Vector-borne Transmission Research Articles

Integrating Community Ecology into Models of Vector-Borne Virus Transmission.

Vector-borne plant viruses are a diverse and dynamic threat to agriculture with hundreds of economically damaging viruses and insect vector species. Mathematical models have greatly increased our understanding of how alterations of vector life history and host-vector-pathogen interactions can affect virus transmission. However, insect vectors also interact with species such as predators and competitors in food webs, and these interactions affect vector population size and behaviors in ways that mediate virus transmission. Studies assessing how species' interactions affect vector-borne pathogen transmission are limited in both number and scale, hampering the development of models that appropriately capture community-level effects on virus prevalence. Here, we review vector traits and community factors that affect virus transmission, explore the existing models of vector-borne virus transmission and areas where the principles of community ecology could improve the models and management, and finally evaluate virus transmission in agricultural systems. We conclude that models have expanded our understanding of disease dynamics through simulations of transmission but are limited in their ability to reflect the complexity of ecological interactions in real systems. We also document a need for experiments in agroecosystems, where the high availability of historical and remote-sensing data could serve to validate and improve vector-borne virus transmission models.

Lake Sinai virus is a diverse, globally distributed but not emerging multi-strain honeybee virus.

Domesticated honeybees and wild bees are some of the most important beneficial insects for human and environmental health, but infectious diseases pose a serious risk to these pollinators, particularly following the emergence of the ectoparasitic mite Varroa destructor as a viral vector. The acquisition of this novel viral vector from the Asian honeybee Apis ceranae has fundamentally changed viral epidemiology in its new host, the western honeybee A. mellifera. While the recently discovered Lake Sinai Viruses (LSV) have been associated with weak honeybee colonies, they have not been associated with vector-borne transmission. By combining a large-scale multi-year survey of LSV in Chinese A. mellifera and A. cerana honeybee colonies with globally available LSV-sequence data, we investigate the global epidemiology of this virus. We find that globally distributed LSV is a highly diverse multi-strain virus, which is predominantly associated with the western honeybee A. mellifera. In contrast to the vector-borne deformed wing virus, LSV is not an emerging disease. Instead, demographic reconstruction and strong global and local population structure indicates that it is a highly variable multi-strain virus in a stable association with its main host, the western honeybee. Prevalence patterns in China suggest a potential role for migratory beekeeping in the spread of this pathogen, demonstrating the potential for disease transmission with the man-made transport of beneficial insects.

Humidity - The overlooked variable in the thermal biology of mosquito-borne disease.

Vector-borne diseases cause significant financial and human loss, with billions of dollars spent on control. Arthropod vectors experience a complex suite of environmental factors that affect fitness, population growth and species interactions across multiple spatial and temporal scales. Temperature and water availability are two of the most important abiotic variables influencing their distributions and abundances. While extensive research on temperature exists, the influence of humidity on vector and pathogen parameters affecting disease dynamics are less understood. Humidity is often underemphasized, and when considered, is often treated as independent of temperature even though desiccation likely contributes to declines in trait performance at warmer temperatures. This Perspectives explores how humidity shapes the thermal performance of mosquito-borne pathogen transmission. We summarize what is known about its effects and propose a conceptual model for how temperature and humidity interact to shape the range of temperatures across which mosquitoes persist and achieve high transmission potential. We discuss how failing to account for these interactions hinders efforts to forecast transmission dynamics and respond to epidemics of mosquito-borne infections. We outline future research areas that will ground the effects of humidity on the thermal biology of pathogen transmission in a theoretical and empirical framework to improve spatial and temporal prediction of vector-borne pathogen transmission.

Marginal risk of domestic vector-borne Trypanosoma cruzi transmission after improved vector control of Triatoma infestans across a rural-to-urban gradient in the Argentine Chaco

The interruption of domestic vector-borne transmission of Trypanosoma cruzi in the Americas remains one of the main goals of the World Health Organization 2021–2030 road map for neglected tropical diseases. We implemented a longitudinal intervention program over 2015–2022 to suppress (peri)domestic Triatoma infestans in the municipality of Avia Terai, Chaco Province, Argentina and found that house infestation (3851 houses inspected) and triatomine abundance decreased over the first 2 years post-intervention (YPI), and remained stable thereafter associated to moderate pyrethroid resistant foci. Here we assessed selected components of transmission risk after interventions across the rural-to-urban gradient. We used multistage random sampling to select a municipality-wide sample of T. infestans. We examined 356 insects collected in 87 houses for T. cruzi infection using kDNA-PCR and identified their bloodmeal sources using an indirect ELISA. The overall prevalence of T. cruzi infection post-intervention was 1.7% (95% CI 0.7–3.6). Few houses (5.7%) (95% CI 2.5–12.8) harbored infected triatomines across the gradient. Infected triatomines were found in 5 peri‑urban or rural dwellings over 1–4 years post-intervention. No infected insect was found in the urban area. The human blood index decreased from 66.2 at baseline to 42.8 at 1YPI and then increased to 92.9 at 4–5 YPI in the few infested domiciles detected. The percentage of houses with human-fed bugs displayed a similar temporal trend. Our results indicate marginal risks of domestic vector-borne transmission across the district after implementation of the intervention program. Ensuring sustainable vector surveillance coupled with human etiological diagnosis and treatment in hiperendemic areas like the Gran Chaco region, is urgently needed.252 words

Wind-assisted high-altitude dispersal of mosquitoes and other insects in East Africa.

Knowledge of insect dispersal is relevant to the control of agricultural pests, vector-borne transmission of human and veterinary pathogens, and insect biodiversity. Previous studies in a malaria endemic area of the Sahel region in West Africa revealed high-altitude, long-distance migration of insects and various mosquito species. The objective of the current study was to assess whether similar behavior is exhibited by mosquitoes and other insects around the Lake Victoria basin region of Kenya in East Africa. Insects were sampled monthly from dusk to dawn over 1 year using sticky nets suspended on a tethered helium-filled balloon. A total of 17,883 insects were caught on nets tethered at 90, 120, and 160 m above ground level; 818 insects were caught in control nets. Small insects (<0.5 cm, n = 15,250) were predominant regardless of height compared with large insects (>0.5 cm, n = 2,334) and mosquitoes (n = 299). Seven orders were identified; dipteran was the most common. Barcoding molecular assays of 184 mosquitoes identified 7 genera, with Culex being the most common (65.8%) and Anopheles being the least common (5.4%). The survival rate of mosquitoes, experimentally exposed to high-altitude overnight, was significantly lower than controls maintained in the laboratory (19% vs. 85%). There were no significant differences in mosquito survival and oviposition rate according to capture height. These data suggest that windborne dispersal activity of mosquito vectors of malaria and other diseases occurs on a broad scale in sub-Saharan Africa.

Northern and central Chile still free of emerging flaviviruses in mosquitoes (Diptera: Culicidae).

Geographic isolation and strict control limits in border areas have kept Chile free from various pathogens, including Flavivirus. However, the scenario is changing mainly due to climate change, the reintroduction of more aggressive mosquitoes, and the great wave of migration of people from endemic countries in recent years. Hence, it is necessary to surveillance mosquitoes to anticipate a possible outbreak in the population and take action to control it. This study aimed to investigate the presence of Flavivirus RNA by molecular tools with consensus primers in mosquitoes collected in the extreme north and central Chile. From 2019 to 2021, a prospective study was carried out in localities of Northern and part of Central Chile. Larvae, pupae, and adults of mosquitoes were collected in rural and urban sites in each locality. The collected samples were pooled by species and geographical location and tested using RT-PCR and RT-qPCR to determine presence of Flavivirus. 3085 specimens were collected, the most abundant specie Culex quinquefasciatus in the North and Aedes (Ochlerotatus) albifasciatus in the Center of Chile. Both genera are associated with Flavivirus transmission. However, PCR and RT-PCR did not detect Flavivirus RNA in the mosquitoes studied. These negative results indicate we are still a free Flavivirus country, which is reaffirmed by the non-existence of endemic human cases. Despite this, routine surveillance of mosquitoes and the pathogens they carry is highly recommended to evaluate each area-specific risk of vector-borne transmission.

Genomic analysis of two phlebotomine sand fly vectors of Leishmania from the New and Old World.

Phlebotomine sand flies are of global significance as important vectors of human disease, transmitting bacterial, viral, and protozoan pathogens, including the kinetoplastid parasites of the genus Leishmania, the causative agents of devastating diseases collectively termed leishmaniasis. More than 40 pathogenic Leishmania species are transmitted to humans by approximately 35 sand fly species in 98 countries with hundreds of millions of people at risk around the world. No approved efficacious vaccine exists for leishmaniasis and available therapeutic drugs are either toxic and/or expensive, or the parasites are becoming resistant to the more recently developed drugs. Therefore, sand fly and/or reservoir control are currently the most effective strategies to break transmission. To better understand the biology of sand flies, including the mechanisms involved in their vectorial capacity, insecticide resistance, and population structures we sequenced the genomes of two geographically widespread and important sand fly vector species: Phlebotomus papatasi, a vector of Leishmania parasites that cause cutaneous leishmaniasis, (distributed in Europe, the Middle East and North Africa) and Lutzomyia longipalpis, a vector of Leishmania parasites that cause visceral leishmaniasis (distributed across Central and South America). We categorized and curated genes involved in processes important to their roles as disease vectors, including chemosensation, blood feeding, circadian rhythm, immunity, and detoxification, as well as mobile genetic elements. We also defined gene orthology and observed micro-synteny among the genomes. Finally, we present the genetic diversity and population structure of these species in their respective geographical areas. These genomes will be a foundation on which to base future efforts to prevent vector-borne transmission of Leishmania parasites.

Ecological predictors of mosquito population and arbovirus transmission synchrony estimates.

Quantifying synchrony in species population fluctuations and determining its driving factors can inform multiple aspects of ecological and epidemiological research and policy decisions. We examined seasonal mosquito and arbovirus surveillance data collected in Connecticut, United States from 2001 to 2020 to quantify spatial relationships in 19 mosquito species and 7 arboviruses timeseries accounting for environmental factors such as climate and land cover characteristics. We determined that mosquito collections, on average, were significantly correlated up to 10 km though highly variable among the examined species. Few arboviruses displayed any synchrony and significant maximum correlated distances never exceeded 5 km. After accounting for distance, mixed effects models showed that mosquito or arbovirus identity explained more variance in synchrony estimates than climate or land cover factors. Correlated mosquito collections up to 10-20 km suggest that mosquito control operations for nuisance and disease vectors alike must expand treatment zones to regional scales for operations to have population-level impacts. Species identity matters as well, and some mosquito species will require much larger treatment zones than others. The much shorter correlated detection distances for arboviruses reinforce the notion that focal-level processes drive vector-borne pathogen transmission dynamics and risk of spillover into human populations.

First Report of Swinepox in a Wild Boar in Italy: Pathologic and Molecular Findings.

Swinepox virus (SWPV) is responsible for sporadic acute poxvirus infections in swine worldwide, causing a pathognomonic eruptive proliferative dermatitis. Beside direct and congenital transmission, the pig louse Haematopinus suis acts as a mechanical vector and favors virus infection through skin lesions. Infections are generally described in domestic pigs, while only a few cases have been reported in wild boars, in Austria and Germany. In September 2022, SWPV infection was suspected at post-mortem examination of a wild boar piglet with characteristic lesions in Liguria, Northwest Italy. The piglet was heavily parasitized by swine lice (H. suis). SWPV was then confirmed by histological and molecular analyses. Possible viral co-infections were also investigated (African swine fever virus, classical swine fever virus, parvovirus, circovirus, Aujeszky's disease virus and hepatitis E virus). This article describes gross and histopathologic features of SWPV infection, differential diagnosis, and potential vector-borne transmission to domestic pigs, presenting a brief review of the literature on the topic. SWPV infection is reported in wild boars in Italy for the first time. The finding of SWPV in a wild boar in an area with a very limited pig population may suggest the existence of a "wildlife cycle" in the area. Further investigations are needed to understand the real risk of transmission of SWPV to domestic pigs as well as the role of other arthropod vectors.

Two needs, one deed: optimising malaria outcomes through mangrove interventions in ghana

Uncertainties around deforestation influences on vector-borne disease transmission and prevalence means that varieties of forest management techniques must be included in evaluations of health management policies.This commentary presents ideas for improving malaria management policy in marginal communities, where both elimination of health inequalities and mangrove restoration are desirable interventions. It relies on results of novel application of Qualitative Comparative Analysis (QCA) on causal relationships influencing malaria incidence in Ghana. Restoration-related mangrove conditions were investigated alongside the predominant vector control strategies.QCA findings show ecological conditions of temperature reduction, improved water quality, arrest of mangrove land conversion and presence of biological control agents combining diversely to amplify impacts of personal protective measures, especially insecticide treated net usage. The viewpoint is that ecosystem and health mangers must collaborate in capacity building, trend monitoring and creation of new knowledge to ensure that cross-sector benefits are sufficiently addressed in policy reforms. Further research required to reveal how mangrove presence and/or restoration affect malaria parasite prevalence and transmission dynamics in mangrove mosquitoes, to identify pathways for modifying and tailoring vector-control strategies to suit needs in mangrove communities.QCA could be a valuable causal inference technique for bringing clarity to nature-health relationships because it makes room for analysis of 'conjunctural' impacts of non-nature conditions.

Annals for Hospitalists - February 2023

Annals for Hospitalists - February 2023

Host-pathogen interaction in arthropod vectors: Lessons from viral infections.

Haematophagous arthropods can harbor various pathogens including viruses, bacteria, protozoa, and nematodes. Insects possess an innate immune system comprising of both cellular and humoral components to fight against various infections. Haemocytes, the cellular components of haemolymph, are central to the insect immune system as their primary functions include phagocytosis, encapsulation, coagulation, detoxification, and storage and distribution of nutritive materials. Plasmatocytes and granulocytesare also involved in cellular defense responses. Blood-feeding arthropods, such as mosquitoes and ticks, can harbour a variety of viral pathogens that can cause infectious diseases in both human and animal hosts. Therefore, it is imperative to study the virus-vector-host relationships since arthropod vectors are important constituents of the ecosystem. Regardless of the complex immune response of these arthropod vectors, the viruses usually manage to survive and are transmitted to the eventual host. A multidisciplinary approach utilizing novel and strategic interventions is required to control ectoparasite infestations and block vector-borne transmission of viral pathogens to humans and animals. In this review, we discuss the arthropod immune response to viral infections with a primary focus on the innate immune responses of ticks and mosquitoes. We aim to summarize critically the vector immune system and their infection transmission strategies to mammalian hosts to foster debate that could help in developing new therapeutic strategies to protect human and animal hosts against arthropod-borne viral infections.

Close-kin mark-recapture methods to estimate demographic parameters of mosquitoes.

Close-kin mark-recapture (CKMR) methods have recently been used to infer demographic parameters such as census population size and survival for fish of interest to fisheries and conservation. These methods have advantages over traditional mark-recapture methods as the mark is genetic, removing the need for physical marking and recapturing that may interfere with parameter estimation. For mosquitoes, the spatial distribution of close-kin pairs has been used to estimate mean dispersal distance, of relevance to vector-borne disease transmission and novel biocontrol strategies. Here, we extend CKMR methods to the life history of mosquitoes and comparable insects. We derive kinship probabilities for mother-offspring, father-offspring, full-sibling and half-sibling pairs, where an individual in each pair may be a larva, pupa or adult. A pseudo-likelihood approach is used to combine the marginal probabilities of all kinship pairs. To test the effectiveness of this approach at estimating mosquito demographic parameters, we develop an individual-based model of mosquito life history incorporating egg, larva, pupa and adult life stages. The simulation labels each individual with a unique identification number, enabling close-kin relationships to be inferred for sampled individuals. Using the dengue vector Aedes aegypti as a case study, we find the CKMR approach provides unbiased estimates of adult census population size, adult and larval mortality rates, and larval life stage duration for logistically feasible sampling schemes. Considering a simulated population of 3,000 adult mosquitoes, estimation of adult parameters is accurate when ca. 40 adult females are sampled biweekly over a three month period. Estimation of larval parameters is accurate when adult sampling is supplemented with ca. 120 larvae sampled biweekly over the same period. The methods are also effective at detecting intervention-induced increases in adult mortality and decreases in population size. As the cost of genome sequencing declines, CKMR holds great promise for characterizing the demography of mosquitoes and comparable insects of epidemiological and agricultural significance.

Domestic Triatoma spp. Infections with Trypanosoma cruzi, Household Infestations, and Molecular Identification in Oaxaca, México.

In Latin America, Mexico is the country with the second highest annual estimated number of Chagas disease cases, caused by Trypanosoma cruzi, due to vector-borne transmission. The state of Oaxaca is the location of the first documented human cases of Chagas disease in Mexico and contained the highest T. cruzi seropositive rate (3.5%) from blood donors. Here, entomological surveys, from 2017 to 2019, were conducted to collect triatomines in 124 villages of 60 municipalities. Four principal domestic Triatoma spp. (Hemiptera: Triatominae), Triatoma phyllosoma, T. barberi, T. mazzotti, and T. dimidiata, of Oaxaca, Mexico were identified by morphology and molecular analysis of the barcode region of the cytochrome oxidase 1 (cox1 or COI or CO1) gene. A total of 41 out of 83 T. phyllosoma specimens examined by microscopy were positive for T. cruzi (49%), 49 out of 171 for T. barberi (28%), 31 out of 177 for T. mazzotti (17%), and none out of 10 for T. dimidiata (0%). Overall, the infestation index was 3.1% of households containing at least one triatomine; the crowding index was a mean of two Triatoma spp./household; and the colonization index was 0.38 for households based on presence of nymphs. Geographical distribution of triatomines in Oaxaca at the municipality level and endophilic behavior is also reported. Precise identification, endophilic habits, and infection rates of these triatomines are paramount for vector control programs of the Ministry of Health of Oaxaca and beyond.

Evidence of Lumpy Skin Virus DNA in Blood-Feeding Flies During Outbreaks in Russia in 2018-2019

Abstract In this study we report the testing of blood-feeding and synanthropic flies captured near animals affected by lumpy skin disease virus (LSDV) in Russia during the outbreaks in the Kurgan region in 2018 and Saratov region in 2019. The insects of interest were the stable fly Stomoxys calcitrans, Tabanidae horse flies, Culicoides midges and the house fly Musca domestica examined as individuals or pools. The obtained findings demonstrate that viral DNA was found in pools of S.calcitrans and M. domestica and in the head and abdomen of stable flies. This is the first report of LSDV DNA detection in Tabanidae flies from the field. The presented data are envisaged to help further guide the search for putative vectors of LSDV in different climatic regions and interpret laboratory-controlled experiments on vector-borne transmission of LSDV.

Vector microbiome: will global climate change affect vector competence and pathogen transmission?

Vector-borne diseases are among the greatest causes of human suffering globally. Several studies have linked climate change and increasing temperature with rises in vector abundance, and in the incidence and geographical distribution of diseases. The microbiome of vectors can have profound effects on how efficiently a vector sustains pathogen development and transmission. Growing evidence indicates that the composition of vectors' gut microbiome might change with shifts in temperature. Nonetheless, due to a lack of studies on vector microbiome turnover under a changing climate, the consequences for vector-borne disease incidence are still unknown. Here, we argue that climate change effects on vector competence are still poorly understood and the expected increase in vector-borne disease transmission might not follow a relationship as simple and straightforward as past research has suggested. Furthermore, we pose questions that are yet to be answered to enhance our current understanding of the effect of climate change on vector microbiomes, competence, and, ultimately, vector-borne diseases transmission.

Field Evaluation of Novel Spatial Repellent Controlled Release Devices (CRDs) against Mosquitoes in an Outdoor Setting in the Northern Peruvian Amazon.

U.S. military troops are exposed to mosquito-borne pathogens when deployed to endemic regions. Personal protective measures such as permethrin-treated uniforms and dermal repellents are the cornerstones of mosquito-borne disease prevention for the U.S. military. These measures have limitations and additional personal protection tools, such as spatial repellent devices to decrease the risk of vector-borne pathogen transmission, are required. Novel spatial repellent controlled-release devices formulated with metofluthrin were evaluated in an outdoor setting in the northern Amazon of Peru to evaluate performance under field conditions. The metofluthrin emitting devices lowered the number of mosquitoes captured in protected human landing collections (HLC) compared to blank devices, although there were effect differences between Anopheles spp. and species in other mosquito genera. A computational-experimental model was developed to correlate HLC and active ingredient (AI) concentrations as a function of time and space. Results show a strong correlation between the released AI and the decrease in HLC. This model represents the first effort to obtain a predictive analytical tool on device performance using HLC as the entomological endpoint.

Patterns and Ecological Mechanisms of Tick-Borne Disease Exposure Risk in Acadia National Park, Mount Desert Island, Maine, United States.

National parks are unique and significant vector-borne pathogen transmission settings, engaging over 300 million people in outdoor recreation per year. In this study, we integrated vector surveys and ecological habitat feature data in spatial models to characterize tick-borne disease exposure risk in Acadia National Park (ANP), Maine. To determine the broad-scale patterns of blacklegged tick Ixodes scapularis Say (Acari: Ixodidae) densities in ANP, we conducted host-seeking tick collections at 114 sites across the park over two years. Using these tick survey data and geospatial landscape feature data (i.e., land cover, elevation, forest patch size, and aspect) we developed a random forest model of nymphal tick density. We found that host-seeking tick density varies significantly across the park and is particularly high in areas characterized by deciduous forest cover and relatively low elevation. To explore potential fine-scale ecological drivers of tick density spatial patterns, we quantified microclimate conditions, host activity, and vegetation characteristics at a subset of 19 sites. We identified significant differences in microclimate conditions but not host activity or vegetation metrics across broad-scale landscape feature classes. Mean temperature and mean humidity were correlated to nymphal densities and therefore may provide a mechanistic link between landscape features and blacklegged tick densities. Finally, we detected multiple tick-borne pathogens in both ticks and small mammals sampled in ANP, including Borrelia burgdorferi, Babesia microti, and Anaplasma phagocytophilum. Our findings demonstrate the value of using ecological metrics to estimate vector-borne disease exposure risk and provide insight into habitat characteristics that may drive tick-borne disease exposure risk.

Evolutionary consequences of vector-borne transmission: how using vectors shapes host, vector and pathogen evolution.

Transmission mode is a key factor that influences host–parasite coevolution. Vector-borne pathogens are among the most important disease agents for humans and wildlife due to their broad distribution, high diversity, prevalence and lethality. They comprise some of the most important and widespread human pathogens, such as yellow fever, leishmania and malaria. Vector-borne parasites (in this review, those transmitted by blood-feeding Diptera) follow unique transmission routes towards their vertebrate hosts. Consequently, each part of this tri-partite (i.e. parasite, vector and host) interaction can influence co- and counter-evolutionary pressures among antagonists. This mode of transmission may favour the evolution of greater virulence to the vertebrate host; however, pathogen–vector interactions can also have a broad spectrum of fitness costs to the insect vector. To complete their life cycle, vector-borne pathogens must overcome immune responses from 2 unrelated organisms, since they can activate responses in both vertebrate and invertebrate hosts, possibly creating a trade-off between investments against both types of immunity. Here, we assess how dipteran vector-borne transmission shapes the evolution of hosts, vectors and the pathogens themselves. Hosts, vectors and pathogens co-evolve together in a constant antagonistic arms race with each participant's primary goal being to maximize its performance and fitness.

Understanding pathogen survival and transmission by arthropod vectors to prevent human disease.

Many endemic poverty-associated diseases, such as malaria and leishmaniasis, are transmitted by arthropod vectors. Pathogens must interact with specific molecules in the vector gut, the microbiota, and the vector immune system to survive and be transmitted. The vertebrate host, in turn, is infected when the pathogen and vector-derived factors, such as salivary proteins, are delivered into the skin by a vector bite. Here, we review recent progress in our understanding of the biology of pathogen transmission from the human to the vector and back, from the vector to the host. We also highlight recent advances in the biology of vector-borne disease transmission, which have translated into additional strategies to prevent human disease by either reducing vector populations or by disrupting their ability to transmit pathogens.