspicion, diagnostic capacity, detection, and surveillance programs should be strengthened, including intersectoral public health policies for their prevention and control.
... Instead, this discordance may reflect differences in relative amounts of T. cruzi and R. prolixus eDNA deposition/ differential rates of eDNA degradation between species, or the gene copy number between the two targets used for qPCR detection; in our assay the LoD for the T. cruzi satellite DNA was an order of magnitude more sensitive compared to the 12S rRNA in R. prolixus. Alternatively, these findings may be indicative of active infected vectors in these houses; parasite transmission is known to be highly precarious and inefficient, requiring an estimated 900-4000 infected contacts per case 61 and previous studies in Casanare have identified houses where 100% of collected Rhodnius are positive for T. cruzi 62 . While human infection was only self-reported in two houses, T. cruzi transmission in this area is also under-diagnosed due to substantial heterogeneity in acute symptomology 57 and other significant barriers to adequate healthcare, including lack of diagnostics, infrastructure and financial investment, and limited physician awareness 63 . ...
... Instead, between June-September 2021, cotton-tipped swabs (Guangzhou Improve Medical Instruments Co., Ltd, China) were used to sample triatomine and T. cruzi eDNA from different surfaces in houses and peri-domestic structures in Agualinda and San Isidro, municipality of Pore, Department of Casanare, Colombia (endemic for Chagas disease) and Prado Veraniego, municipality of Bogotá (non-endemic for Chagas disease) ( Fig. 6; Supplementary file S2). Each dry swab was used to wipe one random 10 cm 2 surface area of a selected part of the house/peri-domestic structure; roofs were not sampled because in Casanare, Rhodnius are preferentially found in the walls 62 . Householders completed a short questionnaire to confirm triatomine infestation and T. cruzi infection. ...
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Chagas disease vector control relies on prompt, accurate identification of houses infested with triatomine bugs for targeted insecticide spraying. However, most current detection methods are laborious, lack standardization, have substantial operational costs and limited sensitivity, especially when triatomine bug densities are low or highly focal. We evaluated the use of FTA cards or cotton-tipped swabs to develop a low-technology, non-invasive method of detecting environmental DNA (eDNA) from both triatomine bugs and Trypanosoma cruzi for use in household surveillance in eastern Colombia, an endemic region for Chagas disease. Study findings demonstrated that Rhodnius prolixus eDNA, collected on FTA cards, can be detected at temperatures between 21 and 32 °C, when deposited by individual, recently blood-fed nymphs. Additionally, cotton-tipped swabs are a feasible tool for field sampling of both T. cruzi and R. prolixus eDNA in infested households and may be preferable due to their lower cost. eDNA detection should not yet replace current surveillance tools, but instead be evaluated in parallel as a more sensitive, higher-throughput, lower cost alternative. eDNA collection requires virtually no skills or resources in situ and therefore has the potential to be implemented in endemic communities as part of citizen science initiatives to control Chagas disease transmission.
... Wild populations of locally native triatomine-bug species are involved in most such transmission events [5,6]. For example, palm-dwelling bugs of the genus Rhodnius often invade, and sometimes breed in, human dwellings across southern Mesoamerica [7], northern South America including Colombia and Ecuador [8,9], the Orinoco basin [10,11], the Cerrado and Caatinga of central-northeastern Brazil [12][13][14], and Amazonia [14,15]. ...
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Attalea palms provide primary habitat to Rhodnius spp., vectors of Trypanosoma cruzi . Flying from palms, these blood-sucking bugs often invade houses and can infect people directly or via food contamination. Chagas disease (CD) risk may therefore increase when Attalea palms thrive near houses. For example, Attalea dominate many deforested landscapes of eastern Amazonia, where acute-CD outbreaks are disturbingly frequent. Despite this possible link between deforestation and CD risk, the population-level responses of Amazonian Attalea and their resident Rhodnius to anthropogenic landscape disturbance remain largely uncharted. We studied adult Attalea palms in old-growth forest (OGF), young secondary forest (YSF), and cattle pasture (CP) in two localities of eastern Amazonia. We recorded 1856 Attalea along 10 transects (153.6 ha), and detected infestation by Rhodnius spp. in 18 of 280 systematically-sampled palms (33 bugs caught). Distance-sampling models suggest that, relative to OGF, adult Attalea density declined by 70–80% in CP and then recovered in YSF. Site-occupancy models estimate a strong positive effect of deforestation on palm-infestation odds (β CP-infestation = 4.82±1.14 SE), with a moderate decline in recovering YSF (β YSF-infestation = 2.66±1.10 SE). Similarly, N -mixture models suggest that, relative to OGF, mean vector density sharply increased in CP palms (β CP-density = 3.20±0.62 SE) and then tapered in YSF (β YSF-density = 1.61±0.76 SE). Together, these results indicate that disturbed landscapes may support between ~2.5 (YSF) and ~5.1 (CP) times more Attalea -dwelling Rhodnius spp. per unit area than OGF. We provide evidence that deforestation may favor palm-dwelling CD vectors in eastern Amazonia. Importantly, our landscape-disturbance effect estimates explicitly take account of (i) imperfect palm and bug detection and (ii) the uncertainties about infestation and vector density arising from sparse bug data. These results suggest that incorporating landscape-disturbance metrics into the spatial stratification of transmission risk could help enhance CD surveillance and prevention in Amazonia.
... (39,43,50) Findings from Colombia and Venezuela, for example, clearly substantiate the need for surveillance programs capable of gauging the epidemiological risk posed by wild R. prolixus populations inhabiting palms of the Orinoco basin. (51,52,53,54) Recent records of R. prolixus in agribusiness plantations of African oil-palms (Elaeis guineensis) outline a potentially emerging challenge that is yet to be characterised in terms of human infection risk. (55,56) Wild R. ecuadoriensis populations are similarly common in Phytelephas palm-crowns across central-western Ecuador. ...
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Chagas disease (CD) still imposes a heavy burden on most Latin American countries. Vector-borne and mother-to-child transmission cause several thousand new infections per year, and at least 5 million people carry Trypanosoma cruzi. Access to diagnosis and medical care, however, is far from universal. Starting in the 1990s, CD-endemic countries and the Pan American Health Organization-World Health Organization (PAHO-WHO) launched a series of multinational initiatives for CD control-surveillance. An overview of the initiatives' aims, achievements, and challenges reveals some key common themes that we discuss here in the context of the WHO 2030 goals for CD. Transmission of T. cruzi via blood transfusion and organ transplantation is effectively under control. T. cruzi, however, is a zoonotic pathogen with 100+ vector species widely spread across the Americas; interrupting vector-borne transmission seems therefore unfeasible. Stronger surveillance systems are, and will continue to be, needed to monitor and control CD. Prevention of vertical transmission demands boosting current efforts to screen pregnant and childbearing-aged women. Finally, integral patient care is a critical unmet need in most countries. The decades-long experience of the initiatives, in sum, hints at the practical impossibility of interrupting vector-borne T. cruzi transmission in the Americas. The concept of disease control seems to provide a more realistic description of what can in effect be achieved by 2030.
... Venezuela, northern Colombia, northern and central-west Brazil, and the Guiana region are potential at-risk areas for Chagas disease. This result matches zones with current disease transmission [92], except for Guyana, Surinam, and French Guyana, where Chagas disease is not a public health concern [92, 93], although T. infestans is the main vector in Brazil [94] and Rhodnius prolixus (Stal, 1859) in Colombia and Venezuela [95,96]. In 2011, all the previously endemic Central America countries were formally certified as free of Chagas disease transmission thanks to control strategies for eradication of the main domestic vector, R. prolixus [97]. ...
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Ecoepidemiological scenarios for Chagas disease transmission are complex, so vector control measures to decrease human-vector contact and prevent infection transmission are difficult to implement in all geographic contexts. This study assessed the geographic abundance patterns of two vector species of Chagas disease: Triatoma maculata (Erich-son, 1848) and Rhodnius pallescens (Barber, 1932) in Latin America. We modeled their potential distribution using the maximum entropy algorithm implemented in Maxent and calculated distances to their niche centroid by fitting a minimum-volume ellipsoid. In addition, to determine which method would accurately explain geographic abundance patterns, we compared the correlation between population abundance and the distance to the ecological niche centroid (DNC) and between population abundance and Maxent environmental suit-ability. The potential distribution estimated for T. maculata showed that environmental suit-ability covers a large area, from Panama to Northern Brazil. R. pallescens showed a more restricted potential distribution, with environmental suitability covering mostly the coastal zone of Costa Rica and some areas in Nicaragua, Honduras, Belize and the Yucatá n Peninsula in Mexico, northern Colombia, Acre, and Rondô nia states in Brazil, as well as a small region of the western Brazilian Amazon. We found a negative slope in the relationship between population abundance and the DNC in both species. R. pallecens has a more extensive potential latitudinal range than previously reported, and the distribution model for T. maculata corroborates previous studies. In addition, population abundance increases according to the niche centroid proximity, indicating that population abundance is limited by the set of scenopoetic variables at coarser scales (non-interactive variables) used to determine the ecological niche. These findings might be used by public health agencies in Latin America to implement actions and support programs for disease prevention and vector PLOS ONE PLOS ONE | https://doi.org/10.1371/journal.pone.
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Chagas disease is considered a public health issue in Colombia, where many regions are endemic. Triatoma dimidiata is an important vector after Rhodnius prolixus , and it is gaining importance in Boyacá, eastern Colombia. Following the recent elimination of R . prolixus in the region, it is pivotal to understand the behavior of T . dimidiata and the transmission dynamics of T . cruzi . We used qPCR and Next Generation Sequencing (NGS) to evaluate T . cruzi infection, parasite load, feeding profiles, and T . cruzi genotyping for T . dimidiata specimens collected in nine municipalities in Boyacá and explored T . dimidiata population genetics. We found that T . dimidiata populations are composed by a single population with similar genetic characteristics that present infection rates up to 70%, high parasite loads up to 1.46 × 10 ⁹ parasite-equivalents/mL, a feeding behavior that comprises at least 17 domestic, synanthropic and sylvatic species, and a wide diversity of TcI genotypes even within a single specimen. These results imply that T . dimidiata behavior is similar to other successful vectors, having a wide variety of blood sources and contributing to the circulation of different genotypes of the parasite, highlighting its importance for T . cruzi transmission and risk for humans. In the light of the elimination of R . prolixus in Boyacá and the results we found, we suggest that T . dimidiata should become a new target for vector control programs. We hope this study provides enough information to enhance surveillance programs and a future effective interruption of T . cruzi vector transmission in endemic regions.
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Background: Oil palm plantation establishment in Colombia has the potential to impact Chagas disease transmis-sion by increasing the distribution range of Rhodnius prolixus. In fact, previous studies have reported Trypanosoma cruzi natural infection in R. prolixus captured in oil palms (Elaeis guineensis) in the Orinoco region, Colombia. The aim of this study is to understand T. cruzi infection in vectors in oil palm plantations relative to community composition and host dietary specialization by analyzing vector blood meals and comparing these results to vectors captured in a native palm tree species, Attalea butyracea. Methods: Rhodnius prolixus nymphs (n=316) were collected from A. butyracea and E. guineensis palms in Taura-mena, Casanare, Colombia. Vector blood meals from these nymphs were determined by amplifying and sequencing a vertebrate-specific 12S rRNA gene fragment. Results: Eighteen vertebrate species were identified and pigs (Sus scrofa) made up the highest proportion of blood meals in both habitats, followed by house mouse (Mus musculus) and opossum (Didelphis marsupialis). Individual bugs feeding only from generalist mammal species had the highest predicted vector infection rate, suggesting that gener-alist mammalian species are more competent hosts for T. cruzi infection . Conclusions: Oil palm plantations and A. butyracea palms found in altered areas provide a similar quality habitat for R. prolixus populations in terms of blood meal availability. Both habitats showed similarities in vector infection rate and potential host species, representing a single T. cruzi transmission scenario at the introduced oil palm plantation and native Attalea palm interface.
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Background: Chagas disease (CD) is caused by the protozoan parasite Trypanosoma cruzi, and is transmitted by hematophagous insects of the family Reduviidae. Psammolestes arthuri is a sylvatic triatomine distributed in Colombia and Venezuela which feeds on birds and there are a few studies that have reported Ps. arthuri naturally infected with T. cruzi. In Colombia, Ps. arthuri has been found in dwellings, making it important to evaluate its possible role in the T. cruzi transmission cycle. We aimed to evaluate the presence of T. cruzi and feeding sources of Ps. arthuri to elucidate new possible scenarios of T. cruzi transmission in the country. Methods: A total of 60 Ps. arthuri were collected in Arauca and Casanare, Colombia. We detected and genotyped T. cruzi and identified feeding sources. The frequency of the presence of T. cruzi was obtained and compared with different eco-epidemiological variables. Multiple correspondence analysis was conducted to explore associations between eco-epidemiological variables and the presence of T. cruzi; with these results, a logistic regression was used to determine statistical associations. Results: The infection rate of T. cruzi was 70.7% and was mostly associated with insect stage, sex, bird nest and feeding source. Regarding discrete typing units (DTUs), TcI was found in 54.7% samples, of which 21.7% (5/23) were TcIDom, 52.1% (12/23) had mixed infection (TcIDom-TcISylv), and single infection with TcISylv was not detected. Mixed infections (TcI/TcII-TcVI) were found in 9.52% (4/42) of the samples; of these, 14.2% (6/42) were TcII-TcVI. A total of 15 feeding sources were identified and the most frequent were: Cranioleuca baroni (35.85%), Homo sapiens (26.42%), Thraupis episcopus (11.32%) and Serinus albogularis (3.77%). Conclusions: Although Ps. arthuri is mainly ornithophilic, this species may be feeding on other animals that can be infected with T. cruzi, possibly playing a role maintaining the zoonotic cycle of the parasite. Further studies with molecular techniques and wider sampling are needed to improve information regarding infection rates, ecotopes and habits with the aim of evaluating whether Ps. arthuri could be a potential T. cruzi vector.
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Triatoma infestans (Hemiptera: Reduviidae) is a vector of the Trypanosoma cruzi parasite, causative agent of Chagas disease. During the last decade, vector control activities have been systematically carried out in northwestern Argentina, an endemic region for this disease. The general aim of this study to evaluate was spatio-temporal variation of infestation by T. infestans in rural communities of Los Llanos in La Rioja province. We estimated house infestation using two sampling methods: passive and active. Passive collection was conducted with community participation collecting triatomines. Six passive collections were carried out in 397 houses during the warm season between 2014 and 2017. Active collection of T. infestans was thoroughly performed by trained staff for 60 minutes and was carried out once in March 2016. The estimate of intradomestic infestation did not show significant differences between both collection methods (p = 0.39). However, passive collection method had lower sensitivity than active collection method for the estimation of peridomestic infestation and intradomestic colonization (PDI: p< 0.01; ID colonization: p< 0.01). The results obtained with passive collection methods showed that the infestation in the study area was spatially heterogeneous and temporally variable. Intradomiciliary infestation decreased over time (14.4% to 7.9%, p<0.05) although the effect of the chemical treatment application was not associated with the infestation level of T. infestans (p = 0.15) and the Departments had a different response each year (p<0.01). A high infestation cluster was located in the south of our study area during 2016–2017. The vector presence in the houses confirms the importance of to improve entomological surveillance programs. The search for triatomines carried out by the inhabitants might be a useful method to complement the activities of vector control programs in isolated and rural areas.
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