Host Feeding of Mosquitoes (Diptera: Culicidae) Associated with the ...

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ABSTRACT In 1993, Rift Valley fever (RVF) virus reappeared in Egypt. We determined the prevalence and feeding patterns of mosquitoes in 5 villages where ...
Host Feeding of Mosquitoes (Diptera: Culicidae) Associated with the Recurrence of Rift Valley Fever in Egypt ADEL M. GAD,1 HODA A. FARID,1 REDA R. M. RAMZY,1 MAHMOUD B. RIAD,1 STEVEN M. PRESLEY,2, 3 STANTON E. COPE,2, 4 MOSSAD M. HASSAN,1 AND ALI N. HASSAN1

J. Med. Entomol. 36(6): 709Ð714 (1999)

ABSTRACT In 1993, Rift Valley fever (RVF) virus reappeared in Egypt. We determined the prevalence and feeding patterns of mosquitoes in 5 villages where the virus was active. Of 10 species recovered, Aedes caspius (Pallas), Culex pipiens L., Cx. antennatus (Becker), and Cx. perexiguus Theobald constituted 99% of ⬎35,000 mosquitoes captured in dry ice-baited CDC light traps. Ae. caspius was most prevalent, except at NagÕ El Hagar where it was replaced by Cx. perexiguus. Cx. pipiens ranked 2nd, except at NagÕ El Ghuneimiya, where it was replaced by Cx. antennatus. Most blood meals analyzed by an enzyme-linked immunosorbent assay reacted to ⱖ1 antiserum. Cx. pipiens was mainly anthropophagic, and therefore may have been the main vector of RVF virus among humans. Ae. caspius feeds were chießy from humans, bovines, and equines. Cx. antennatus and Cx. perexiguus fed generally on bovines. Mixed blood meals from humans and RVF virus susceptible animals were identiÞed in the predominant mosquitoes. Prevalence and host selection, as well as predicted probability for a blood meal being interrupted, indicated that Ae. caspius may have served as a bridge vector between humans and bovines in 4 of the villages. Cx. perexiguus may have played this role at NagÕ El Hagar. Because potential vectors are abundant, susceptible domestic animals are associated closely with humans, and surveillance of imported livestock is not systematic, we conclude that RVF virus sporadically will recur in Egypt. KEY WORDS mosquito, blood meal, Rift Valley fever, Egypt

RIFT VALLEY FEVER (RVF) virus was Þrst introduced into southern Egypt in 1977 from where it rapidly spread northward to the Nile Delta causing an estimated 600 human deaths as well as abortion and death in sheep and cattle (Hoogstraal et al. 1979, Meegan 1979). The virus persisted during 1978. After a 12-yr absence, RVF virus reappeared in May 1993 in southern Egypt, with an estimated 600 Ð1,500 human infections and widespread abortions and deaths in domestic livestock. Sera collected from sheep, goats, buffalo, and cattle in the Aswan governorate were positive for antibodies to RVF virus (Arthur et al. 1993). Evidence of RVF virus activity also was detected in the Nile Delta and the Faiyum Oasis (Corwin et al. 1993, WHO 1994). To acquire RVF virus, mosquitoes must feed on viremic mammals; therefore, it is important to understand mosquito host-feeding patterns. During the 1977Ð1978 epidemics, Culex pipiens L. was implicated as the primary vector of RVF virus, based on a single virus isolation from an unengorged female (Hoogstraal et al. 1979) and its blood feeding habits (Kenawy 1 Research and Training Center on Vectors of Diseases, Ain Shams University, Cairo, Egypt. 2 Naval Medical Research Unit No. 3, Abbassia, Cairo, Egypt. 3 Current address: Training Programs Br C 462, Marine Corps Combat Development Command, 3300 Russell Road, Quantico, VA 22134 Ð 5001. 4 Current address: Navy Environmental Health Center, 2510 Walmer Avenue, Norfolk, VA 23513.

et al. 1987, Gad et al. 1995). Aedes caspius (Pallas) and Cx. antennatus (Becker) were suspected of disseminating the virus among livestock, based on feeding patterns (Kenawy et al. 1987, Gad et al. 1995) and vector competence (Gad et al. 1987). However, these studies of host selection by mosquitoes (Zimmerman et al. 1985) were carried out after RVF virus was last documented in 1981 (Imam et al. 1981). During the RVF virus outbreak in 1993, we initiated a multidisciplinary study in Aswan governorate. Entomological efforts determined the prevalence and host feeding patterns of mosquitoes at 5 villages where human or livestock disease was occurring. Materials and Methods Mosquito Collections. Mosquitoes were sampled from 14 to 24 August 1993 in the Aswan governorate on the southernmost part of the Nile Valley in 5 agricultural villages north of Aswan City (Fig. 1) where animal and human RVF virus infections were occurring. The villages were environmentally and socioeconomically similar. Houses generally were associated with animal sheds where domestic animals (horses, donkeys, cattle, buffalo, goats, sheep, and poultry) were kept at night. Epidemiological investigations in NagÕ El Hagar and Sabil Abu El Magd revealed that the human population exceeded 2,000 in each village. Animal host censuses included only those animals susceptible to RVF virus. In NagÕ El Hagar (n ⫽ 44

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Fig. 1. Mosquito collection sites in Southern Egypt (numbered).

households), bovines (cattle only) and ovines (sheep and goats) constituted 13.5 and 86.5%, respectively, of the livestock (n ⫽ 252). Host populations consisted of 7.4 humans, 0.8 bovines, and 5.0 ovines per household. In Sabil Abu El Magd (n ⫽ 52 households), bovines (cattle and buffaloes) and ovines accounted for 36.5 and 63.5%, respectively, of the livestock (n ⫽ 214). There were 7.0 humans, 1.5 bovines, and 2.6 ovines per household. Houses mostly were surrounded by sugarcane Þelds except in NagÕ El Hagar. Mosquitoes were collected by dry ice-baited traps (without light) operated from sunset to sunrise. Blood-fed mosquitoes were recovered from these traps, and on a few occasions collected resting inside buildings. From 7 to 28 traps per village per night were hung outdoors on trees or streetlights near houses on the edges of cultivated Þelds during 6 consecutive nights in NagÕ El Hagar, 4 in Sabil Abu El Magd, and 2 in El Raghama. NagÕ El Ghuneimiya and El Naghaghra were each sampled once, because these villages had been treated with insecticides after the 1st night. Traps were checked every 2 h and the catching net replaced when full of insects. Specimens were identiÞed on dry ice accord-

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ing to the keys of Gad (1963) and Harbach (1985). Blood-fed mosquitoes were separated by species and location, each group placed in a labeled screwcap vial and stored at ⫺70⬚C until tested for blood meal source at Ain Shams University. Blood Meal Identification. Only mosquitoes captured in traps were tested. Blood meals were identiÞed using the direct enzyme immunoassay (EIA) developed by Beier et al. (1988), with slight modiÞcation. Brießy, individual mosquitoes were homogenized in phosphate buffered saline. Polyvinyl chloride plates (Falcon 3912 microtiter plates, Becton Dickinson, Oxnard, CA) were sensitized by incubating each mosquito homogenate in duplicate wells. Plates then were washed with PBS containing 0.05% Tween 20, and 50 ␮l of host-speciÞc peroxidase conjugate (human, bovine, ovine, equine, canine, cat, rat, and chicken, Sigma, St. Louis, MO), diluted at 1:2000 (or 1:250 for bovine) in boiled casein, were added to each well. Plates were incubated, washed and optical densities at 410 nm determined with an enzyme-linked immunosorbent assay (ELISA) reader (MR 4000 Dynatech, Alexandria, VA) 15 min after the addition of ABTS peroxidase substrate (Kirkegaard & Perry, Gaithersburg, MD). Positive controls consisting of mixed unfed mosquitoes and host blood from our sera bank, and negative controls consisting of unfed mosquitoes were included on each microtiter plate. To decrease cross reactivity, heterologous serum (8 hosts) was added to the conjugate solution for each test. Positive samples were those with absorbance values exceeding mean plus 3 times the standard deviation of the negative controls. Multiple feedings were detected by repeating the assay for the whole range of hosts tested. The probability of interrupted feeding was determined as in Burkot et al. (1988) and assumed that the probability of interruption was the same for human and nonhuman hosts. Only meals containing blood from humans and ovines or bovines were used to evaluate mosquito feeding behavior regarding hosts susceptible to RVF virus (Ghoneim and Woods 1983). Results Prevalence of adult mosquitoes varied among the 5 study villages (Table 1). From 4 to 10 species were recovered from each village. Ae. caspius, Cx. pipiens, Cx. antennatus, and Cx. perexiguus were collected from all 5 villages where they constituted 98.7% of the 35,289 specimens. Of the specimens collected, 664 were blood-fed to repletion. Mosquito species each with ⬍1% prevalence were Cx. poicilipes (Theobald), Uranotaenia unguiculata Edwards, Anopheles pharoensis Theobald, An. tenebrosus Doenitz, An. sergentii (Theobald), and An. multicolor Cambouliu. Two to 4 species were abundant (at least 5%) in each village. Ae. caspius predominated, except at NagÕ El Hagar where Cx. perexiguus was most prevalent. Cx. pipiens ranked 2nd in prevalence, except at NagÕ El Ghuneimiya where it was replaced by Cx. antennatus. The pattern of mosquito abundance in the study villages followed that observed for species prevalence. An average 30.3Ð

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Table 1. Mosquito species composition determined by CO2-baited CDC traps (without light) from rural villages in Aswan governorate, 14 –24 August 1993 % of total females Mosquito species

NagÕ El Ghuneimiya (18)

El Raghama (42)

El Naghaghra (7)

Sabil Abu El Magd (68)

NagÕ El Hagar (89)

Ae. caspius Cx. pipiens Cx. antennatus Cx. perexiguus Total specimensa No. per trap-night

43.53 12.25 32.43 8.71 2,433 135.2

79.81 19.39 0.39 0.41 5,353 127.5

65.15 12.67 12.28 0.40 505 72.4

93.56 4.70 0.67 0.02 8,514 125.2

14.60 28.28 9.49 46.04 18,484 207.7

Numbers in parentheses represent total trap-nights. Including mosquito species with ⬍1% prevalence each (Cx. poicilipes, U. unguiculata, An. pharoensis, An. tenebrosus, An. sergentii, An. multicolor). a

17.1 female Ae. caspius were collected per trap-night per village. Other predominant mosquitoes were less abundant: with 5.9 Ð58.7 female per trap-night per village for Cx. pipiens, 0.5Ð 43.8 for Cx. antennatus and ⬍0.1Ð95.6 for Cx. perexiguus. Average mosquito density was lowest at El Naghaghra and highest at NagÕ El Hagar (Table 1). Of 664 blood engorged mosquitoes analyzed by EIA, 92.2% reacted to ⱖ1 antiserum (Table 2) and 14.9% of these reacted to ⱖ2 antisera. Large mammals (humans, bovines and equids) constituted most hosts identiÞed for the predominant mosquitoes (Table 2). Ae. caspius fed frequently on human, bovine and equine hosts, although this pattern varied among villages (Table 3) (␹2 ⫽ 46.7, df ⫽ 16, P ⬍ 0.01). Frequent human feeds by this mosquito were observed in Raghama and NagÕ El Hagar. In Sabil Abu El Magd females fed predominantly on large mammals. Ovine feeds by this mosquito were more frequent in Raghama than in the other 2 villages. Cx. pipiens was mainly anthropophagic (Table 3). The proportional meals consisting of human, bovine, equine and ovine blood did not vary among villages for this species (␹2 ⫽ 10.1, df ⫽ 6, P ⬎ 0.05). Cx. antennatus and Cx. perexiguus fed mostly on bovines (Table 2). Ovine feeds by predominant mosquitoes were 2.8%. Dog, rat, cat and chicken feeds amounted to 3.4% for Ae. caspius, 5.4% for Cx. pipiens, 8.3% for Cx. antennatus, and 9.0% for Cx. perexiguus. All 4 mosquitoes fed on unidentiÞed hosts. Of 28 An. tenebrosus, 89.3 and 10.7% fed on humans and bovines, respectively. Two human and 1 equine feeds were detected for 3 An. pharoensis. One An. multicolor fed on horse blood, whereas 1 unidentiÞed blood meal was from U. unguiculata. Mixed meals were recognized in the 4 predominant mosquitoes from all 5 villages, and also in An. tenebrosus (Table 4). Of 99 mixed blood meals, 91% were Table 2.

double feeds and 9% were triple feeds. Mosquito feeds containing blood from humans and RVF virus susceptible animals (bovines or ovines) constituted 28.3% of multiple feeds and 4.2% of all blood meals. Such feeds were 35.3 and 14.8% of mixed meals by Ae. caspius from NagÕ El Hagar (n ⫽ 17) and Sabil Abu El Magd (n ⫽ 27), respectively, and 40.7% of those by Cx. pipiens from NagÕ El Hagar (n ⫽ 27). Mosquito feeds containing human blood and blood from nonsusceptible RVF virus animals were 26.3 and 3.9% of multiple and total meals, respectively. Such mixed blood meal groups constituted 58.8 and 3.7% of Ae. caspius meals from NagÕ El Hagar and Sabil Abu El Magd respectively, and 22.2% of Cx. pipiens meals from NagÕ El Hagar. Overall, the probability of a blood meal being interrupted was 0.10. In villages where ⬎100 meals were tested, the proportion of mixed meals estimated the probability of interruption of a meal by Ae. caspius (Table 5). The predicted probability for interrupted meals by this species was 0.096 in NagÕ El Hagar and 0.043 in Sabil Abu El Magd. Discussion Of 14 mosquito species known to occur in the Aswan governorate (Kenawy et al. 1987), 10 were recovered from villages where cases of RVF virus infections were reported. Serological evidence of infections came from blood samples collected during the same period and region from humans and livestock (Arthur et al. 1993). Ae. caspius, Cx. pipiens, Cx. perexiguus, and Cx. antennatus predominated in outdoor trap collections. No systematic indoor collections were made. However, only Ae. caspius (n ⫽ 102) were found resting in 2 bedrooms at Sabil Abu El Magd. Females (n ⫽ 14) of this species were recovered in 1 bedroom at NagÕ El Hagar as well. Other sampling

Single blood meal hosts of mosquitoes collected from Aswan governorate, 14 –24 August 1993

Mosquito species Ae. caspius Cx. pipiens Cx. antennatus Cx. perexiguus

n 318 112 36 67

Blood meal hosts (% total) Human

Bovine

Ovine

Equine

Dog

Cat

Rat

Chicken

Nonreactor

38.4 59.8 13.9 8.9

26.4 9.8 30.6 50.7

3.8 1.8 0.0 1.5

23.3 7.1 19.4 16.5

1.9 0.9 5.5 0.0

0.3 0.0 0.0 1.5

0.6 0.0 2.8 4.5

0.6 4.5 0.0 3.0

4.7 16.1 27.8 13.4

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Table 3.

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Single blood meal hosts of mosquitoes collected from villages in Aswan governorate, 14 –24 August 1993

Mosquito tested in village Ae. caspius Raghama Sabil Abu El Magd NagÕ El Hagar Cx. pipiens Raghama Sabil Abu El Magd NagÕ El Hagar

Blood meal hosts (% total) n

Human

Bovine

Equine

Ovine

Dog

Cat

Rat

Chicken

Nonreactor

40 157 108

40.0 28.0 57.4

17.5 31.2 19.4

20.0 32.6 11.1

10.0 3.2 2.8

2.5 1.9 1.9

0.0 0.6 0.0

0.0 0.6 0.0

0.0 0.0 1.9

10.0 1.9 5.5

41 15 52

65.8 46.7 57.7

4.9 33.3 7.7

9.7 13.3 3.8

2.5 0.0 1.9

0.0 0.0 1.9

0.0 0.0 0.0

0.0 0.0 0.0

4.9 0.0 5.8

12.2 6.7 21.2

methods might have produced a different pattern. Indeed, an earlier study carried out in the Aswan governorate (Kenawy et al. 1987) revealed that although Ae. caspius prevailed outdoors, and Cx. pipiens represented 95% of indoor collections. The predominant species fed on large mammalian hosts including humans, bovines, equines, and to a much lesser extent, ovines. Vector competence studies of mosquitoes collected in epizootic areas during the 1993 outbreak (Turell et al. 1996) revealed that the 4 predominant species were susceptible to infection and able to transmit RVF virus. We suggest that these mosquitoes were the chief vectors of RVF virus in the 5 villages studied. Earlier reports of mosquito blood feeding in Egypt were based on precipitin tests and failed to detect mixed meals (Gad et al. 1995). The EIA currently used revealed that mixed meals including human and bovine or ovine blood were common in the predominant species from all 5 villages, particularly Ae. caspius, indicating that a signiÞcant proportion of the mosquito population in Aswan governorate acted Table 4. Multiple blood meal sources of mosquitoes in Aswan governorate, 14 –24 August 1993 % mosquito blood meal hosts Blood meal

Ae. caspius

Cx. pipiens

Cx. perexiguus

All species

Human/Bovine Human/Equine Human/Ovine Human/Dog Human/Rat Human/Chicken Bovine/Equine Bovine/Ovine Bovine/Dog Bovine/Rat Equine/Ovine Equine/Dog Equine/Rat Human/Bovine/Equine Human/Bovine/Ovine Human/Equine/Ovine Human/Ovine/Dog Human/Ovine/Rat Bovine/Equine/Ovine Bovine/Ovine/Cat Bovine/Ovine/Rat Total

14.6 20.8 4.1 2.1 4.1 0.0 27.1 2.1 2.1 8.3 6.3 0.0 2.1 2.1 0.0 0.0 0.0 0.0 2.1 2.1 0.0 48

14.8 14.8 17.7 0.0 8.8 2.9 2.9 23.6 0.0 0.0 0.0 0.0 0.0 0.0 2.9 2.9 2.9 2.9 0.0 0.0 2.9 34

10.0 0.0 0.0 0.0 10.0 0.0 30.0 0.0 10.0 0.0 20.0 10.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 10.0 10

15.2 15.2 8.1 1.0 9.1 1.0 18.2 9.1 3.0 4.0 5.1 1.0 1.0 1.0 1.0 1.0 1.0 1.0 1.0 1.0 2.0 99a

a Including blood meals by Cx. antennatus (1 human/bovine, 2 human/rat, 1 bovine/equine, 1 bovine/dog) and An. tenebrosus (1 human/bovine, 1 human/rat).

as a bridge vector of RVF virus between humans and susceptible animals. Based on abundance, feeding behavior, susceptibility to infection, and ability to transmit the virus, Ae. caspius may have played an important role in RVF virus transmission in at least 4 of the villages, serving as the major bridge vector between humans and bovines. Furthermore, interrupted feeds between humans and ovines or bovines by this mosquito indicated frequent host contacts among these hosts, in villages where it predominated. Ae. caspius was suspected of disseminating RVF virus among animal populations during the 1977Ð1978 epidemics (Kenawy et al. 1987). In the Aswan governorate, it is associated closely with sugar cane plantations. In NagÕ El Hagar, where there were no sugarcane Þelds when collections were made, Cx. perexiguus predominated, feeding mainly on bovines, but also on humans, and therefore acting as the primary link between animals and humans in that village. Cx. pipiens was the 2nd most abundant mosquito, except at NagÕ El Ghuneimiya. Its marked anthropophagy indicated that it may have been the main vector of RVF virus among humans. Earlier studies reported similar observations for Cx. pipiens from the Aswan (Kenawy et al. 1987) and Sharqiya (Gad et al. 1995) governorates. Zoophagy was reported for females from Gharbiya governorate (Zimmerman et al. 1985). In the Faiyum Oasis, this species exhibited an elevated forage ratio for bovines and ovines (Beier et al. 1986). Much of the geographic variation in host-feeding by mosquito species in Egypt has been attributed to relative host abundance, which is largely a reßection of ecological conditions and human customs (Zimmerman et al. 1985, Beier et al. 1987). Because ovines were abundant in Sabil Abu El Magd and NagÕ El Hagar, the low number of ovine feeds could not be related to low sheep/goat populations in these villages. Cx. antennatus constituted approximately one-third of collected mosquitoes and fed mainly on bovines, as well as humans and other large mammals. This mosquito may have been the main link vector for RVF virus between humans and animals in Sharqiya (Gad et al. 1995). Interestingly, ⬇42% of Cx. antennatus feeds were unidentiÞed. In the Nile Delta, this mosquito fed exclusively on large mammals (Zimmerman et al. 1985), with a marked preference for ovines (Gad et al. 1995). Its host range is wider in other parts of Africa, where it appears to feed on large mammals as well as birds (Chandler et al. 1975, 1976). However, few Cx. antennatus fed on

November 1999 Table 5.

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713

Probability that Ae. caspius feeding on humans takes a multiple blood meal Predicted

Village

No. human meals

No. mixed human mealsa

Total meals

Proportion mixed human meals

Qb

IHc

Sabil Abu El Magd NagÕ El Hagar

44 62

3 6

184 125

0.016 0.048

0.247 0.520

0.043 0.096

a

Meal with human and bovine or ovine blood. Q, proportion of meals with only human blood ⫹ (proportion of mixed human meals/2). Assuming IH ⫽ IN ⫽ probability of interruption of a human (IH) or nonhuman (IN) blood meal ⫽ proportion of mixed blood meals/2Q (1 Ð Q). b c

domestic birds in Lower Egypt and unidentiÞed feeds by this mosquito did not react with general bird antisera (Gad et al. 1995). Therefore, it is doubtful that most nonreacting blood meals by Cx. antennatus were from wild birds. Our Þndings demonstrated that the 4 dominant mosquito species feed on a wide variety of hosts, and thus are quite opportunistic in their feeding behavior, conÞrming earlier reports (Kenawy et al. 1987, Gad et al. 1995). This is important because these mosquitoes may have served as a bridge vector between humans and domestic animals. The basic transmission cycle of RVF virus in Egypt, although poorly understood, differs from that in subSaharan Africa where infections recur after particularly wet seasons. No true ßoodwater mosquito species occur in Egypt, where the agricultural land is irrigated regularly and therefore not exposed to drought periods. Moreover, although Ae. caspius lays droughtresistant eggs (unpublished data), vertical transmission of RVF virus by this species is questionable, because no transovarial transmission seems to occur in aedines (Macintosh and Jupp 1981) or in Cx. pipiens (Turell et al. 1984, Romoser et al. 1992). Furthermore, no animal reservoir host has been demonstrated (Hoogstraal et al. 1979). Therefore, it is most likely that RVF virus does not become established, but rather has to be reintroduced into Egypt. Camels (Hoogstraal et al. 1979) or sheep (Gad et al. 1986) smuggled from Sudan are thought to have introduced the virus into Egypt in 1977, and the same scenario may have been repeated. Several possible modes of RVF virus transmission have been contemplated. Biological transmission of RVF virus from viremic livestock to vectors to other vertebrates has been generally admitted. High viremias occurred in infected humans and livestock (Hoogstraal et al. 1979, Meegan 1979) and were sufÞcient to infect potential vectors (Turell et al. 1996). Therefore, both humans and domestic animals may have served as an important source of infection. Furthermore, because of high titered viremias in vertebrate hosts, mechanical transmission by mosquitoes was suspected during the 1977 epizootic/epidemic (Hoogstraal et al. 1979, Meegan and Bailey 1988). Mechanical transmission has been demonstrated experimentally in Cx. pipiens (Hoch et al. 1985), which were able to transmit RVF virus by probing, even if they failed to feed (Gargan et al. 1983). This, combined with abundance in areas where RVF virus occurs, may extend the importance of interrupted feed-

ing by infected Cx. pipiens, because it would increase its chances of transmitting RVF virus. However, no data exist regarding mechanical transmission by other potential vectors, so that interrupted feeding by such mosquitoes only indicated their potential for increased transmission. Aerosol transmission from vertebrates to humans by inhalation of virus during animal slaughtering (Hoogstraal et al. 1979) and transmission through contact with infected animal tissues (Van Velden et al. 1977) have been documented. Therefore, as long as humans live in close association with susceptible domestic animals, and without systematic surveillance of livestock introduced through Sudan, RVF virus sporadically will be imported into Egypt. This statement is supported by our study, which demonstrated that 12 yr after the 1st RVF virus epidemic, potential vectors that feed on both humans and animals remain available, and could contribute to the dissemination of RVF virus in Egypt. Acknowledgments This study was supported in part by the Research and Training Center on Vectors of Diseases, Ain Shams University.

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