Age and socio-economic status affect dengue and COVID-19 incidence: spatio-temporal analysis of the 2020 syndemic in Buenos Aires City.

In early 2020, Argentina experienced the worst dengue outbreak in its history, concomitant with first-to-date increasing COVID-19 cases. Dengue epidemics in temperate Argentina have already been described as spatially heterogeneous; in the previous 2016 outbreak, transmission occurred 7.3 times more frequently in slums compared to the rest of Buenos Aires City (CABA). These informal settlements have deficient sanitary conditions, precarious housing and high incidence of social vulnerabilities. The purpose of this work was to study the spatio-temporal patterns of the 2020 dengue epidemic in CABA in relation to socio-economic living conditions of its inhabitants and its interaction with the onset of COVID-19. The study considered the period between Jan 1st and May 30th 2020. Dengue and COVID-19 databases were obtained from the National Health Surveillance System; each record was anonymized and geo-localized. The city was divided according to census tracts and grouped in four socio-economic strata: slums, high, mid and low residential. An aligned-rank transform ANOVA was performed to test for differences in the incidence of dengue and COVID-19, and age at death due to COVID-19, among socio-economic strata, four age categories and their interaction. The incidence by cluster was calculated with a distance matrix up to 600 m from the centroid. Spatial joint dengue and COVID-19 risk was estimated by multiplying the nominal risk for each disease, defined from 1 (low) to 5 (high) according to their quantiles. During the study period, 7,175 dengue cases were registered in CABA (incidence rate 23.3 cases per 10,000 inh), 29.2% of which occurred in slums. During the same period, 8,809 cases of COVID-19 were registered (28.6 cases per 10,000 inh); over half (51.4%) occurred in slums, where the median age of cases (29 years old) was lower than in residential areas (42 years old). The mean age of the deceased was 58 years old in slums compared to 79 years old outside. The percentage of deaths in patients under 60 years old was 56% in slums compared to 8% in the rest of the city. The incidence of both diseases was higher in slums than in residential areas for most age categories. Spatial patterns were heterogeneous: dengue presented higher incidence values in the southern sector of the city and the west, and low values in highly urbanized quarters, whereas COVID-19 presented higher values in the east, south, high populated areas and slums. The lowest joint risk clusters were located mainly in high residential areas, whereas high joint risk was observed mainly in the south, some western clusters, the historical part of the city and center north. The social epidemiological perspective of dengue and COVID-19 differed, given that socio environmental heterogeneity influenced the burden of both viruses in a different manner. Despite the overwhelming effect of the COVID-19 pandemic, health care towards other diseases, especially in territories with pre-existing vulnerabilities, should not be unattended.

Assessment of combined tools and strategies for Aedes aegypti control with low environmental impact.

The control of the mosquito vector Aedes aegypti L. (Diptera: Culicidae) is the main action against dengue, chikungunya, and Zika. The excessive use of conventional insecticides has promoted the development of other control methods and strategies with lower environmental impact. We evaluated the effectiveness of applying triflumuron 1 ppm and emptying water-filled containers in a field trial in temperate Argentina. Both control methods were implemented either individually or combined and regularly from the beginning of the mosquito reproductive season or once it reached peak abundance. The impact on a non-target midge of the genus Chironomus was also tested. The highest reductions of Ae. aegypti were achieved in treatments which included triflumuron. This effect was stronger when applied from the beginning of the reproductive season, with < 1.3% of positive containers throughout the entire season. No enhancing effects were obtained when combining both control methods. Treatments with triflumuron were not completely innocuous for the non-target species, with Chironomus sp. more susceptible to treatments including triflumuron applied from the beginning of the reproductive season than all others. Sharp reductions of mosquito populations in urban environments with high density of water-filled containers are possible with minimum container management efforts, by applying triflumuron 1 ppm every 6 weeks. In temperate urban settings, better results can be obtained when applications begin early in the reproductive season of the mosquito vector Aedes aegypti.

Is autumn the key for dengue epidemics in non endemic regions? The case of Argentina.

BACKGROUND: Dengue is a major and rapidly increasing public health problem. In Argentina, the southern extreme of its distribution in the Americas, epidemic transmission takes place during the warm season. Since its re-emergence in 1998 two major outbreaks have occurred, the biggest during 2016. To identify the environmental factors that trigger epidemic events, we analyzed the occurrence and magnitude of dengue outbreaks in time and space at different scales in association with climatic, geographic and demographic variables and number of cases in endemic neighboring countries. METHODS: Information on dengue cases was obtained from dengue notifications reported in the National Health Surveillance System. The resulting database was analyzed by Generalized Linear Mixed Models (GLMM) under three methodological approaches to: identify in which years the most important outbreaks occurred in association with environmental variables and propose a risk estimation for future epidemics (temporal approach); characterize which variables explain the occurrence of local outbreaks through time (spatio-temporal approach); and select the environmental drivers of the geographical distribution of dengue positive districts during 2016 (spatial approach). RESULTS: Within the temporal approach, the number of dengue cases country-wide between 2009 and 2016 was positively associated with the number of dengue cases in bordering endemic countries and negatively with the days necessary for transmission (DNT) during the previous autumn in the central region of the country. Annual epidemic intensity in the period between 1999-2016 was associated with DNT during previous autumn and winter. Regarding the spatio-temporal approach, dengue cases within a district were also associated with mild conditions in the previous autumn along with the number of dengue cases in neighboring countries. As for the spatial approach, the best model for the occurrence of two or more dengue cases per district included autumn minimum temperature and human population as fixed factors, and the province as a grouping variable. Explanatory power of all models was high, in the range 57-95%. DISCUSSION: Given the epidemic nature of dengue in Argentina, virus pressure from endemic neighboring countries along with climatic conditions are crucial to explain disease dynamics. In the three methodological approaches, temperature conditions during autumn were best associated with dengue patterns. We propose that mild autumns represent an advantage for mosquito vector populations and that, in temperate regions, this advantage manifests as a larger egg bank from which the adult population will re-emerge in spring. This may constitute a valuable anticipating tool for high transmission risk events.

Distribution of the members of the Pipiens Assemblage in the sympatric area from Argentina: which is where and when?

Given their medical and veterinary relevance, the members of the Pipiens Assemblage are a worldwide target of ecological research. The distribution of Culex pipiens s.s. and Cx. quinquefasciatus converge in Buenos Aires, Argentina, where hybrids have been detected. Each member of the assemblage exhibits a distinct eco-physiological behaviour that can affect its efficiency in pathogen transmission. Our aim was to identify the environmental drivers for the spatio-temporal distribution of each member, focusing on latitudinal and urbanisation gradients. Immatures of mosquitoes were surveyed in artificial containers found within 11 public cemeteries, raised up to the adult stage and identified by their male genitalia. The distribution of each member was associated with the environment in a Generalized Linear Model. The variable accounting for most of the heterogeneity was latitude; Cx. quinquefasciatus was collected more frequently at northern cemeteries, whereas Cx. pipiens and hybrids were more likely at the southern extreme. The urbanisation gradient was also associated with the occurrence of Cx. quinquefasciatus and hybrids at the high and low end, respectively. Other relevant variables were cemetery total area, the proportion with graves and the presence of plastic flowers in the containers. The spatial distribution of the members of the Pipiens Assemblage within the sympatric region in South America is driven by environmental features. The information presented herein provides essential baseline data for surveillance programs and control activities.

Distribution of the members of the Pipiens Assemblage in the sympatric area from Argentina: which is where and when?

Given their medical and veterinary relevance, the members of the Pipiens Assemblage are a worldwide target of ecological research. The distribution of Culex pipiens s.s. and Cx. quinquefasciatus converge in Buenos Aires, Argentina, where hybrids have been detected. Each member of the assemblage exhibits a distinct eco-physiological behaviour that can affect its efficiency in pathogen transmission. Our aim was to identify the environmental drivers for the spatio-temporal distribution of each member, focusing on latitudinal and urbanisation gradients. Immatures of mosquitoes were surveyed in artificial containers found within 11 public cemeteries, raised up to the adult stage and identified by their male genitalia. The distribution of each member was associated with the environment in a Generalized Linear Model. The variable accounting for most of the heterogeneity was latitude; Cx. quinquefasciatus was collected more frequently at northern cemeteries, whereas Cx. pipiens and hybrids were more likely at the southern extreme. The urbanisation gradient was also associated with the occurrence of Cx. quinquefasciatus and hybrids at the high and low end, respectively. Other relevant variables were cemetery total area, the proportion with graves and the presence of plastic flowers in the containers. The spatial distribution of the members of the Pipiens Assemblage within the sympatric region in South America is driven by environmental features. The information presented herein provides essential baseline data for surveillance programs and control activities.

Regional Extinctions and Quaternary Shifts in the Geographic Range of Lestodelphys halli, the Southernmost Living Marsupial: Clues for Its Conservation.

The Patagonian opossum (Lestodelphys halli), the southernmost living marsupial, inhabits dry and open environments, mainly in the Patagonian steppe (between ~32 °S and ~49 °S). Its rich fossil record shows its occurrence further north in Central Argentina during the Quaternary. The paleoenvironmental meaning of the past distribution of L. halli has been mostly addressed in a subjective framework without an explicit connection with the climatic "space" currently occupied by this animal. Here, we assessed the potential distribution of this species and the changes occurred in its geographic range during late Pleistocene-Holocene times and linked the results obtained with conservation issues. To this end, we generated three potential distribution models with fossil records and three with current ones, using MaxEnt software. These models showed a decrease in the suitable habitat conditions for the species, highlighting a range shift from Central-Eastern to South-Western Argentina. Our results support that the presence of L. halli in the Pampean region during the Pleistocene-Holocene can be related to precipitation and temperature variables and that its current presence in Patagonia is more related to temperature and dominant soils. The models obtained suggest that the species has been experiencing a reduction in its geographic range since the middle Holocene, a process that is in accordance with a general increase in moisture and temperature in Central Argentina. Considering the findings of our work and the future scenario of global warming projected for Patagonia, we might expect a harsh impact on the distribution range of this opossum in the near future.

Waiting for chikungunya fever in Argentina: spatio-temporal risk maps.

Chikungunya virus (CHIKV) transmission has been detected in America in 2013 and recently reached south up to Bolivia, Brazil and Paraguay, bordering countries of Argentina. The presence of the mosquito Aedes aegypti in half of the country together with the regional context drove us to make a rapid assessment of transmission risk. Temperature thresholds for vector breeding and for virus transmission, together with adult activity from the literature, were mapped on a monthly basis to estimate risk. Transmission of chikungunya by Ae. aegypti in the world was seen at monthly mean temperatures from 21-34ºC, with the majority occurring between 26-28ºC. In Argentina temperatures above 21ºC are observed since September in the northeast, expanding south until January and retreating back to the northeast in April. The maximum area under risk encompasses more than half the country and around 32 million inhabitants. Vector adult activity was registered where monthly means temperatures exceeded 13ºC, in the northeast all over the year and in the northern half from September-May. The models herein proposed show that conditions for transmission are already present. Considering the regional context and the historic inability to control dengue in the region, chikungunya fever illness seems unavoidable.

Is temperature the main cause of dengue rise in non-endemic countries? The case of Argentina.

BACKGROUND: Dengue cases have increased during the last decades, particularly in non-endemic areas, and Argentina was no exception in the southern transmission fringe. Although temperature rise has been blamed for this, human population growth, increased travel and inefficient vector control may also be implicated. The relative contribution of geographic, demographic and climatic of variables on the occurrence of dengue cases was evaluated. METHODS: According to dengue history in the country, the study was divided in two decades, a first decade corresponding to the reemergence of the disease and the second including several epidemics. Annual dengue risk was modeled by a temperature-based mechanistic model as annual days of possible transmission. The spatial distribution of dengue occurrence was modeled as a function of the output of the mechanistic model, climatic, geographic and demographic variables for both decades. RESULTS: According to the temperature-based model dengue risk increased between the two decades, and epidemics of the last decade coincided with high annual risk. Dengue spatial occurrence was best modeled by a combination of climatic, demographic and geographic variables and province as a grouping factor. It was positively associated with days of possible transmission, human population number, population fall and distance to water bodies. When considered separately, the classification performance of demographic variables was higher than that of climatic and geographic variables. CONCLUSIONS: Temperature, though useful to estimate annual transmission risk, does not fully describe the distribution of dengue occurrence at the country scale. Indeed, when taken separately, climatic variables performed worse than geographic or demographic variables. A combination of the three types was best for this task.

Epidemiology of canine heartworm in its southern distribution limit in South America: Risk factors, inter-annual trend and spatial patterns.

This study was aimed at understanding some aspects of the canine heartworm epidemiology in the southern distribution limit of the parasite in South America. With this objective, 19,298 blood samples of owned dogs from 65 localities of 13 municipalities of Buenos Aires Province were tested for Dirofilaria immitis circulating microfilariae and/or female antigens. The overall heartworm prevalence was 1.63% by microhematocrit tube technique (n=19,136), 3.65% by modified Knott (n=713), and 14.41% by antigen test kit (n=118). Microfilaremic dogs showed a median of 1933 microfilariae per millilitre (q1=375, q3=5625, n=100). Male dogs belonging to breeds of short hair and large size recorded significantly higher prevalences than the other categories. Also, the prevalence increased significantly with the age and only dogs younger than 12 months were not found infected. A clear decreasing trend of the annual prevalence was observed during the whole study period, from 3.91% in 2001 to 1.17% in 2006. D. immitis-infected dogs were detected in 32 localities of 9 municipalities (prevalence range: 0.2-6.7%). Generalized linear models were used to assess associations between heartworm prevalence and environmental variables. The resulting significant models were univariate and included variables related with soil cover and human population density. The best model predicted maximum heartworm prevalences around middle values of bare soil cover, and lower at high and low covers. According to our analyses, canine heartworm infection in urban temperate Argentina could be described as relatively low, endemic, and spatially heterogeneous. Host and environmental factors affecting heartworm transmission at local level were identified and discussed.

Hantavirus reservoir Oligoryzomys longicaudatus spatial distribution sensitivity to climate change scenarios in Argentine Patagonia.

BACKGROUND: Oligoryzomys longicaudatus (colilargo) is the rodent responsible for hantavirus pulmonary syndrome (HPS) in Argentine Patagonia. In past decades (1967-1998), trends of precipitation reduction and surface air temperature increase have been observed in western Patagonia. We explore how the potential distribution of the hantavirus reservoir would change under different climate change scenarios based on the observed trends. METHODS: Four scenarios of potential climate change were constructed using temperature and precipitation changes observed in Argentine Patagonia between 1967 and 1998: Scenario 1 assumed no change in precipitation but a temperature trend as observed; scenario 2 assumed no changes in temperature but a precipitation trend as observed; Scenario 3 included changes in both temperature and precipitation trends as observed; Scenario 4 assumed changes in both temperature and precipitation trends as observed but doubled. We used a validated spatial distribution model of O. longicaudatus as a function of temperature and precipitation. From the model probability of the rodent presence was calculated for each scenario. RESULTS: If changes in precipitation follow previous trends, the probability of the colilargo presence would fall in the HPS transmission zone of northern Patagonia. If temperature and precipitation trends remain at current levels for 60 years or double in the future 30 years, the probability of the rodent presence and the associated total area of potential distribution would diminish throughout Patagonia; the areas of potential distribution for colilargos would shift eastwards. These results suggest that future changes in Patagonia climate may lower transmission risk through a reduction in the potential distribution of the rodent reservoir. CONCLUSION: According to our model the rates of temperature and precipitation changes observed between 1967 and 1998 may produce significant changes in the rodent distribution in an equivalent period of time only in certain areas. Given that changes maintain for 60 years or double in 30 years, the hantavirus reservoir Oligoryzomys longicaudatus may contract its distribution in Argentine Patagonia extensively.

Aedes aegypti, Aedes albopictus, and dengue in Argentina: current knowledge and future directions.

Since the reinfestation of South American countries by Ae. aegypti, dengue fever (DF) and dengue hemorrhagic fever (DHF) have become a major public health concern. The aim of this paper was to review the information related with Aedes vectors and dengue in Argentina since the reintroduction of Ae. aegypti in 1986. The geographic distribution of Ae. albopictus is restricted to the Northeast, and that of Ae. aegypti has expanded towards the South and the West in comparison with the records during the eradication campaign in the 1960s. Since 1998, 4,718 DF cases have been reported concentrated in the provinces of Salta, Formosa, Misiones, Jujuy and Corrientes. Despite the circulation of three dengue virus serotypes (DENV-1, -2 and -3) in the North of the country, DHF has not occurred until the present. The information published over the last two decades regarding mosquito abundance, temporal variations, habitat characteristics, competition, and chemical and biological control, was reviewed. Considering the available information, issues pending in Argentina are discussed. The presence of three DENV, the potential spread of Ae. albopictus, and the predicted climate change suggest that dengue situation will get worse in the region. Research efforts should be increased in the Northern provinces, where DHF is currently an actual risk.

Aedes aegypti, Aedes albopictus, and dengue in Argentina: current knowledge and future directions

Since the reinfestation of South American countries by Ae. aegypti, dengue fever (DF) and dengue hemorrhagic fever (DHF) have become a major public health concern. The aim of this paper was to review the information related with Aedes vectors and dengue in Argentina since the reintroduction of Ae. aegypti in 1986. The geographic distribution of Ae. albopictus is restricted to the Northeast, and that of Ae. aegypti has expanded towards the South and the West in comparison with the records during the eradication campaign in the 1960s. Since 1998, 4,718 DF cases have been reported concentrated in the provinces of Salta, Formosa, Misiones, Jujuy and Corrientes. Despite the circulation of three dengue virus serotypes (DENV-1, -2 and -3) in the North of the country, DHF has not occurred until the present. The information published over the last two decades regarding mosquito abundance, temporal variations, habitat characteristics, competition, and chemical and biological control, was reviewed. Considering the available information, issues pending in Argentina are discussed. The presence of three DENV, the potential spread of Ae. albopictus, and the predicted climate change suggest that dengue situation will get worse in the region. Research efforts should be increased in the Northern provinces, where DHF is currently an actual risk.

Dynamics of Fasciola hepatica transmission in the Andean Patagonian valleys, Argentina.

We described the transmission dynamics of Fasciola hepatica at its southern distribution range. Studies of prevalence and egg output in cattle and population dynamics and infection in snails were performed in a farm in the Andean Patagonian valleys, Argentina, between December 1998 and February 2002. Snail surveys were conducted from spring to autumn. Infection was diagnosed coprologically in the whole herd at the beginning and end of the study, and in a cohort of heifers at the beginning and end of 2001. A twice-a-year anthelmintic treatment was implemented in 1999. The relationship of the variables mentioned above with temperature and rainfall was determined. Lymnaea viatrix showed a life-span of about 15 months and an annual pattern of population dynamics. Specimens were frequently found in temporary environments and lagoons, and rarely in streams. Snail abundance and soil-water availability were directly related in temporary environments and inversely related in lagoons. Overall prevalence in L. viatrix was 0.67% (range: 0.9-14%) and infection was detected in summer and autumn. At the beginning of the study, calves were the least infected age group (15%). Prevalences and median egg counts in grazing animals were similar at the beginning (heifers: 81%, 3.3 epg; cows: 60%, 1.3 epg) and end of the study (heifers and cows: around 51%, 1 epg). Likewise, the prevalence in the cohort of heifers remained similar (around 40%) between surveys. Transmission to cattle was highly effective despite of the short activity period and the low infection rate of snails, and the regular anthelminthic treatment. There would be two seasonal transmission peaks, one in summer-autumn, when infected snails were present, and the other in early spring due to overwintering metacercariae. Some recommendations based on the climatic conditions of the region are provided to minimize snail infection and ultimately to reduce the incidence of fasciolosis in cattle.

Spatial and temporal transmission risk of Dirofilaria immitis in Argentina.

The aim of this work was to assess spatial and seasonal Dirofilaria immitis transmission risk throughout Argentina with models based on the temperature threshold below which filarial development will not proceed in the mosquito (i.e. 14 degrees C), the occurrence and the number of potential vector mosquito species, and the Heartworm Development Units derived from the degree-days concept. The four models showed a similar increasing southwest-northeast tendency and correlated significantly with canine prevalences used as external validation data. About one-third of Argentina would be suitable for heartworm transmission and the highest risk areas include the north-eastern provinces. According to our models, heartworm transmission is markedly seasonal with peaks in January and February; no region would support transmission throughout the year. To improve the present models, it is necessary to know which mosquito species are competent rather than potential vectors in the country. We believe the present study provides the first risk assessment maps for D. immitis transmission in the Southern Hemisphere and provides a useful guide for heartworm prevention during the transmission periods in different regions of Argentina.

[Spatio-temporal variability in the transmission of dengue in Buenos Aires City]. / Variación espacio-temporal del riesgo de transmisión de dengue en la Ciudad de Buenos Aires.

Cases of dengue detected in Buenos Aires City between 1999 and 2000 confirmed the possibility of epidemic outbreaks. The activity of its vector Aedes aegypi was monitored to study the spatial and temporal risk of dengue transmission. Adult oviposition activity of Aedes aegypti showed an heterogeneous spatio-temporal distribution pattern. It was detected between October and May. The vector was detected from spring to fall in the Northern, Western and Southern areas of the city (periphery) and only in summer in the Eastern part (downtown-river). The proportion of infested sites differed between the three periods but the infested areas coincided spatially. Although a spatial and temporal heterogeneity exists, the pattern repeated itself during the three periods suggesting stable dynamics. The not infested areas presented the highest population and employees densities while the areas infested during the three periods the lowest. This might represent an attenuation of the risk, because higher densities do not coincide with higher infestation. From the point of view of the vector the risk of transmission would concentrate between January and March and occupy 50% of the city surface in the periphery.

Variacion espacio-temporal del riesgo de transmision de dengue en la ciudad de Buenos Aires / Spatio-temporal variability in the transmission of dengue in Buenos Aires city

Los casos de dengue detectados en la Ciudad de Buenos Aires entre 1999 y 2000 confirmaron la posibilidad de brotes epidémicos. Para estudiar el riesgo de transmisión de dengue espacial y temporalmente se midió la actividad de su vector, el mosquito Aedes aegypti. La actividad de ovipostura del vector mostró un patrón de distribución heterogéneo en el tiempo y el espacio. Ocurrió entre octubre y mayo. En las áreas del Norte, Oeste y Sur de la ciudad (periferia) el vector fue detectado entre la primavera y el otoño en tanto que en las áreas del Este (microcentro-río) sólo en el verano. La proporción de sitios infestados varió entre los 3 períodos de estudio, pero las zonas infestadas coincidieron espacialmente. Aunque se observó variación anual y espacial de la infestación, el patrón se repitió durante los 3 años de estudio sugiriendo una dinámica estable. Las áreas de la ciudad no infestadas presentaron las mayores densidades de población y de empleados, mientras que las infestadas durante los 3 períodos presentaron las menores densidades. Esto podría representar una atenuación del riesgo, ya que no coincide la mayor densidad de habitantes con la mayor infestación. El riesgo de transmisión desde el punto de vista del vector se concentraría entre enero y marzo y ocuparía el 50% de la superficie de la ciudad en la periferia.

Variación espacio-temporal del riesgo de transmisión de dengue en la Ciudad de Buenos Aires. / [Spatio-temporal variability in the transmission of dengue in Buenos Aires City]

Cases of dengue detected in Buenos Aires City between 1999 and 2000 confirmed the possibility of epidemic outbreaks. The activity of its vector Aedes aegypi was monitored to study the spatial and temporal risk of dengue transmission. Adult oviposition activity of Aedes aegypti showed an heterogeneous spatio-temporal distribution pattern. It was detected between October and May. The vector was detected from spring to fall in the Northern, Western and Southern areas of the city (periphery) and only in summer in the Eastern part (downtown-river). The proportion of infested sites differed between the three periods but the infested areas coincided spatially. Although a spatial and temporal heterogeneity exists, the pattern repeated itself during the three periods suggesting stable dynamics. The not infested areas presented the highest population and employees densities while the areas infested during the three periods the lowest. This might represent an attenuation of the risk, because higher densities do not coincide with higher infestation. From the point of view of the vector the risk of transmission would concentrate between January and March and occupy 50

of the city surface in the periphery.

Variacion espacio-temporal del riesgo de transmision de dengue en la ciudad de Buenos Aires / Spatio-temporal variability in the transmission of dengue in Buenos Aires city

Los casos de dengue detectados en la Ciudad de Buenos Aires entre 1999 y 2000 confirmaron la posibilidad de brotes epidémicos. Para estudiar el riesgo de transmisión de dengue espacial y temporalmente se midió la actividad de su vector, el mosquito Aedes aegypti. La actividad de ovipostura del vector mostró un patrón de distribución heterogéneo en el tiempo y el espacio. Ocurrió entre octubre y mayo. En las áreas del Norte, Oeste y Sur de la ciudad (periferia) el vector fue detectado entre la primavera y el otoño en tanto que en las áreas del Este (microcentro-río) sólo en el verano. La proporción de sitios infestados varió entre los 3 períodos de estudio, pero las zonas infestadas coincidieron espacialmente. Aunque se observó variación anual y espacial de la infestación, el patrón se repitió durante los 3 años de estudio sugiriendo una dinámica estable. Las áreas de la ciudad no infestadas presentaron las mayores densidades de población y de empleados, mientras que las infestadas durante los 3 períodos presentaron las menores densidades. Esto podría representar una atenuación del riesgo, ya que no coincide la mayor densidad de habitantes con la mayor infestación. El riesgo de transmisión desde el punto de vista del vector se concentraría entre enero y marzo y ocuparía el 50% de la superficie de la ciudad en la periferia.(AU)