Egypt, located in northeastern Africa, serves as a connector between Asia, Europe, and Africa. This unique geographic location, within the World Health Organization’s Eastern Mediterranean Region (EMR) and the Middle East and North Africa Region (MENA), complicates mosquito-borne virus (MBV) surveillance and control.
There are at least five common mosquito-borne viruses (MBVs) recorded in Egypt, including dengue virus (DENV), Rift Valley fever virus (RVFV), West Nile virus (WNV), Chikungunya virus, and Sindbis virus. Unexpected outbreaks caused by MBVs reflect the deficiencies of the MBV surveillance system in Egypt. This systematic review characterized the epidemiology of MBV prevalence in Egypt. Human, animal, and vector prevalence studies on MBVs in Egypt were retrieved from Web of Science, PubMed, and Bing Scholar, and 33 eligible studies were included for further analyses.
The common drawback for surveillance of MBVs in Egypt is the lack of seroprevalence studies on MBVs, especially in this century.
Mosquito-Borne Viruses in Egypt
At least five MBVs have been recorded in Egypt: dengue virus (DENV), Rift Valley fever virus (RVFV), Sindbis virus (SINV), West Nile virus (WNV), and Chikungunya virus (CHIKV). In addition to RVFV and DENV, sporadic cases or seropositivity for WNV [24,25], SINV [26], and CHIKV [27] have been reported in Egypt. The occurrence of unexpected disease outbreaks and occasional exported cases indicate that undetected DENV/WNV transmission occurred in Egypt before these events. These occurrences also reflect the deficiencies of the MBV surveillance system in Egypt, especially the absence of a system for early warning. In this article, we present a systematic review of the historical records of MBVs in Egypt to characterize the epidemiology of MBVs, with the aim of achieving evidence-based and informed risk prevention and control of these viruses and the diseases they cause.
Rift Valley Fever (RVF)
Four Rift valley fever (RVF) outbreaks occurred in the mid-to-late twentieth century and early in this century, i.e., in 1977-1978, 1993-1994, 1996-1997, and 2003. These outbreaks resulted in dramatic economic losses in the livestock industry, as well as loss of human lives. In recent decades, the expansion of live attenuated vaccines to animals has effectively slowed the spread of RVFV and curbed outbreaks. In the past decade, the seroprevalence of RVFV antibodies was more than 20% in some unvaccinated livestock in both the Upper Egypt and Nile Valley governorates, indicating the circulation of RVFV in Egypt.
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RVFV was isolated from rats (one out of eight), although RVFV antibodies were not observed in wild rodents during the 1977-1978 RVF epidemic in Sharqiya, Egypt. A positivity rate of RVFV antibodies of approximately 30% was detected in 300 tested blood samples of the wild black rat Rattus rattus in the Behera governorate around the year 2000. Cx. pipiens and Cx. antennatus are the primary vectors of RVFV in Egypt, as confirmed by virus isolation tests based on wild samples, while Ae. caspius was suspected to transmit RVFV in livestock animals.
Over 30% of the camels sampled at the southern borders of Egypt were seropositive for RVFV antibodies, according to an investigation of the 1977 RVF outbreak.
Dengue Fever
Dengue outbreaks in Egypt were reported in 1799 in Cairo and Alexandria. In 1937, 2594 human cases were recorded in Cairo. DENV has been largely controlled in Egypt by focusing on the eradication of its mosquito vector, Aedes aegypti, following the introduction and intense usage of the DDT insecticide. In 2011, DENV was unexpectedly detected in two Italian tourists returning from South Egypt. In 2015, a DENV resurgence occurred in the Dairoute District of the Assyoute (Assiut) Governorate, with at least 253 cases. In 2017, two cases of DENV were reported in travelers returning to Moscow, Russia, from Hurghada, Egypt, on the Red Sea coast. In the same year, a DENV outbreak with at least 680 cases occurred in the Red Sea Governorate, where the reintroduction and breeding of Ae. aegypti were confirmed.
Three human prevalence studies for DENV were identified. Seroprevalence in healthy male university students was 0.3% in 1969 and was absent in the serum samples of children with acute febrile illness in 1968 in Alexandria. This gap in the literature has existed for half a century. In Sohag and Assiut in 2019, the positive rates of DENV antibodies in the general population aged <21 years, 21 to 40 years, and >40 years old were 25%, 11.32%, and 10%, respectively, and 3.30% in local camels.
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West Nile Virus (WNV)
A total of 11 seroprevalence studies of WNV were identified from the eligible reports. WNV, first detected in Egypt, can be traced back to 1951. It was isolated from three serum samples of 251 children with a history of fever who lived in a community that is 30 km away from Cairo. The prevalence of the WNV antibody was 3% (15/437) among school children aged 8 to 14 years living in the Nile Valley governorates in 1989.
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During the period from 1999 to 2002, the human seroprevalence rates for the WNV antibody ranged from 1% to 35% in Upper Egypt, Middle Egypt, Lower Egypt, North Sinai, and South Sinai, while the seroconversion rates were 18%, 17%, and 7% in Upper Egypt, Middle Egypt, and Lower Egypt, respectively. Notably, 49% of seroconverters reported an undiagnosed febrile illness during the studied years. In 1999, the WNV antibody had the highest seropositivity rate (143/264, 54.14%) among MBVs in Egyptian workers at sewage treatment plants (STPs).
The WNV antibody positivity rates in adult horses ranged from 14% in Alexandria (northern Egypt) to 89% in Qena (Upper Egypt), according to a neutralization test carried out in 1959. In a study conducted in 2018, 16.8% of 930 horses from five governorates in the Nile Valley were serologically positive for WNV, with the highest seroprevalence in horses aged more than 15 years.
In the same year, the seroprevalence rates for WNV in other domestic livestock in the Nile Valley governorates (Qalyoubiya, Menoufiya, Kafr El-Sheikh, and Gharbiya) were 18% (18/100), 0% (0/50), 40% (20/50), 3.5% (3/85), and 5.3% (4/75) in cattle, buffalo, camels, sheep, and goats, respectively. For chickens, the seroconversion rate for the WNV antibody, detected using ELISA, ranged from 4% in Lower Egypt to 47% in Middle Egypt during the period from 1999 to 2002.
Culex pipiens, Cx. antennatus, and Cx. perexiguus were identified as vectors of WNV in Egypt. In addition to mosquitoes, the natural infection of WNV in ticks (Argas reflexus hermannii) was found in pigeon cotes located in Kafr El-Sheikh in 1960.
Sindbis Virus (SINV)
Four prevalence studies for SINV in Egypt were eligible for inclusion in the systematic review, and all were conducted before 2000. In 1968, SINV antigens were detected by hemagglutination inhibition and complement fixation in 4% acute sera from children living in Alexandria. In 1969, the seropositivity rate for SINV was 6% among 1113 male university students.
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In 1952, SINV was first isolated from Cx. pipiens and Cx. univittatus samples collected from a village located a few kilometers away from Cairo. In mosquito samples collected from Aswan in 1993, three pools out of 9011 individuals of Cx. perexiguus were determined to be positive for SINV by virus isolation tests, whereas no SINV was found in Anopheles multicolor, An. pharoensis, An. tenebrosus, Cx. antennatus, Cx. pipiens, Cx. poicilipes, Ae. (=Ochlerotatus) caspius, or Urranotaenia unguiculata.
Chikungunya Virus (CHIKV)
In 1984, the seropositivity rate for the CHIKV antibody was determined to be 14% among 502 tested sera samples from the general population in Egypt.
Aedes aegypti: The Yellow Fever Mosquito
Aedes aegypti (or from Greek αηδής 'hateful' and from Latin, meaning 'of Egypt'), sometimes called the Egyptian mosquito, dengue mosquito or yellow fever mosquito, is a mosquito that spreads diseases like dengue fever, yellow fever, malaria, and chikungunya. The mosquito can be recognized by black and white markings on its legs and a marking in the form of a lyre on the upper surface of its thorax.
Aedes aegypti is a 4-to-7-millimetre-long (5⁄32 to 35⁄128 in), dark mosquito which can be recognized by white markings on its legs and a marking in the form of a lyre on the upper surface of its thorax. Females are larger than males. Microscopically females possess small palps tipped with silver or white scales, and their antennae have sparse short hairs, whereas those of males are feathery. Males live off fruit and only the female bites for blood, which she needs to mature her eggs.
To find a host, she is attracted to chemical compounds emitted by mammals, including ammonia, carbon dioxide, lactic acid, and octenol. Scientists at The United States Department of Agriculture (USDA) Agricultural Research Service studied the specific chemical structure of octenol to better understand why this chemical attracts the mosquito to its host and found the mosquito has a preference for "right-handed" (dextrorotatory) octenol molecules. The preference for biting humans is dependent on expression of the odorant receptor AaegOr4.
The white eggs are laid separately into water and not together, unlike most other mosquitoes, and soon turn black.
Distribution and Spread of Aedes aegypti
In 2016, Zika virus-capable mosquito populations have been found adapting for persistence in warm temperate climates. Such a population has been identified to exist in parts of Washington, DC, and genetic evidence suggests they survived at least the last four winters in the region. As the world's climate becomes warmer, the range of Aedes aegypti and a hardier species originating in Asia, the tiger mosquito Aedes albopictus, which can expand its range to relatively cooler climates, will inexorably spread north and south.
In continental Europe, Aedes aegypti is not established but it has been found in localities close to Europe such as the Asian part of Turkey. However, a single adult female specimen was found in Marseille (Southern France) in 2018.
The invasive success of Ae. aegypti has largely been due to international travel and trade. Historically, Ae. aegypti has moved from continent to continent via ships and was previously established in southern Europe from the late 18th to the mid-20th century. Its disappearance from the Mediterranean, Black Sea and Macaronesian biogeographical region (Canary Islands, Madeira and the Azores) is not well understood . It has since recolonised Madeira , reappeared in parts of southern Russia and Georgia (Krasnodar Krai and Abkhazia) , and reportedly been introduced into the Netherlands , Canary Islands and Cyprus .
VectorNet field studies have shown the species to be widespread across extended areas of Georgia, including the capital city, Tbilisi, and it has also spread into north-eastern Türkiye . Nowadays it is one of the most widespread mosquito species globally. If Ae. aegypti is introduced into southern Europe, there are no climatic or environmental reasons as to why it could not survive .
Dispersal via shipping (ferries) from Madeira is still thought to represent the greatest risk for the introduction of this mosquito into Europe. Ae. aegypti thrives in densely populated areas without reliable water supplies, waste management and sanitation . It is suggested that Ae. aegypti evolved its domestic behaviour in West Africa, and its widespread colonisation and distribution across the tropics led to highly efficient inter-human transmission of viruses, such as dengue .
Genome Sequencing and Genetic Modification
In 2007, the genome of Aedes aegypti was published, after it had been sequenced and analyzed by a consortium including scientists at The Institute for Genomic Research (now part of the J. Craig Venter Institute), the European Bioinformatics Institute, the Broad Institute, and the University of Notre Dame. The effort in sequencing its DNA was intended to provide new avenues for research into insecticides and possible genetic modification to prevent the spread of virus. This was the second mosquito species to have its genome sequenced in full (the first was Anopheles gambiae).
Ae. aegypti has been genetically modified to suppress its own species in an approach similar to the sterile insect technique, thereby reducing the risk of disease. The mosquitoes, known as OX513A, were developed by Oxitec, a spinout of Oxford University. Field trials in the Cayman Islands, in Juazeiro, Brazil, and in Panama have shown that the OX513A mosquitoes reduced the target mosquito populations by more than 90%.
Diseases Transmitted by Aedes aegypti
Aedes aegypti is a known vector of several viruses including yellow fever virus, dengue virus chikungunya virus and Zika virus. In Europe, imported cases infected with these viruses are reported every year . Therefore, the potential establishment of this mosquito in Europe raises concerns about autochthonous transmission of these arboviruses , particularly in southern Europe where climatic conditions are most suitable for the re-establishment of the species.
Aedes aegypti is the primary vector of chikungunya virus . Transovarial transmission was demonstrated by Aitken et al. under laboratory conditions and the virus has been detected in wild-caught male Ae. aegypti. Transovarial transmission may help with the maintenance of the virus in nature . Aedes aegypti has been involved in virtually all chikungunya epidemics in Africa, India and other countries in South-East Asia . The species caused an outbreak of chikungunya in Kenya (2004) and the Comoros islands (2005), affecting 63% of the population in the latter case . An entomological investigation following an outbreak of chikungunya virus in Yemen (2010/2011) revealed the presence of the virus in field-collected Ae. aegypti in the outbreak area . More recently, Ae. aegypti was involved in large chikungunya outbreaks in the Pacific and the Caribbean .
Aedes aegypti is the primary vector of dengue. All four dengue serotypes have been isolated from field-collected Ae. aegypti . Aedes aegypti has long been recognised as a vector of dengue, causing major dengue fever epidemics in the Americas and South-East Asia. The global incidence of dengue has also increased over the past 25 years . Historically, outbreaks have also been reported in Europe, with one of the largest outbreaks on record occurring in Athens and neighbouring areas of Greece during the period 1927-1928 . In 2012, a large outbreak of dengue fever occurred in the Portuguese Autonomous Region of Madeira where Ae. aegypti is present .
Yellow fever is maintained in a sylvatic cycle between monkeys and mosquitoes of Aedes or Haemagogus genera . Aedes aegypti is the vector involved in urban transmission of yellow fever where only humans are the amplifying host. Yellow fever transmission has been reported from countries across sub-Saharan Africa and in tropical areas across South and Central America, from Panama to the northern part of Argentina . Autochthonous transmission of yellow fever has never been detected in Asia, although the Ae. aegypti mosquito is present there .
Zika virus is maintained in a sylvatic cycle involving non-human primates and a wide variety of sylvatic and peri-domestic Aedes mosquitoes. Aedes aegypti is considered the most important vector for Zika virus transmission to humans. Aedes aegypti mosquitoes were found infected in the wild (reviewed in [56]). More recently, the species was found infected during the Zika virus outbreak in Brazil .
Prevention and Control Measures
The Centers for Disease Control and Prevention traveler's page on preventing dengue fever suggests using mosquito repellents that contain DEET (N, N-diethylmetatoluamide, 20% to 30%). Once a week, scrub off eggs sticking to wet containers, seal or discard them. The mosquitoes prefer to breed in areas of stagnant water, such as flower vases, uncovered barrels, buckets, and discarded tires, but the most dangerous areas are wet shower floors and toilet tanks, as they allow the mosquitos to breed in the residence.
The spread of Ae. aegypti-borne diseases has been aided by the global spread of Ae. aegypti over the past 25 years . Although currently limited in spread due to its intolerance to temperate winters, climate change could result in an increased distribution of Ae. As the human population grows, sites in which this mosquito can thrive will increase, providing further habitats. This fact, coupled with the close proximity of humans and the tendency of Ae. aegypti to feed on multiple hosts during one gonotrophic cycle , increases the risk of disease transmission in such areas.
Traditional methods such as source reduction, public education and insecticide application are routinely implemented by municipalities to reduce Aedes populations, but with limited success, probably because of poor participation of communities, and a lack of coordination and synchronised implementation .
Using a combination of control methods as opposed to one strategy is suggested to be most effective, and will reduce the chance of introducing selective pressures - e.g. on oviposition site selection .
Protective clothing and repellents are also advocated to reduce exposure to Ae. aegypti, as well as the spraying of indoor living spaces with pyrethrin.
Conclusion
It is clear that if Ae. aegypti re-establishes itself in the European regions it previously inhabited and spreads, it will have a significant impact on public health. The spread of Ae. aegypti-borne diseases has been aided by the global spread of Ae. aegypti over the past 25 years.
Table 1: Mosquito-Borne Viruses and Their Vectors in Egypt
| Virus | Primary Vector(s) in Egypt |
|---|---|
| Dengue Virus (DENV) | Aedes aegypti |
| Rift Valley Fever Virus (RVFV) | Culex pipiens, Culex antennatus |
| West Nile Virus (WNV) | Culex pipiens, Culex antennatus, Culex perexiguus |
| Sindbis Virus (SINV) | Culex pipiens, Culex univittatus, Culex perexiguus |
| Chikungunya Virus (CHIKV) | Aedes aegypti |
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