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Journal ArticleDOI

Brugia malayi microfilariae (Nematoda: Filaridae) enhance the infectivity of Venezuelan equine encephalitis virus to Aedes mosquitoes (Diptera: Culicidae).

01 Nov 1999-Journal of Medical Entomology (Entomological Society of America)-Vol. 36, Iss: 6, pp 758-763
TL;DR: The contrasting effects of microfilarial enhancement of viral infectivity and MF-induced mortality in mosquitoes differed among mosquito species and were determined by the nature and consequences of MF penetration through the mosquito midgut, but not to differences in mosquito susceptibilities to parenterally introduced virus.
Abstract: We examined the potentially conflicting effects that microfilarial ( MF) enhancement of viral infectivity and MF-induced mortality in mosquitoes have on the vectorial capacity of Aedes aegypti (L.), Aedes triseriatus (Say), and Aedes taeniorhynchus (Wiedemann) for Venezuelan equine encephalitis virus (VEE) when mosquitoes feed on gerbils co-infected with Brugia malayi (Buckley). Groups of mosquitoes were fed on gerbils that were either dually infected (VEE plus B. malayi MF) or singly infected (VEE only). Mosquito mortality was recorded daily, and 5-8 d later, surviving mosquitoes were assayed for disseminated viral infection. The contrasting effects of MF enhancement and MF-induced mortality differed among mosquito species and were determined by the nature and consequences of MF penetration through the mosquito midgut, but not to differences in mosquito susceptibilities to parenterally introduced virus. In Ae. aegypti, MF-induced mortality was high and tended to eliminate any significant effect of MF enhancement. In Ae. triseriatus, MF-induced mortality was low, and feeding on dually infected hosts resulted in 9 times as many mosquitoes with disseminated viral infections as did feeding on singly-infected hosts. In Ae. taeniorhynchus, MF-induced mortality was extremely high, yet under our experimental conditions, feeding on a dually infected hosts resulted in nearly 30 times as many disseminated infections as did feeding on singly infected hosts. The final outcome on vectorial capacity depended on the specific combination of MF, virus, and mosquito species involved. Therefore, future efforts toward understanding MF enhancement should be directed toward mosquito-virus-parasite species combinations that occur together in nature.
Citations
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Journal ArticleDOI
TL;DR: The understanding of the interplay between mosquitoes and the immune system of their hosts is still in its infancy, but it is clear that there is great potential for exploiting this interplay in the control of mosquito‐borne diseases.
Abstract: The intimate contact between mosquitoes and the immune system of their hosts is generally not considered important because of the transient nature of mosquito feeding. However, when hosts are exposed to many feeding mosquitoes, they develop immune responses against a range of salivary antigens. Understanding the importance of these responses will provide new tools for monitoring vector populations and identifying individuals at risk of mosquito-borne diseases, and allow the development of novel methods for monitoring control and mosquito-release programmes. Antibodies targeting the mosquito midgut are also important in the development of mosquito vaccines. The feasibility of this approach has been demonstrated and future research opportunities are considered in this review. The potential impact of mosquito vaccines is also discussed. Our understanding of the interplay between mosquitoes and the immune system of their hosts is still in its infancy, but it is clear that there is great potential for exploiting this interplay in the control of mosquito-borne diseases.

77 citations

Journal ArticleDOI
TL;DR: A series of recombinant alphaviruses, based upon the genome of ONNV, designed for the expression of heterologous genes, that will be a valuable asset in parasite–mosquito interaction and interference research and to serve as tools for antimalaria studies.
Abstract: Arthropod-borne alphaviruses transmitted by mosquitoes almost exclusively use culicines; however, the alphavirus o'nyong-nyong (ONNV) has the unusual characteristic of being transmitted primarily by anopheline mosquitoes This unusual attribute makes ONNV a valuable tool in the characterization of mosquito determinants of infection as well as a useful expression system in Anopheles species We developed a series of recombinant alphaviruses, based upon the genome of ONNV, designed for the expression of heterologous genes The backbone genome is a full-length infectious cDNA clone of ONNV from which wild-type virus can be rescued Additional constructs are variants of the primary clone and contain the complete genome plus a duplicated subgenomic promoter element with a multiple cloning site for insertion of heterologous genes We inserted a green fluorescent protein (GFP) gene downstream of this promoter and used it to characterize infection and dissemination patterns of ONNV within An gambiae mosquitoes These experiments allowed us to identify atypical sites of initial infection and dissemination patterns in this mosquito species not frequently observed in comparable culicine infections The utility of these ONNVs for studies in anopheline mosquitoes includes the potential for identification of vector infection determinants and to serve as tools for antimalaria studies Viruses that can express a heterologous gene in a vector and rapidly and efficiently infect numerous tissues in An gambiae mosquitoes will be a valuable asset in parasite-mosquito interaction and interference research

68 citations


Cites background from "Brugia malayi microfilariae (Nemato..."

  • ...taeniorhynchus coinfected with microfilariae (Vaughan & Turell, 1996a; Vaughan et al., 1999)....

    [...]

  • ...Disseminated VEE and EEE virus infections were also found up to thirty times more frequently in Ae. taeniorhynchus coinfected with microfilariae (Vaughan & Turell, 1996a; Vaughan et al., 1999)....

    [...]

Journal ArticleDOI
TL;DR: The alterations in mosquito feeding propensity reported here would occur if parasites have been selected to make infected vertebrate hosts more attractive to mosquitoes, and infected mosquitoes are more likely to seek out new blood meals.
Abstract: Arthropod vectors of disease may encounter more than one infected host during the course of their lifetime. The consequences of super-infection to parasite development are rarely investigated, but may have substantial epidemiological and evolutionary consequences. Using a rodent malaria model system, behavioural avoidance of super-infection was tested by examining whether already-infected Anopheles stephensi mosquitoes were less responsive to new vertebrate hosts if they were infected. Additionally, a second dose of parasites was given to malaria-infected mosquitoes on a biologically realistic time scale to test whether it impeded the development of a first infection. No effect of a second infected blood meal on either the prevalence or parasite burden arising from a first was found. Furthermore, it was found that not only were infected mosquitoes more likely to take a second blood meal than their uninfected counterparts, they were disproportionately drawn to infected hosts. The alterations in mosquito feeding propensity reported here would occur if parasites have been selected to make infected vertebrate hosts more attractive to mosquitoes, and infected mosquitoes are more likely to seek out new blood meals. Although such a strategy might increase the risk of super-infection, this study suggests the cost to parasite development is not high and as such would be unlikely to outweigh the potential benefits of increasing the contact rate between the parasite's two obligate hosts.

58 citations


Cites background from "Brugia malayi microfilariae (Nemato..."

  • ...For example, in the laboratory, pathogen transmission can be enhanced when different parasite species co-occur in the same individual vector, a phenomenon that has been observed in some [1-4] but not all mosquito species that have been tested [1,4]....

    [...]

Journal ArticleDOI
TL;DR: Eleven species were evaluated from Florida to determine which of these species should be targeted for control should Rift Valley fever virus (RVFV) be detected in North America and how environmental factors affect transmission.
Abstract: We evaluated Aedes atlanticus Dyar and Knab, Aedes infirmatus Dyar and Knab, Aedes vexans (Meigen), Anopheles crucians Wiedemann, Coquillettidia perturbans (Walker), Culex nigripalpus Theobald, Mansonia dyari Belkin, Heinemann, and Page, and Psorophora ferox (Von Humboldt) from Florida to determine which of these species should be targeted for control should Rift Valley fever virus (RVFV) be detected in North America. Female mosquitoes that had fed on adult hamsters inoculated with RVFV were incubated for 7-21 d at 26 degrees C, then allowed to refeed on susceptible hamsters, and tested to determine infection, dissemination, and transmission rates. We also inoculated mosquitoes intrathoracically, held them for 7 d, and then allowed them to feed on a susceptible hamster to check for a salivary gland barrier. When exposed to hamsters with viremias > or = 10(7.6) plaque-forming units per milliliter of blood, at least some individuals in each of the species tested became infected; however, Cx. nigripalpus, An. crucians, and Ae. infirmatus were essentially incompetent vectors in the laboratory because of either a midgut escape or salivary gland barrier. Each of the other species should be considered as potential vectors and would need to be controlled if RVFV were introduced into an area where they were found. Additional studies need to be conducted with other geographic populations of these species and to determine how environmental factors affect transmission.

52 citations


Cites background from "Brugia malayi microfilariae (Nemato..."

  • ...Similar examples of microÞlarial enhancement have been shown with other mosquito and virus and Þlarial worm combinations (Turell et al. 1987, Vaughan et al. 1999)....

    [...]

Book ChapterDOI
TL;DR: Evidence indicates the existence of a salivary gland infection barrier in Anopheles stephensi and the basal lamina may prevent access to mosquito cell surface virus receptors and help explain why anopheline mosquitoes are relatively incompetent arbovirus transmitters when compared to culicines.
Abstract: Knowledge of the fate of an arbovirus in a mosquito is fundamental to understanding the mosquito’s competence to transmit the virus When a competent mosquito ingests viremic vertebrate blood, virus infects midgut epithelial cells and replicates, then disseminates to other tissues, including salivary glands and/or ovaries The virus is then transmitted to the next vertebrate host horizontally via bite and/or vertically to the mosquito’s offspring Not all mosquitoes that ingest virus become infected or, if infected, transmit virus Several “barriers” to arbovirus passage, and ultimately transmission, have been identified in incompetent or partially competent mosquitoes, including, among others, gut escape barriers and salivary gland infection barriers The extra-cellular basal lamina around the midgut epithelium and the basal lamina that surrounds the salivary glands may act as such barriers Midgut basal lamina pore sizes are significantly smaller than arboviruses and ultrastructural evidence suggests that midgut tracheae and tracheoles may provide a means for viruses to circumvent this barrier Further, immunocytochemical evidence indicates the existence of a salivary gland infection barrier in Anopheles stephensi The basal lamina may prevent access to mosquito cell surface virus receptors and help explain why anopheline mosquitoes are relatively incompetent arbovirus transmitters when compared to culicines

49 citations

References
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Journal ArticleDOI
TL;DR: It is suggested that certain key parameters determine whether dual virus/mf host infections will enhance arboviral infectivity to mosquitoes, including species differences in the capacity of mf to penetrate the mosquito midgut, the amount of virus passing into the hemocoel during mf penetration, and the innate susceptibility of mosquitoes to hemocoelsomically introduced virus.
Abstract: When mosquitoes feed on a vertebrate host that is infected concurrently with virus and microfilariae (mf), both pathogens are ingested. If mf penetrate the mosquito midgut, a small portion of the ingested virus may disseminate directly into the mosquito hemocoel. This phenomenon, termed microfilarial enhancement of arboviral transmission, has the potential to enhance the infectivity of arboviruses to mosquitoes. We investigated whether concurrent ingestion of Brugia mf and eastern equine encephalitis virus would enhance the infectivity and subsequent transmissibility of the virus by Aedes mosquitoes. Trials with Ae. triseriatus and B. pahangi mf indicated that microfilarial enhancement was dose dependent. Both a sufficient number of penetrating mf and a sufficient viremia were required for enhancement to occur. Furthermore, studies with B. malayi and three species of Aedes indicated that under comparable conditions of host viremia and microfilaremia, microfilarial enhancement occurred in some mosquito species (i.e., Ae. aegypti and Ae. taeniorhynchus) but not in others (Ae. triseriatus). We suggest that certain key parameters determine whether dual virus/mf host infections will enhance arboviral infectivity to mosquitoes. These include species differences in the capacity of mf to penetrate the mosquito midgut, the amount of virus passing into the hemocoel during mf penetration, and the innate susceptibility of mosquitoes to hemocoelomically introduced virus.

27 citations

Journal ArticleDOI
TL;DR: In this paper, concurrent ingestion of dengue 2 virus and microfilariae of Brugia malayi would increase viral infection and dissemination rates in Aedes aegypti.
Abstract: : We investigated whether concurrent ingestion of dengue 2 virus and microfilariae of Brugia malayi would increase viral infection and dissemination rates in Aedes aegypti. Infection rates were similar in mosquitoes that ingested virus along or both virus and microfilariae concurrently. However, viral dissemination rates, as determined by recovery of dengue virus from both legs and bodies separately, were significantly greater in mosquitoes that ingested both agents concurrently than in those that ingested virus alone. This study confirms that vectorial capacity of a natural vector of an arbovirus may be enhanced by the concurrent ingestion of microfilariae.

26 citations

Journal Article
TL;DR: It is concluded that refractoriness of Ae.
Abstract: Studies were conducted to compare early phenomena associated with W. bancrofti infection and further development in the filaria vector Culex pipiens and the refractory mosquito Aedes caspius. Ingestion rates evaluated immediately after simultaneous feeding on an infected human were 69.1% for 43 Cx. pipiens and 35.7% for 28 Ae. caspius. The observed number of mf ingested by either mosquito did not vary significantly (2.7 +/- 1.4, and 2.3 +/- 0.9, respectively) and, based on the size of the blood meal ingested (2.8 and 2.3 microliters respectively), a two-fold mf concentration factor was recorded for both species. Blood ingested by Cx. pipiens (N = 16) and Ae. caspius (N = 10) clotted within 120 and 90 min post-feeding respectively. The time difference observed, however, did not affect significantly the rates of migration into the hemocele (56 and 67% respectively). Comparison of initial infection rates with those obtained after the extrinsic incubation period of the parasite was completed, indicated that the proportion of infected Cx. pipiens was reduced by 3.9% and that of Ae. caspius by 30.0%. Furthermore, the observed infectivity ratio of 265 Cx. pipiens that had an infective blood meal was 0.74 and only 0.009 for 70 Ae. caspius. It is concluded that refractoriness of Ae. caspius to W. bancrofti is expressed through the feeding mechanism itself, by severely limiting the mf ingestion rate, and through physiological processes that inhibited the development of ingested worms.

24 citations

Journal ArticleDOI
TL;DR: Brugia beaveri sp.
Abstract: Brugia beaveri sp. n., from the lymph nodes, skin, and carcass of the raccoon (Procyon lotor) in Louisiana is described. This is the first Brugia species to be reported from mammals in North America. It differs from the six other described species of the genus generally in the smaller body size of the female, the size and structure of the spicules, and the larger microfilaria which has a distinctively long cephalic space. A sheathed microfilaria of the Brugia type was first discovered in the United States in 1953 in a thick blood film from a raccoon (Procyon lotor) from Lafitte, Louisiana (Beaver, personal communication). A similar microfilaria was found in the blood of a bobcat (Lynx rufus) in Florida in 1960 (Orihel, personal communication). In neither case was the adult worm recovered. In February 1963, sheathed microfilariae were again found in raccoons in Louisiana. The adult worm was subsequently recovered and is here described as a new species of the genus Brugia Buckley, 1960. It is the first species of this genus to be described from the United States, the second reported from the Western Hemisphere (Orihel, 1963). MATERIALS AND METHODS Seven raccoons were collected from an area near Rosedale, Louisiana, approximately 90 miles northwest of New Orleans. As six of the animals had been captured alive, their blood could be examined repeatedly before they were necropsied. Microfilariae in blood samples were fixed in 2% formalin. A dilute Azur II solution was added to formalin-fixed microfilariae to bring out morphologic details. Microfilariae were also studied in thick and thin blood films. Thick films were air dried, dehemoglobinized in 0.85% saline, fixed in hot (60 C) 70% alcohol, and stained with dilute Delafield's hematoxylin. Thin blood films were Received for publication 8 August 1963. * This study was supported in part by grants 2E-2 and AI-04919-01 from the National Institutes of Health, Public Health Service. fixed in methyl alcohol and stained 1 hr with Giemsa (2% in pH 7.0 buffered water). Adult worms were recovered by soaking the skin, carcass, and lymphatic tissues in warm 0.85% saline solution as described by Dunn (1931). In the examination of one raccoon in which seven worms were recovered the soaking fluid was, in addition, filtered through coarse filter paper; the material on the surface of the filter paper was then washed into a large petri dish and examined with a dissecting microscope. Adult worms were fixed in glacial acetic acid (Berland, 1961), transferred to 70% alcohol containing 5% glycerine, and then gradually brought into pure glycerine, the medium in which they were studied. All drawings were made with the aid of a camera lucida. Brugia beaveri sp. n. Brugia microfilariae were found in five of the seven raccoons examined. Microfilariae of a Dipetalonema sp. were found in six and those of Dirofilaria tenuis in all of the animals. Adult worms of the new Brugia species were recovered from only two. However, one of the seven raccoons was dead when brought into the laboratory and, although it had Brugia microfilariae in the blood, it was not examined for adult worms. From one raccoon a single male was recovered from the saline in which the skin had soaked. From the other, two complete males, a broken male, three complete females, and a broken female were recovered. One male was recovered from an axillary lymph node and another from a popliteal node; all other specimens were found in the saline in which the skin and carcass had been immersed.

23 citations