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.
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TL;DR: Results indicated that, over the 14-year simulation period, mf-induced acceleration of the EIP would generate more frequent (but not necessarily more severe) epidemics.
Abstract: Concurrent ingestion of microfilariae (mf) and arboviruses by mosquitoes can enhance the transmission of virus compared with when virus is ingested alone. We studied the effect of mf enhancement on the extrinsic incubation period (EIP) of dengue 1 virus within Aedes aegypti mosquitoes by feeding mosquitoes on blood that either contained virus plus Brugia malayi mf or virus only. Mosquitoes were sampled over time to determine viral dissemination rates. Co-ingestion of mf and virus reduced viral EIP by over half. We used the computer simulation program, DENSiM, to compare the predicted patterns of dengue incidence that would result from such a shortened EIP versus the EIP derived from the control (i.e., virus only) group of mosquitoes. Results indicated that, over the 14-year simulation period, mf-induced acceleration of the EIP would generate more frequent (but not necessarily more severe) epidemics. Potential interactions between arboviruses and hematozoans deserve closer scrutiny.
10 citations
TL;DR: Investigation of the establishment and rapid spread of West Nile virus (WNV) across the mid-western United States found that mosquitoes, WNV, and passerine MF do interact in nature, and closer attention should be paid to the potential of MF to enhance mosquito transmission of arboviruses.
Abstract: Vertebrate reservoirs of arboviruses are often infected with microfilariae (MF). Laboratory studies have shown that MF can enhance the infectivity of arboviruses to mosquitoes. Soon after being ingested, MF penetrate the mosquito midgut. If the host blood also contains virus (i.e., vertebrate is dually infected), penetrating MF may introduce virus into the hemocoel. This can transform otherwise virus-incompetent mosquito species into virus-competent species and simultaneously accelerate viral development, allowing mosquitoes to transmit virus sooner than normal. This phenomenon is termed microfilarial enhancement of arboviral transmission. The prevalence of MF is very high in many passerine populations in North America. Therefore, we investigated if microfilarial enhancement could have facilitated the establishment and rapid spread of West Nile virus (WNV) across the mid-western United States. Our investigations revealed that mosquitoes, WNV, and passerine MF do interact in nature because; 1) 17% of 54 common grackles (Quiscalus quiscula L.), 8% of 26 American robins (Turdus migratorius L.), and 33% of three eastern kingbirds (Tyrannus tyrannus L.) were concurrently microfilaremic and seropositive to WNV; 2) feeding activities of mosquitoes overlapped temporally with the appearance of MF in the blood of common grackles; 3) mosquitoes fed on common grackles and American robins in nature; and 4) mosquito ingestion of two taxonomically distant species of passerine MF (i.e., Chandlerella quiscali and Eufilaria spp.) resulted in penetration of mosquito midguts. To estimate the theoretical effect that MF enhancement could have on WNV transmission in areas of high MF prevalence, vectorial capacity values were calculated for Culex mosquitoes feeding on common grackles, whereby MF enhancement was either invoked or ignored. For Cx. pipiens, vectorial capacity increased over three-fold when potential effects of MF were included in the calculations. For Cx. tarsalis, the effect was less (i.e., 1.4-fold increase). Closer attention should be paid to the potential of MF to enhance mosquito transmission of arboviruses.
9 citations
Cites background or methods or result from "Brugia malayi microfilariae (Nemato..."
...…this might seem low, it is comparable to penetration intensities reported in two previous trials (means ranged from 1 to 3 MF) wherein three Aedes spp. mosquitoes were fed on gerbils concurrently infected with Brugia spp. MF and different arboviruses (Vaughan and Turell 1996, Vaughan et al. 1999)....
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...…of MF and arboviruses by mosquitoes and biting midges can result in signiÞcantly greater infectivity of the arbovirus than when the same dose of arbovirus is ingested alone (Mellor and Boorman 1980; Turell et al. 1984, 1987; Zytoon et al. 1993; Vaughan and Turell 1996; Vaughan et al. 1999)....
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...Thus, a mosquito species does not have to be a competent vector for the Þlarioid parasite to have a potential role in MF enhancement (Vaughan et al. 1999)....
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...…phenomenon of MF enhancement was described over 30 yr ago and has been demonstrated by three different research groups for at least nine different vector-arbovirus-MF model systems (Mellor and Boorman 1980; Turell et al. 1984, 1987; Zytoon et al. 1993; Vaughan and Turell 1996; Vaughan et al. 1999)....
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TL;DR: The potential exists that M. ozzardi mf had the ability to penetrate the midgut of Aedes aegypti (L.) and thus play a potential role in the enhancement of dengue transmission.
Abstract: When virus and microfilariae are ingested concurrently by a mosquito, microfilariae (mf) may penetrate the mosquito midgut and introduce virus directly into the mosquito hemocoel, allowing mosquitoes to become infectious much sooner than normal and enhancing transmission of viruses by mosquitoes. Mansonella ozzardi (Manson) is a benign filarial nematode parasite of humans in Latin America and is transmitted by black flies (Diptera: Simuliidae) and biting midges (Diptera: Ceratopogonidae). Because M. ozzardi and dengue are sympatric, we wanted to know whether M. ozzardi mf had the ability to penetrate the midgut of Aedes aegypti (L.) (Diptera: Culicidae) and thus play a potential role in the enhancement of dengue transmission. To test this, the F1 progeny from locally collected Ae. aegypti were fed on M. ozzardi-infected human males in an endemic village in northern Trinidad. Mosquitoes were dissected at various times after feeding and examined for mf in the midguts and thoraces. Microfilariae penetrated the midguts of 43% of 63 mosquitoes that ingested mf. Overall, 11% of mf penetrated the midgut by 17 h after being ingested. The intensity of midgut penetration was positively correlated to the numbers of mf ingested. Because midgut penetration is a key requirement for mf enhancement to occur, the potential exists that M. ozzardi could be involved in the enhancement of dengue virus transmission.
9 citations
Cites background from "Brugia malayi microfilariae (Nemato..."
...This was illustrated in a study examining the ability of co-ingested mf ofBrugiamalayi to affect the ability ofOchlerotatus taeniorhynchus (Wiedemann) (Diptera: Culicidae) transmit Venezuelan equine encephalomyelitis virus (family Togaviridae, genus Alphavirus, VEEV) (Vaughan et al. 1999)....
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...…(mf) and arboviruses by vector arthropods has been shown to result in signiÞcantly more efÞcient transmission of the virus than when the same dose of virus was ingested alone (Mellor and Boorman 1980; Turell et al. 1984, 1987; Zytoon et al. 1993; Vaughan and Turell 1996; Vaughan et al. 1999)....
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...It has been shown in laboratory studies that mosquitoes that feed on vertebrates co-infected with mf and an arbovirus are signiÞcantly more efÞcient vectorsof thevirus thanmosquitoes that ingest virus alone (Turell et al. 1984, 1987; Zytoon et al. 1993; Vaughan and Turell 1996, Vaughan et al. 1999)....
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...Most laboratory studies of mf enhancement have used various arboviruses with Brugia spp. mf and Aedes/Ochlerotatus spp. mosquitoes as experimental model systems (Turell et al. 1984, 1987; Vaughan and Turell 1996; Vaughan et al. 1999)....
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TL;DR: Stable flies acquired PRRSV from the bloodmeal and the amount of virus in the flies declined with time, indicating virus did not replicate in fly digestive tissues, and detectable virus quantities in the intrathoracically inoculated stable flies followed an exponential decay curve.
Abstract: We investigated the acquisition of porcine reproductive and respiratory syndrome (PRRS) virus by the stable fly (Diptera: Muscidae; Stomoxys calcitrans (L.)) through a bloodmeal, and virus persistence in the digestive organs of the fly using virus isolation and quantitative reverse-transcription PCR (qRT-PCR). Stable flies were fed blood containing live virus, modified live vaccine virus, chemically inactivated virus, or no virus. Stable flies acquired PRRSV from the bloodmeal and the amount of virus in the flies declined with time, indicating virus did not replicate in fly digestive tissues. Virus RNA was recovered from the flies fed live virus up to 24 h postfeeding using virus isolation techniques and 96 h using qRT-PCR. We further examined the fate of PRRSV in the hemolymph of the flies following intrathoracic injection to bypass the midgut barrier. PRRSV was detected in intrathoracically inoculated adult stable flies for 10 d using qRT-PCR. In contrast to what we observed in the digestive tract, detectable virus quantities in the intrathoracically inoculated stable flies followed an exponential decay curve. The amount of virus decreased fourfold in the first 3 d and remained stable thereafter, up to 10 d.
9 citations
TL;DR: Experimental evidence is presented that suggests that certain alphaviruses may adhere or otherwise associate with sheathed Brugia malayi MF in the blood of a dually-infected host and that the virus is carried into the mosquito hemocoel by the MF during their penetration of the mosquito midgut.
Abstract: Concurrent ingestion of microfilariae (MF) and arboviruses by mosquitoes can enhance mosquito transmission of virus compared to when virus is ingested alone. Within hours of being ingested, MF penetrate the mosquito midgut and introduce virus into mosquito hemocoel, creating a disseminated viral infection much sooner than normal. How virus is actually introduced is not known. In this report, we present experimental evidence that suggests that certain alphaviruses may adhere or otherwise associate with sheathed Brugia malayi MF in the blood of a dually-infected host and that the virus is carried into the mosquito hemocoel by the MF during their penetration of the mosquito midgut. The mechanism of MF enhancement may be more complex than simple leakage of viremic blood into the hemocoel during MF penetration. The affinity of arboviruses to adhere to or otherwise associate with MF may depend on the specific combination of the virus and MF involved in a dual host infection. This in turn may determine the relative importance that MF enhancement has within an arbovirus transmission system.
9 citations
References
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TL;DR: This review summarises aspects of current knowledge on the frequency of multiparasite infections, the factors which influence them, and their pathogenic significance.
419 citations
TL;DR: A molecular clone of Venezuelan equine encephalitis virus (VEE) was constructed from four cDNAs that were synthesized using the viral RNA genome as template.
285 citations
TL;DR: Examination of legs and bodies separately provided a rapid and efficient method of determining dissemination status and all females developed a disseminated infection and successfully transmitted virus by bite if allowed to feed on a susceptible hamster or suckling mouse.
Abstract: Following ingestion of 10(4.2) to 10(7.2) plaque-forming units (PFU) of Rift Valley fever (RVF) virus, 662 of 850 female Culex pipiens (78%) became infected. Those mosquitoes that became infected separated into two distinct groups: 1) those with a nondisseminated infection limited to the gut, and 2) those with a disseminated infection. The former group contained a median of 10(3.2) PFU, while those females with a disseminated infection contained a median of 10(5.5) PFU. Only those females with a disseminated infection were capable of transmitting virus by bite to a susceptible hamster. This is consistent with a mesenteronal escape barrier to viral dissemination. Following intrathoracic inoculation of RVF virus, all females developed a disseminated infection (26/26) and successfully transmitted virus by bite (49/49) if allowed to feed on a susceptible hamster or suckling mouse. Examination of legs and bodies separately provided a rapid and efficient method of determining dissemination status.
150 citations
125 citations
TL;DR: This study evaluated changes in infection and transmission rates, and viral titers in F1 through F16 generation Cx.
Abstract: : Field and laboratory findings implicated Culex pipiens as a vector of Rift Valley fever (RVF) virus during the 1977-1978 epizoodtics/epidemics in Egypt. This study evaluated changes in infection and transmission rates, and viral titters in F sub 1 through F sub 16 generation Cx. pipiens mosquitoes orally infected with RVF virus. Infection and transmission rates of RVF virus by this species changed significantly during the colonization process. However, the ultimate viral titers of either the transmitting or the infected nontransmitting mosquitoes were not affected by the colonization process. Following ingestion of virus, Cx. pipiens could be separated into three distinct subpopulations, an uninfected group and two types of infected mosquitoes - transmitters and nontransmitters. Transmitters contained significantly more virus (approximately 100-fold) than nontransmitters. These results demonstrated that not every infected female mosquito should be considered a competent vector, even if the species (population) is known to be a primary vector. Transmission was also accomplished by probing mosquitoes which were unsuccessful in obtaining a blood meal. These data document the long-held suspicion that vector competence studies based upon laboratory-colonized specimens may not represent the field situation.
104 citations