Mosquitoes of Etiological Concern in Kenya

Created by: Xiaomin Hu

Kenya is among the most affected tropical countries with pathogen transmitting Culicidae vectors. For decades, insect vectors have contributed to the emergence and distribution of viral and parasitic pathogens. Outbreaks and diseases have a great impact on a country’s economy, as resources that would otherwise be used for developmental projects are redirected to curb hospitalization cases and manage outbreaks. Infected invasive mosquito species have been shown to increasingly cross both local and global boarders due to the presence of increased environmental changes, trade, and tourism. In Kenya, there have been several mosquito-borne disease outbreaks such as the recent outbreaks along the coast of Kenya, involving chikungunya and dengue. This certainly calls for the implementation of strategies aimed at strengthening integrated vector management programs. Here we look at mosquitoes of public health concern in Kenya, while highlighting the pathogens they have been linked with over the years and across various regions. 

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1. Introduction

The term “vector-borne” has become a commonly used term, especially in tropical and subtropical countries where emerging and re-emerging vector-related diseases frequently occur. One-sixth of human diseases is associated with vector-borne pathogens, with approximately more than half of the global population currently estimated to be in danger of contracting these diseases [1]. Hematophagous mosquitoes are the leading vectors among arthropods because of the significant role they play in disseminating microfilariae, arboviruses, and Plasmodium parasites that seem endemic to sub-Saharan Africa [2,3]. The majority of these pathogens are maintained in zoonotic cycles and humans are typically coincidental dead-end hosts with a none-to-minimal role in the cycle of the pathogen [4].
Mosquito vectoral ability is greatly influenced by the availability of conducive breeding grounds, which is in turn, influenced by the spatial heterogeneity as well as the temporal variability of the environment [5]. Mosquitoes, pathogens, and hosts each endure and reproduce within certain ideal climatic conditions and changes in these conditions can greatly alter these pathogen transmission/competences. In this scope, temperature and level of precipitation are the most influential climatic components, but other factors such as sunshine length, sea level elevation, and wind have been shown to have considerable effects [6,7]. These vectors often adjust to changes in temperature by changing topographical distribution. For instance, the advent of malaria cases in the cooler regions of East African highlands may be attributed to climate change, which has led to an increase in mosquitoes in the highlands as they warm up [8]. Variability in precipitation may also have a direct influence on distribution of mosquito-borne diseases. When precipitation increases, the presence of disease vectors is also expected to rise due to the expansion of the existent larval habitat and emergence of new breeding zones [6]. Each mosquito species has unique environmental resilience limits dependent upon the availability of favorable aquatic larval habitats and the closeness of vertebrate hosts that serve as their source of blood meals. This reliance of mosquito species on aquatic environments is a constant part of their lifecycle and the availability of a suitable aquatic domain, which is a requirement for the development of eggs, larvae, and pupae, and basically determines the abundance of mosquito species.
Kenya represents a topographically diverse tropical/subtropical country which harbors a large diversity of mosquito species of public health importance. Many factors contribute to the extensive proliferation of mosquitoes ranging from global warming, sporadic floods, improper waste disposal, irrigation canals, presence of several lakes/rivers, and low altitudes around coastal regions. Consequently, an upsurge in emerging and re-emerging mosquito-borne pathogens over the years has been recorded with increased research efforts geared towards mosquitoes and their pathogens [9]. Increased urbanization, tourism, and international trade have led some of these species and pathogens to cross local and international borders to new territories. This dispersal poses both local and global health threats if proper mitigation measures are not put in place. Nevertheless, not all mosquito species are associated with human diseases, thus, this review highlights species of the main mosquito genera to which pathogens have been associated/detected and their countrywide distribution based on published data and reported cases. Additionally, this information provides a guide to proper mosquito control strategies by comparing the methods currently applied in the country and proposed alternative methods applied in other countries affected by mosquito disease burden.

2. Mosquito-Borne Disease Endemic Regions in Kenya

Kenya, as a tropical country, is among the most affected sub-Saharan regions with mosquito-related ailments. The countrywide distribution of mosquito species is, however, not well documented with most studies focusing on disease endemic regions. Some of these regions include Garissa, Mandera, and Turkana situated in the north and north-eastern parts of the country and characterized as arid and semi-arid regions (Figure 1A). During rainy seasons, flood water acts as breeding areas for mosquito species. Rift Valley fever outbreaks were recorded in this area in 1997/98 and 2006/07 [10,11]. Other viruses reported from the regions include West Nile virus (WNV), Ndumu virus (NDUV), Babanki virus (BBKV), and orthobunyaviruses isolated from the flood water Aedes and Culex species [4]. For decades, the coastal region of Kenya (Kwale, Kilifi, Mombasa, Lamu) has also reported multiple outbreaks resulting from mosquito-borne pathogens making it one of the most endemic regions. The contributing factors are majorly the low altitude which provides a conductive environment for mosquito breeding and high human population composed of both locals and global tourists. Mosquitoes of interest in this coastal region in terms of pathogen transmission include: Aedes aegypti that transmits dengue fever and chikungunya [12,13]; Anopheles species (Anopheles gambiaeAnopheles arabiensis, Anopheles funestusAnopheles merus) which are associated with malaria and bancroftian filariasis sporozoites [14,15], and Culex quinquefasciatus [16] among others as demonstrated in Figure 1A–C.
 
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Figure 1. Mosquito-borne disease endemic regions based on distribution of pathogens and associated mosquito species (maps were constructed using the free and open-source Quantum GIS software (https://qgis.org/en/site/) using data compiled from Table 1 and Table 2. (A) Abundance of mosquito-borne viruses detected/isolated in various counties. (B) Distribution of the major malaria vectors in numbers in different counties. (C) Counties in which Wuchereria bancrofti has been detected from mosquitoes.
 
Table 1. Summary of the main mosquito species in which viruses have been detected/isolated in Kenya.
Genera Species Virus Isolated/Detected 1 County of Virus Detection Reference
Aedes A. aegypti DENV, CHKV Mombasa, Mandera, Kilifi, Lamu, Busia [12,13,33,55,57,58]
  A. africanus YFV Baringo, [59]
  A. albicosta DENV, CHKV Mombasa, Kilifi, Lamu, Kwale [33]
  A. circumluteolus RVFV, BBKV, NDUV, SMFV Garissa [4,36]
  A. fryeri DENV Mombasa, Kilifi, Lamu, Kwale [33]
  A. fulgens DENV, CHKV Mombasa, Kilifi, Lamu, Kwale [33]
  A. keniensis YFV Baringo [59]
  A. Luridus NDUV Tana River [4]
  A. mcintoshi RVFV, NDUV, PGAV, BUNV, BBKV, PGAV, SMFV, NRIV Garissa [4,11,36,40]
    DENV, CHKV Mombasa, Kilifi, Lamu, Kwale [33]
  A. ochraceus RVFV, NDUV, BUNV, BBKV, SNBV, SMFV Garissa [4,11,36,37,38]
    DENV, CHKV Mombasa, Kilifi, Lamu, Kwale [33]
  A. pembaensis RVFV Kilifi [4]
    DENV, CHKV Mombasa, Kilifi, Lamu, Kwale [33]
  A. sudanensis BBKV, SNBV, WNV Garissa [36]
    NDUV Tana River [39]
Anopheles An. funestus ONNV Kisumu [59]
    BUNV Kajiado [4]
    NRIV Tana River [4]
  An. gambiae BUNV Homabay [20]
  An. squamosus RVFV Garissa [11]
Culex Cx. bitaeniorhynchus RVFV Kilifi [11]
    NDUV Tana River [39]
  Cx. cinereus NDUV Busia [4]
  Cx. pipiens USUV Kisumu [4]
    NDUV Garissa, Tana River [38,39]
  Cx. poicilipes RVFV Kilifi [11]
  Cx. quinquefasciatus RVFV Baringo, Garissa [11,60]
    WNV, SNBV Garissa [36,60]
  Cx. rubinotus NDUV Baringo [4]
  Cx. univittatus RVFV Baringo [11]
    BUNV Homa Bay [20]
    SNBV West Pokot, Nakuru, Busia [4,37,61]
    WNV Garissa, Turkana, West Pokot [4,61]
  Cx. vansomereni NDUV Tana River [39]
    BBKV, SNBV Nakuru [4,37]
  Cx. zombaensis RVFV Nakuru [62]
    BBKV Kiambu [4]
Mansonia Mn. africana RVFV Nakuru, Baringo, Garissa [11,60,62]
    NDUV Baringo [4]
  Mn. uniformis RVFV Baringo, Garissa [40,60]
    NDUV Baringo [36]
Genera: A, Aedes; An, Anopheles; Cx, Culex; Mn, Mansonia. 1 Abbreviations: DENV—dengue virus, CHKV—chikungunya virus, RVFV—Rift Valley fever virus, NDUV—Ndumu virus, PGAV—Pongola virus, BUNV—Bunyamwera virus, BBKV—Babanki virus, SMFV—Semliki Forest virus, NRIV—Ngari virus, YFV—yellow fever virus, SNBV—Sindbis virus, WNV—West Nile virus, USUV—Usutu virus, ONNV—O’nyong’nyong virus.
 
Table 2. Summary of the dominant malaria and Bancroftian filariasis mosquito vectors distributed in Kenya.
Parasite Associated Human Ailment Dominant Mosquito Species Counties of Vector Distribution Reference
Plasmodium falciparum Malaria An. gambiae s.s., An. arabiensis, An. funestus, An. merus Kwale, Kilifi [71,75,81,93,94]
    An. gambiae ss, An. arabiensis, An. funestus Taita-Taveta, Lamu, Kajiado, Embu, Nakuru, Baringo, Bungoma, Kirinyaga, Kiambu, Busia, Siaya, Kakamega, Vihiga, Homabay, Migori, Kisii, Kisumu, Nandi
    An. gambiae ss, An. arabiensis Narok
    An. arabiensis, An. funestus Tana-River, Makueni, Machakos, Trans-Nzoia
    An. funestus Samburu, Isiolo, Garissa, Mombasa, Uasin-Gishu, Nyamira
    An. arabiensis Turkana
    An. gambiae ss Tharaka-Nithi
Wuchereria bancrofti Bancroftian filariasis An. gambiae sl, An. funestus, Cx. quinquefasciatus Kwale, Kilifi, Lamu [50,91,95]
Genera: AnAnophelesCxCulex.
 
Mosquito-related studies have been carried out in some of the mainlands surrounding lakes in Kenya, such as Lake Victoria and Lake Baringo due to the prevalence of malaria [17]. Other outbreaks such as Rift Valley fever near Lake Baringo also led to intensified surveillance on arbovirus mosquito vectors in the surrounding regions [4,18,19,20]. The favorable tropical climate and swampy areas around the lake regions throughout the year is among the factors favoring the high diversity of mosquito species [18,21]. A study by Lutomiah et al. [22] which recorded high numbers of Culex pipiens and Culex univittatus around the two lake regions additionally associated this abundance to highly humid conditions and the presence of migratory birds. Other lake regions in Kenya that are important for mosquito-related studies include areas around Lake Naivasha [23,24], Lake Bogoria, and Lake Nakuru [20,24] (Figure 1A,B).
Over the years, several malaria and arbovirus seropositive cases have been recorded in Kakamega and Busia located in the western part of Kenya [25,26,27]. In a study conducted in 2013, Kakamega and Busia showed high numbers of potential arbovirus vectors, with A. aegypti at 91.8% and 45.6%, respectively, of the total mosquitoes collected in the two regions [22]. Additionally, NDUV has been detected from Culex species collected from Busia [4]. Kakamega’s climate is characterized by high precipitation occurring throughout the year, most likely an influence of the Kakamega tropical rainforest while Busia is known to experience warm temperatures (annual mean temperature of 25 °C). These factors, among others, contribute to the high mosquito densities and consequent disease occurrence in the regions.

3. Overview of the Main Mosquito Genera of Public Health Importance in Kenya and Their Geographical Distribution

The main mosquito species associated with human etiologies in the country belong to four genera (Aedes, Anopheles, Culex, and Mansonia) as discussed below. Their distribution in Kenya has mainly been studied in disease endemic regions and as a result of outbreaks. These data are summarized in Table 1 and Table 2.

3.1. Aedes

Aedes represent a genus of mosquito that were originally known as tropical and subtropical mosquito species but have now been reported in almost all parts of the world apart from Antarctica. This genus comprises over 950 species normally identified by their black and white body coloration, preferential breeding in open water containers, and their daytime feeding, especially mornings and evenings [28]. Much interest in these mosquito species has been due to their role as major vectors of arboviruses across the globe. For instance, in various islands of the south pacific, A. polynesiensis—a primary vector of Wuchereria bancrofti—has also been identified as an endemic dengue vector [29]. Aedes scutellaris, a native species of Papua New Guinea, has also been linked to dengue outbreaks around the region and other pacific islands [30,31]. Aedes aegypti and A. albopictus of African and Asian origins, respectively, are globally known for their invasive nature and role in transmitting viruses that cause chikungunya, dengue fever, yellow fever, Zika, and encephalitis [32]. The success of these species in virus transmission has been attributed to three mechanisms: interaction of vector and the host, transovarial transmission, and sexual mating [28,33].
Kenya harbors more than 80 different Aedes species (http://www.wrbu.org) but not all have been associated with the spread of mosquito viruses. An important species is A. ochraceus which is highly distributed in the arid regions of north-eastern Kenya and linked to the spread of Rift Valley fever virus (RVFV), NDUV, Bunyamwera virus (BUNV), Babanki virus (BBKV), Sindbis virus (SNBV), and Semliki Forest virus (SMFV) in the region [4,11,34,35,36,37,38]. Additionally, this species has also been reported to be associated with RVFV, dengue virus (DENV), and chikungunya virus (CHKV) in coastal counties (Kwale, Kilifi, Mombasa, Lamu) [11,33,39], and some parts of in the western region [22]. Aedes mcintoshi and A. sudanensis are also important arbovirus vectors occasionally reported in coastal and north-eastern regions [4,11,14,22,33,36,40], while A. circumluteolus have been reported in Busia and Garissa counties [4,22,36]. Other Aedes secondary vectors of arboviruses such as: A. tricholabis [4,33], A. Albicosta [33], A. fulgens [33], A. fryeri [33], A. pembaensis [33], and A. Luridus [4] have been identified in various parts of the country and mostly along the Kenyan coastline. Aedes africanus and A. keniensis sampled from Baringo county represent the only field collected Aedes spp. in which successful yellow fever virus (YFV) has been detected in Kenya [41]. Moreover, other Aedes spp. such as Avittatus and Abromeliae have shown competence to DENV and YFV, even though no field detection has been recorded [42,43].
Aedes aegypti, the principal vector of dengue, chikungunya, and other emerging arboviruses is also widely distributed in Kenya [4,33,44] but not uniformly, with more occurrence being recorded in the lowlands [22]. It exists in two forms that were found coexisting sympatrically in Rabai, along the coast of Kenya [45]: the domestic, light-colored A. aegypti aegypti and the sylvatic form, A. aegypti formosus, which is dark in color [45,46]. In addition to morphological differences, definite behavioral variabilities have also been observed between the two forms of A. aegypti [46]. They include a longer developmental time and indoor breeding tendency of the domestic form as opposed to the ancestral sylvatic form that usually breed in forests tree holes and develop within a shorter period [47,48]. This explains the occurrence of A. aegypti formosus in vegetated ecosystems and previous documentation in western Kenya near Kisumu city and in the Kakamega forest [46]. Additionally, the sylvatic type is predominantly zoophilic as compared to the domestic type, which prefers humans for their blood meals.
Rapid urbanization in Kenya, facilitated by the increase in both domestic and international trade has led to major ecological and social changes [14]. These transformations have attracted A. aegypti to urban centers with up to three times the population size compared to rural areas due to the accumulation of non-biodegradable human-made containers that serve as conducive breeding sites to these vectors [12,49,50]. It is, thus, evident that if effective vector control strategies are not enhanced, the rate of arbovirus disease transmission is bound to increase, especially in urban centers.
Sporadic arboviral disease outbreaks associated with Aedes spp. have occurred over several decades in Kenya of which some have shown a tendency to recur in the same or new populations. For example, dengue fever in 1982 (Malindi, coastal region) [51], 2011 (Mandera, north-eastern) [52], and 2013–2014, 2017 (coastal region counties) [12,53]; Rift Valley fever in 1997–1998 (Garissa, north-eastern) [10], 2006–2007 (Garissa and Baringo) [11], 2014–2015, 2018 (north-eastern) [54]; yellow fever in 1992–1993 (Kerio Valley, Rift Valley region) [41]; chikungunya in 2004 (Lamu, coastal region) [55], 2016 (Mandera, north-eastern) [56], and 2018 (Mombasa, coastal region) [13].

3.2. Anopheles

This genera comprises mosquito species that are commonly identified by long palps, dark-brown body coloration, discrete black and white scales located at the wings and a characteristic resting position (stomach area pointing upwards) [63]. Over 460 anopheline species have been recognized across the world, with approximately 7% known to transmit Plasmodium parasites that cause malaria in humans [64]. Malaria is endemic in 91 countries, with about 40% of the world’s population at risk. The latest World Health Organization (WHO) data showed that in 2017, there were 219 million cases of malaria and estimated 435,000 malaria deaths across the world. Out of these, Africa accounted for the most cases and deaths (92% and 93%), respectively [65].
Africa is home to more than 140 anopheline species, of which six of them are primary vectors of malaria parasites (P. falciparumP. vivaxP. ovale, and P. malariae) [66,67]. They include Anopheles gambiaeAnopheles arabiensisAnopheles funestusAnopheles niliAnopheles moucheti, and Anopheles coluzzii [67,68]. However, other than the primary vectors that contribute to 95% of malaria transmission in Africa, secondary Anopheles’ vectors have also been recorded and contribute 5% of the overall transmission. For instance, An. pharoensis and An. ziemanni were found to harbor the malaria parasite P. vivax in Ethiopia at irrigated rice plantations [69]. In Tanzania, An. ziemanniAn. Coustani, and An. squamosus have also been linked to malaria transmission as secondary vectors [70].
In Kenya, Anopheles spp. are a major concern in the public health sector due to their role as malaria transmission agents. In a country-wide study by Okiro et al. [71], out of 166,632 hospital admissions, western Kenya had the highest number of cases (70%) with the Rift Valley highlands (45%) and Kenyan coast (22%) coming in at 2nd and 3rd, respectively. Each year, approximately 3.5 million new malaria cases and 10,700 deaths are recorded, with those residing in the western part of Kenya being at high risk of contracting the disease [72].
The main vectors of malaria in Kenya include the An. gambiae complex (An. gambiae ss, An. arabiensis, An. merus) and An. funestus. These transmit all four Plasmodium parasites with P. falciparum being the most common, accounting for 99% of all malaria cases within the country [73]. Anopheles arabiensis and An. gambiae have been shown to coexist sympatrically, especially in the coastal counties Kilifi and Kwale, and Nyanza counties Kisumu and Siaya [74]. However, evidence has shown that over time An. arabiensis started becoming the more predominant vector where the two coincide [75,76,77]. Anopheles merus is largely distributed within a 25 km radius from the Kenyan coast due to its need to breed in saline water [71,78]. See Figure 1C and Table 2.
Secondary vectors of malaria are also wide spread within the country. For instance, An. pharoensis sampled from a rice irrigation scheme in Mwea, central Kenya, constituted 1.3% and 0.68% P. falciparum by ELISA (enzyme-linked immunosorbent assay) and dissection methods, respectively [79]. This species has also been reported in western region highlands [80]. Anopheles nili has been identified in 26 scattered sites along the coastal areas: Trans Nzoia, Taita and Taveta area, Kaimosi Forest in Vihiga county, Mwea tebere rice plantation, and Thika [81]. Anopheles coustani and An. ziemanni sampled from Taveta and western regions, respectively, have also been implicated as potential secondary vectors [14,82]. Regardless of the country-wide distribution of these potential secondary vectors, their actual role in the transmission of malaria parasites in the country is not well known.
Kenya has been stratified into four malaria epidemiological zones with risk factors determined usually by temperature, altitude, rainfall patterns, and malaria prevalence [83]. These zones are: a) The endemic areas in coastal regions and Lake Victoria in the western region. These areas are characterized by altitudes ranging from 0–1300 m above sea level and stable high malaria prevalence throughout the year. b) Highland epidemic prone areas that experience seasonal malaria transmission with considerable year-to-year variations around the western highlands and between 5–20% prevalence. c) Seasonal malaria transmission areas which include arid and semi-arid areas in the northern and south-eastern parts of the country where they experience short episodes of intense malaria transmission during the rainy seasons. d) Low malaria risk areas in the central highlands of Kenya such as Nairobi, where temperatures are too low for the survival of malaria Plasmodium parasites [83]. However, with changes in annual climatic patterns and increase in global warming, previously malaria-free regions may soon become endemic areas. For instance, mosquito species such as An. arabiensis which were not known to inhabit central Kenya highlands are now being reported [66].
Although the government of Kenya has established various measures that have seen a reduction in malaria prevalence especially in major endemic regions [83], this has not been the case for some counties. In October 2017 and February 2018, malaria outbreaks hit the arid counties of Marsabit, Baringo, and West Pokot leading to numerous hospitalization cases and deaths [84]. This calls for more cohesive policies in the fight against malaria and their respective anopheline vectors.
Apart from the spread of malariaAnopheles spp. are associated with spread of other vector-borne diseases such as: canine heartworm (Dirofilaria immitis) common in the Americas [85,86], lymphatic filariasis, and O’nyong’nyong fever. The first case of O’nyong’nyong virus (ONNV) was reported in Uganda in 1959 and spread through the Victoria basin to western Kenya by 1960 [87]. From this time onwards, this virus has repeatedly been isolated from An. funestus and An. gambiae in different localities within Kenya providing strong evidence that these two mosquito species are indeed the primary vectors [59,88]. Other mosquito-borne viruses detected from Anopheles spp. in the country include: Ngari virus (NRIV) in the Tana River (An. funestus) [4] and BUNV in Homabay (An. gambiae) [20], as summarized in Table 1. Additionally, An. funestus and An. gambiae are also associated with the spread of lymphatic filariasis in the Kenyan coast from Lamu to Kwale where ecological factors favor its transmission [89,90,91,92].

3.3. Culex

Drab in color, the Culex genera comprises up to 1000 species with a fairly weak flying tendency and generally found in all zoogeographical areas ranging from the tropics to cooler temperate regions [96]. Due to their proximity to human settlements, these species are often referred to as common house mosquitoes. They have also been shown to prefer their blood meals from birds that feed at dawn and dusk [97]. Among the multiple Culex spp., Cx. pipiens complex is the most widely distributed across the globe. It comprises Cx. Pipiens L, Cx. quinquefasciatus Say, Cx. pipiens pallens Coquillett, Cx. australicus Dobrotworsky and Drummond, and an autogenous Cx. pipiens subspecies Cx. pipiens molestus Forskal. Worth noting is that the complex species are not easily distinguished morphologically and can only be separated through a combination of molecular techniques, and behavioral and physiological traits [98,99].
Culex spp. are globally known as vectors of human, avian, and animal pathogens such as lymphatic filariasis primarily vectored by Cx. pipiens [100,101]. This disease is caused by a nematode called W. bancrofti which is currently in more than 52 countries where 856 million people live in disease endemic regions (South-East Asia (66%) and African regions (33%)) being at high risk [102]. Culex spp. are also associated with transmission of viruses, with WNV being the most common. The virus is often amplified by Cx. pipiens quinquefasciatus and maintained in a cycle involving humans and birds although other species of the pipiens complex have shown competence in spreading the virus [60,97,103,104]. Originally isolated in Uganda in 1937, this virus has spread globally and has been reported in almost all continents [105]. Other pathogens vectored by Culex spp. include the Saint Louis encephalitis virus (SLEV) [106], equine encephalitis virus (EEV) [107], dog heartworm (Dirofilaria immitis), SNBV, Plasmodium relictum (bird malarias) [103], and RVFV. Whether or not Zika virus is vectored by Culex spp. has been a topic of debate. Sammy et al. [108] noted the possibility of Cx. quinquefasciatus playing a vectorial role in Zika prone areas in Brazil due to their higher abundance compared to A. aegypti, which is a commonly known Zika transmission vector. Later on, Amraoui et al. [109] and Huang et al. [110] rejected this possibility. However, a recent study by Phumee at al. [111] evidenced that vertical transmission of Zika virus by Cx. quinquefasciatus was indeed possible.
According to the Walter–Reed Bioinformatics Unit (WRBU), Kenya harbors approximately 42 Culex spp. (http://www.wrbu.org). The ones with the most public health significance include members of the Cx. pipiens complex, Cx. pipiens L. and Cx. quinquefasciatus Say, whose success in colonizing both urban and rural environs have been attributed to their larval ability to develop in a variety of aquatic habitats [14]. These mosquitoes are highly distributed in Kenyan coast counties and associated with the spread of bancroftian filariasis [90,91,95] and cases of RVF [11,112]. A study by Atoni et al. [17] recorded high numbers of Cx. quinquefasciatus in Kwale county, which had abundant vertebrate viruses based on metagenomic analysis. These species have also been implicated in entomologic studies focusing on WNV, SNBV, and NDUV in Garissa county [38,39,60], RVF in Baringo, Garissa, and Nakuru counties [11,19,60], and Usutu virus in Kisumu [4].
Culex univittatus is another common Culex spp. distributed within the country. Its first vertical natural transmission of WNV was evidenced in the Rift Valley province in a study by Lanciotti et al. [61]. In Baringo county, it has been implicated as a vector of the RVFV [19] and BUNV in the Lake Victoria region [20]. In an entomologic survey by Lutomiah et al. [22], on the abundance of potential mosquito vectors, this species was found to be highly abundant in Kisumu (37%) and Naivasha (21.6%), even though no pathogen screening was conducted.
Other disease important Culex spp. in the country include Cx. bitaeniorhynchus, Cx. cinereus, Cx. poicilipesCx. rubinotus, Cx. Vansomereni, and Cx. zombaensis in which various etiological pathogens have been isolated as summarized in Table 1. Vector competence involving some of these species has also been witnessed. For instance, in a study by Turell et al. [23], Cx. zombaensis collected around the Lake Naivasha region showed high competence for RVFV with an 89% infection rate.

3.4. Mansonia

The Mansonia mosquito species belong to the sub-family Culicinae and are normally characterized by their large body size and asymmetrical wing scale structure with sparkling on their wing veins and legs. They show some resemblance with Aedes, Culex, and Coquillettidia mosquito but the simplicity of their tarsal claws in structure and a truncated abdomen in females sets it apart [113]. Furthermore, Mansonia preferably breed in ponds and permanent waters with aquatic plants where larvae can burrow into the dead plants at the bottom or cling to the roots of the live ones [114]. Its genera comprise 25 globally distributed species in two subgenera: Mansonioides (10 species) and Mansonia (15 species).
The distribution of these species comes with increased vectorial role of human etiologies. Mansonia titillans, a common species in the Americas, is a known vector of Venezuelan equine encephalitis [115]. Recently, Argentina detected SLEV and BUNV for the first time from this species, proving its competent nature to transmit the viruses [116]. In south-east Asia, Mn. bonneae and Mn. dives have been linked to various cases of Brugian and lymphatic filariasis [117]. Africa, as one of the most affected regions of vector-borne diseases, harbors two main and probably the most common Mansonia spp. (Mn. africana and Mn. uniformis). These species have been reported to vector W. bancrofti’s lymphatic filariasis [118,119], RVF [34], Zika [120], among other diseases. Kenya is not an exception, as studies have shown that the two Mansonia spp. are distributed within the country and harbor pathogens of human health importance [4,11,36,40,60].
LaBeaud et al. [60] showed that Mansonia mosquitoes could have significantly contributed to the vectorial transmission of RVF in the 2006–2007 outbreak in the north-eastern region. Out of the 12,080 mosquitos collected during the study, 682 were identified to be Mansonia spp. Further investigation based on molecular screening identified three out of eight pools of Mansonia spp. to be positive for RVFV. Mansonia, like many other female mosquitoes, feed on vertebrate blood for egg development. These vertebrates can lead to amplification of a disease in case of outbreaks. Virus screening from blood-fed Mansonia spp. by Lutomiah et al. [40] during this same RVF outbreak, showed that goats and sheep were the greatest amplifiers of the virus.
Owing to the fact that Mn. uniformis and Mn. africana preferably breed around permanent water bodies, flooded lagoons, and swamps, they have been shown to dominate lake regions in the country. A study by Lutomiah et al. [22] on the abundance of mosquito vectors in various ecological zones in the country revealed high abundance of Mansonia spp. in Baringo (71%) and Kisumu (23%), the home places of Lake Baringo and Lake Victoria. Interestingly, it is here (Baringo) that positive strains of RVFV and NDUV had earlier been detected in Mn. uniformis and Mn. africana [11,36]. This was further evidenced by Ajamma et al. [18], where these species dominated in abundance in the islands and mainlands of both Lake Victoria and Lake Baringo.
Even though Zika virus and W. bancrofti have been detected from Mansonia spp. in some African states [118,120], this has not been the case in Kenya. In a study at the Kenyan Tana delta on vectorial potential of Mansonia spp. to transmit W. bancrofti; all 236 species collected tested negative on PCR (polymerase chain reaction) analysis [121]. However, the study recommended further assessment to be done by infecting Mansonia spp. experimentally with W. bancrofti microfilaria to identify whether or not they can support development of microfilaria up to the infective stages.
 

References

  1. World Health Organization. Global Vector Control Response 2017–2030. 2017. Available online: https://apps.who.int/iris/bitstream/handle/10665/259205/9789241512978-eng.pdf;jsessionid=9C11656832A16B1404639714E44BF08B?sequence=1 (accessed on 4 March 2019)
  2. Braack, L.; Gouveia De Almeida, A.P.; Cornel, A.J.; Swanepoel, R.; De Jager, C. Mosquito-borne arboviruses of African origin: Review of key viruses and vectors. Parasites Vectors 2018, 11, 29, doi:1186/s13071-017-2559-9.
  3. Centers for Disease Control. Lymphatic Filariasis: Epidemiology and Risk Factors, 2019. Available online: https://www.cdc.gov/parasites/lymphaticfilariasis/epi.html (accessed on 4 March 2019).
  4. Ochieng, C.; Lutomiah, J.; Makio, A.; Koka, H.; Chepkorir, E.; Yalwala, S.; Mutisya, J.; Musila, L.; Khamadi, S.; Richardson, J.; et al. Mosquito-borne arbovirus surveillance at selected sites in diverse ecological zones of Kenya; 2007–2012. J. 2013, 10, 140, doi:10.1186/1743-422X-10-140.
  5. Altizer, S.; Dobson, A.; Hosseini, P.; Hudson, P.; Pascual, M.; Rohani, P. Seasonality and the dynamics of infectious diseases. Lett. 2006, 9, 467–484, doi:10.1111/j.1461-0248.2005.00879.x.
  6. Patz,A.; Githeko, A.K.; McCarty, J.P.; Hussein, S.; Confalonieri, U.; DeWet, N. Climate change and Infectious Diseases. World Health Organization. 2003. Available online: https://www.who.int/globalchange/publications/
    climatechangechap6.pdf (accessed on 4 March 2019).
  7. Shi, Z. Impact of Climate Change on the Global Environment and Associated Human Health. Res. 2018, 5, e4934, doi:10.4236/oalib.1104934.
  8. Himeidan, Y.E.; Kweka, E.J. Malaria in East African highlands during the past 30 years: Impact of environmental changes. Physiol. 2012, 3, 315, doi:10.3389/fphys.2012.00315.
  9. Owino, E.A. Aedes mosquitoes and emerging neglected diseases of Kenya. Int. J. Mosq. Res. 2018, 5, 5, 2348–5906
  10. Woods, C.W.; Karpati, A.M.; Grein, T. McCarthy, N.; Gaturuku, P.; Muchiri, E.; Dunster, L.; Henderson, A.; Khan, A.S.; Al, R.S. An Outbreak of Rift Valley Fever in Northeastern Kenya, 1997–98. Infect. Dis. 2002, 8, 138–144, doi:10.3201/eid0802.010023.
  11. Sang, R.; Kioko, E.; Lutomiah, J.; Warigia, M.; Ochieng, C.; O’Guinn, M.; Lee, J.S.; Koka, H.; Godsey, M.; Hoel, D.; et al. Rift Valley fever virus epidemic in Kenya, 2006/2007: The entomologic investigations. J. Trop. Med. Hyg. 2010, 83, 28–37, doi:10.4269/ajtmh.2010.09-0319.
  12. Lutomiah, J.; Barrera, R.; Makio, A.; Mutisya, J.; Koka, H.; Owaka, S.; Koskei, E.; Nyunja, A.; Eyase, F.; Coldren, R.; et al. Dengue Outbreak in Mombasa City, Kenya, 2013–2014: Entomologic Investigations. PLoS Negl. Trop. Dis. 2016, 10, e0004981, doi:10.1371/journal.pntd.0004981.
  13. World Health Organization. Chikungunya—Mombasa, Kenya. 2018. Available online: https://www.who.int/
    csr/don/27-february-2018-chikungunya-kenya/en/ (accessed on 10 March 2019).
  14. Mwangangi, J.M.; Midega, J.; Kahindi, S.; Njoroge, L.; Nzovu, J.; Githure, J.; Mbogo, C.M.; Beier, J.C. Mosquito species abundance and diversity in Malindi, Kenya and their potential implication in pathogen transmission. Res. 2012, 110, 61–71, doi:10.1007/s00436-011-2449-6.
  15. Ogola, E.O.; Odero, J.O.; Mwangangi, J.M.; Masiga, D.K.; Tchouassi, D.P. Population genetics of Anopheles funestus, the African malaria vector, Kenya. Parasites Vectors 2019, 12, 15, doi:10.1186/s13071-018-3252-3.
  16. Atoni, E.; Wang, Y.; Karungu, S.; Waruhiu, C.; Zohaib, A.; Obanda, V.; Agwanda, B.; Mutua, M.; Xia, H.; Yuan, Z. Metagenomic virome analysis of Culex mosquitoes from Kenya and China. Viruses 2018, 10, 30, doi:10.3390/v10010030.
  17. Minakawa, N.; Dida, G.O.; Sonye, G.O.; Futami, K.; Njenga, S.M. Malaria vectors in Lake Victoria and adjacent habitats in western Kenya. PLoS ONE 2012, 7, e32725, doi:10.1371/journal.pone.0032725.
  18. Ajamma, Y.K.; Villinger, J.; Omondi, D.; Salifu, D.; Onchuru,T.O.; Njoroge, L.; Muigai, A.W.T.; Masiga, D.K. Composition and genetic diversity of mosquitoes (Diptera: Culicidae) on Islands and mainland shores of Kenya’s lakes Victoria and baringo. Med. Entomol. 2016, 53, 1348–1363, doi:10.1093/jme/tjw102.
  19. Ondiba, I.M.; Oyieke, F.A.; Nyamongo, I.K.; Estambale, B.B. Diversity, distribution and abundance of potential rift valley fever vectors in Baringo County, Kenya. J. Mosq. Res. 2017, 4, 42–48.
  20. Ajamma, Y.U.; Onchuru, T.O.; Ouso, D.O.; Omondi, D.; Masiga, D.K.; Villinger, J. Vertical transmission of naturally occurring Bunyamwera and insect-specific flavivirus infections in mosquitoes from islands and mainland shores of Lakes Victoria and Baringo in Kenya. PLoS Negl. Trop. Dis. 2018, 12, e0006949, doi:10.1371/journal.pntd.0006949.
  21. Ofulla, A.V.O.; Karanja, D.; Omondi, R.; Okurut, T.; Matano, A.; Jembe, T.; Abila, R.; Boera, P.; Gichuki, J. Relative abundance of mosquitoes and snails associated with water hyacinth and hippo grass in the Nyanza gulf of Lake Victoria. Lakes Reserv. Res. Manag. 2010, 15, 225–271, doi:1111/j.1440-1770.2010.00434.x.
  22. Lutomiah, J.; Bast, J.; Clark, J.; Richardson, J.; Yalwala, S.; Oullo, D.; Mutisya, J.; Mulwa, F.; Musila, L.; Khamadi, S.; et al. Abundance, diversity, and distribution of mosquito vectors in selected ecological regions of Kenya: Public health implications. Vector Ecol. 2013, 38, 134–142, doi:10.1111/j.1948-7134.2013.1201.
  23. Turell, M.J.; Lee, J.S.; Richardson, J.H.; Sang, R.C.; Kioko, E.N.; Agawo, M.O.; Pecor, J.; O’guinn, M.L. Vector Competence of Kenyan Culex zombaensis And Culex quinquefasciatus mosquitoes for Rift Valley Fever Virus. Am. Mosq. Control Assoc. 2007, 23, 378–382, doi:10.2987/5645.1.
  24. Britch, S.C.; Binepal, Y.S.; Ruder, M.G.; Kariithi, H.M.; Linthicum, K.J.; Anyamba, A.; Small, J.L.; Tucker, C.J.; Ateya, L.O.; Oriko, A.A.; et al. Rift Valley Fever Risk Map Model and Seroprevalence in Selected Wild Ungulates and Camels from Kenya. PLoS ONE 2013, 8, e66626, doi:10.1371/journal.pone.0066626.
  25. Tuno, N.; Okeka, W.; Minakawa, N.; Takagi, M.; Yan, G. Survivorship of Anopheles gambiae sensu stricto (Diptera: Culicidae) Larvae in Western Kenya Highland Forest. Med. Entomol. 2005, 42, 270–277.doi:10.1093/jmedent/42.3.270.
  26. Doucoure, S.; Drame, P.M. Salivary biomarkers in the control of mosquito-borne diseases. Insects 2015, 6, 961–976, doi:10.3390/insects6040961.
  27. Iwashita, H.; Higa, Y.; Futami, K.; Lutiali, P.A.; Njenga, S.M.; Nabeshima, T.; Minakawa, N. Mosquito arbovirus survey in selected areas of Kenya: Detection of insect-specific virus. Med. Health 2018, 46, doi:10.1186/s41182-018-0095-8.
  28. Bravo, L.; Roque, V.G.; Brett, J.; Dizon, R.; L’Azou, M. Epidemiology of dengue disease in the Philippines (2000–2011): A systematic literature review. PLoS Negl. Trop. Dis. 2014, 8, e3027, doi:10.1371/journal.pntd.0003027.
  29. Musso, D.; Rodriguez-Morales, A.J.; Levi, J.E.; Cao-Lormeau, V.M.; Gubler, D.J. Unexpected outbreaks of arbovirus infections: Lessons learned from the Pacific and tropical America. Lancet Infect. Dis. 2018, 18, e355–e361, doi:10.1016/ S1473-3099(18)30269-X.
  30. Carrington, L.B.; Simmons, C.P. Human to mosquito transmission of dengue viruses. Immunol. 2014, 5, 290, doi:10.3389/fimmu.2014.00290.
  31. Sharp, T.M.; Mackay, A.J.; Santiago, G.A.; Hunsperger, E.; Nilles, E.J.; Perez-Padilla, J.; Tikomaidraubuta, K.S.; Colon, C.; Amador, M.; Chen, T.; et al. Characteristics of a dengue outbreak in a remote Pacific Island chain—Republic of the Marshall Islands, 2011–2012. PLoS ONE 2014, 9, e108445, doi:10.1371/journal.pone.0108445.
  32. Kraemer, M.U.G.; Sinka, M.E.; Duda, K.A.; Mylne, A.Q.N.; Shearer, F.N.; Barker, C.M.; Moore, C.G.; Carvalho, R.G.; Coelho, G.E.; Bortel, W.V. et al. The global distribution of the arbovirus vectors Aedes aegypti and albopictus. elife 2015, 4, e08347, doi:10.7554/eLife.08347.
  33. Ngala, J.C.; Schmidt Chanasit, J. Entomological Coinfections of Arboviruses Dengue and Chikungunya Viruses along the Coastline of Kenya. Mosq. Res. 2018, 8, 1, doi:10.5376/jmr.2018.08.0001.
  34. Arum, S.O.; Weldon, C.W.; Orindi, B.; Landmann, T.; Tchouassi, D.P.; Affognon, H.D.; Sang, R. Distribution and diversity of the vectors of Rift Valley fever along the livestock movement routes in the northeastern and coastal regions of Kenya. Parasites Vectors 2015, 8, 294, doi:10.1186/s13071-015-0907-1.
  35. Tchouassi, D.P.; Bastos, A.D.S.; Sole, C.L.; Diallo, M.; Lutomiah, J.; Mutisya, J.; Mulwa, F.; Borgemeister, C.; Sang, R.; Torto, B.; et al. Population Genetics of Two Key Mosquito Vectors of Rift Valley Fever Virus Reveals New Insights into the Changing Disease Outbreak Patterns in Kenya. PLoS Negl. Trop. Dis. 2014, 8, e3364 , doi:10.1371/journal.pntd.0003364.
  36. Crabtree, M.; Sang, R.; Lutomiah, L.; Richardson, J.; Miller, B. Arbovirus surveillance of mosquitoes collected at sites of active Rift Valley fever virus transmission: Kenya, 2006– J. Med. Entomol. 2009, 46, 961–964, doi:10.1603/033.046.0431.
  37. Sigei, F.; Nindo, F.; Mukunzi, S.; Ng’ang’a, Z.; Sang, R. Evolutionary analyses of Sindbis virus strains isolated from mosquitoes in Kenya. Virol. 2018, 163, 2465–2469, doi:10.1007/s00705-018-3869-8.
  38. Lutomiah, J.; Ongus, J.; Linthicum, K.J.; Sang, R. Natural Vertical Transmission of Ndumu Virus in Culex pipiens (Diptera: Culicidae) Mosquitoes Collected as Larvae. Med. Entomol. 2014, 51, 1091–1095, doi:10.1603/me14064.
  39. Sang, R.; Lutomiah, J.; Said, M.; Makio, A.; Koka, H.; Koskei, E.; Nyunja, A.; Owaka, S.; Matoke-Muhia, D.; Bukachi, S.; et al. Effects of irrigation and rainfall on the population dynamics of rift valley fever and other arbovirus mosquito vectors in the epidemic-prone Tana-River County, Kenya. Med. Entomol. 2017, 54, 460–470, doi:10.1093/jme/tjw206.
  40. Lutomiah, J.; Omondi, D.; Masiga, M.; Mutai, C.; Mireji, P.O.; Ongus, J.; Linthicum, K.J.; Sang, R. Blood Meal Analysis and Virus Detection in Blood-Fed Mosquitoes Collected During the 2006–2007 Rift Valley Fever Outbreak in Kenya. Vector-Borne Zoonotic Dis. 2014, 14, 656–664, doi:10.1089/vbz.2013.1564.
  41. Sanders, E.J.; Marfin, A.A.; Tukei, P.M.; Kuria, G.; Ademba, G.; Agata, N.N.; Ouma, J.O.; Cropp, C.B.; Karabatsos, N.; Reiter, P.; et al. First recorded outbreak of yellow fever in Kenya, 1992–1993. II. Entomologic investigations. J. Trop. Med. Hyg. 1998, 59, 644–649.
  42. Ellis, B.R.; Sang, R.C.; Horne, K.M.; Higgs, S.; Wesson, D.M. Yellow fever virus susceptibility of two mosquito vectors from Kenya, East Africa. R. Soc. Trop. Med. Hyg. 2012, 106, 387–389, doi:10.1016/j.trstmh.2012.02.007.
  43. Mulwa, F.; Lutomiah, J.; Chepkorir, E.; Okello, S.; Eyase, F.; Tigoi, C.; Kahato, M.; Sang, R. Vector competence of Aedes bromeliae and Aedes vitattus mosquito populations from Kenya for chikungunya virus. PLoS Negl. Trop. Dis. 2018, 12, doi:10.1371/journal.pntd.0006746.
  44. Sang, R.; Arum, S.; Chepkorir, E.; Mosomtai, G.; Tigoi, C.; Sigei, F.; Lwande, O.W.; Landmann, T.; Affognon, H.; Ahlm, C.; et al. Distribution and abundance of key vectors of Rift Valley fever and other arboviruses in two ecologically distinct counties in Kenya. PLoS Negl. Trop. Dis. 2017, 11, e0005341, doi:10.1371/journal.pntd.0005341.
  45. Powell, J.; Tabachnick, W. History of domestication and spread of Aedes aegypti—A Review. Memórias do Instituto Oswaldo Cruz 2013, 108, 11–17, doi:10.1590/0074-0276130395.
  46. Yalwala, S.; Clark, J.; Oullo, D.; Ngonga, D.; Abuom, D.; Wanja, E.; Bast, J. Comparative efficacy of existing surveillance tools for Aedes aegypti in Western Kenya. Vector Ecol. 2015, 40, 301–307, doi:10.1111/jvec.12168.
  47. Ndenga, B.A.;, Mutuku, F.M.; Ngugi, H.N.; Mbakaya, J.O.; Aswani, P.; Musunzaji, P.S.; Vulule, J.; Mukoko, D.; Kitron, U.; LaBeaud, A.D. Characteristics of Aedes aegypti adult mosquitoes in rural and urban areas of western and coastal Kenya. PLoS ONE 2017, 12, e0189971, doi:10.1371/journal.pone.0189971.
  48. McBride, C.S.; Baier, F.; Omondi, A.B.; Spitzer, S.A.; Lutomiah, J.; Sang, R.; Ignell, R.; Vosshall, L.B.; Evolution of mosquito preference for humans linked to an odorant receptor. Nature 2014, 515, 222–227, doi:10.1038/nature13964.
  49. Monath, T. Dengue: The risk to developed and developing countries. Natl. Acad. Sci. USA 1994, 91, 2395–2400.
  50. Ngugi, H.N.; Mutuku, F.M.; Ndenga, B.A.; Musunzaji, P.S.; Mbakaya, J.O.; Aswani, P.; Irungu, L.W.; Mukoko, D.; Vulule, J.; Kitron, U.; et al. Characterization and productivity profiles of Aedes aegypti (L.) breeding habitats across rural and urban landscapes in western and coastal Kenya. Parasites Vectors 2017, 10, 331, doi:10.1186/s13071-017-2271-9.
  51. Johnson, B.; Musoke, S.; Ocheng, D.; Gichogo, A.; Rees, P. Dengue-2 Virus In Kenya. Lancet 1982, 320, 208–209.
  52. Obonyo, M.; Fidhow, A.; Ofula, V. Investigation of laboratory confirmed dengue outbreak in north-eastern Kenya, 2011. PLoS ONE 2018, 13, e0198556, doi:10.1371/journal. pone.0198556.
  53. Voice of Africa. Kenya Health Officials Issue Alert Over Dengue Fever Outbreak. 2017. Available online: https://www.voanews.com/a/kenya-health-officials-alert-dengue-fever-outbreak/3843040.html (accessed on 25 March 2019).
  54. World Health Organization. Rift Valley fever—Kenya. 2018. Available online: https://www.who.int/csr/don/
    18-june-2018-rift-valley-fever-kenya/en/ (accessed on 25 March 2019).
  55. Sergon, K.; Njuguna, C.; Kalani, R.; Ofula, V.; Onyango, C.; Konongoi, L.S.; Bedno, S.; Burke, H.; Dumilla, A.M.; Konde, J.; et al. Seroprevalence of Chikungunya Virus (CHIKV) Infection on Lamu Island, Kenya, October 2004. J. Trop. Med. Hyg. 2008, 78, 333–337, doi:10.4269/ajtmh.2008.78.333.
  56. Berry, I.M.; Eyase, F.; Pollett, S.; Konongoi, S.L.; Joyce, M.G.; Figueroa, K.; Ofula, V.; Koka, H.; Koskei, E.; Nyunja, A.; et al. Global Outbreaks and Origins of a Chikungunya Virus Variant Carrying Mutations Which May Increase Fitness for Aedes aegypti: Revelations from the 2016 Mandera, Kenya Outbreak. J. Trop. Med. Hyg. 2019, 100, 1249-1257, doi:10.4269/ajtmh.18-0980.
  57. Konongoi, S.L.; Ofula, V.; Nyunja, A.; Owaka, S.; Koka, H.; Makio, A.; Koskei, E.; Eyase, F.; Langat, D.; Schoepp, R.J.; et al. Detection of dengue virus serotypes 1, 2 and 3 in selected regions of Kenya: 2011–2014. J. 2016, 13, 182, doi:10.1186/s12985-016-0641-0.
  58. Konongoi, S.L.; Nyunja, A.; Ofula, V.; Owaka, S.; Koka, H.; Koskei, E.; Eyase, F.; Langat, D.; Mancuso, J.; Lutomiah, J.; et al. Human and entomologic investigations of chikungunya outbreak in Mandera, Northeastern Kenya, 2016. PLoS ONE 2018, 13, e0205058, doi:10.1371/journal.pone.0205058.
  59. Johnson, B.K.; Gichogo, A.; Gitau, G.; Patel, N.; Ademba, G.; Kirui, R.; Highton, R.B.; Smith, D.H. Recovery of o’nyong-nyong virus from Anopheles funestus in Western Kenya. R. Soc. Trop. Med. Hyg. 1981, 75, 239–241.
  60. LaBeaud, A.D.; Sutherland, L.J.; Muiruri, S.; Muchiri, E.M.; Gray, L.R.; Zimmerman, P.A.; Hise, A.G.; King, C.H. Arbovirus prevalence in mosquitoes, Kenya. Infect. Dis. 2011, 17, 233–241, doi:10.3201/eid1702.091666.
  61. Miller, B.R.; Nasci, R.S.; Godsey, M.S.; Savage, H.M.; Lutwama, J.J.; Lanciotti, R.S.; Peters, C.J. First field evidence for natural vertical transmission of West Nile virus in Culex univittatus complex mosquitoes from Rift Valley province, Kenya. J. Trop. Med. Hyg. 2000, 62, 240–246, doi:10.4269/ajtmh.2000.62.240.
  62. Logan, T.M.; Linthicum, K.J.; Ksiazek, T.G. Isolation of Rift Valley fever virus from mosquitoes collected during an outbreak in domestic animals in Kenya. Med. Entomol. 1992, 28, 293–295.
  63. Centers for Disease Control. Anopheles 2015. Available online: https://www.cdc.gov/malaria/
    about/biology/index.html#tabs-1-5 (accessed on 25 March 2019).
  64. Harbach, R.E. The Culicidae (Diptera): A review of taxonomy, classification and phylogeny. Zootaxa 2007, 1668, 591–638, doi:10.11646/zootaxa.1668.1.28.
  65. World Health Organization. World Malaria Report at Glance. 2018. Available online: https://www.who.int/
    malaria/media/world-malaria-report-2018/en/ (accessed on 25 March 2019).
  66. Afrane, Y.A.; Bonizzoni, M.; Yan, G. Secondary Malaria Vectors of Sub-Saharan Africa: Threat to Malaria Elimination on the Continent. IntechOpen 2016, 20, 473–490, doi:10.5772/65359.
  67. Mouchet, J.; Carnevale, P.; Coosemans, M.; Julvez, J.; Manguin, S.; Richard-Lenoble, D.; Sircoulon, J. Biodiversity of Malaria Worldwide; John Libbey Eurotext: Montrouge, France, 2001.
  68. Coetzee, M.; Hunt, R.H.; Wilkerson, R.; Della Torre, A.; Coulibaly, M.B.; Besansky, N.J. Anopheles coluzzii and Anopheles amharicus, new members of the Anopheles gambiae Zootaxa 2013, 3619, 246–274, doi:10.11646/zootaxa.3619.3.2.
  69. Kibret, S.; Wilson, G.G.; Tekie, H.; Petros, B. Increased malaria transmission around irrigation schemes in Ethiopia and the potential of canal water management for malaria vector control. J. 2014, 13, 360, doi:10.1186/1475-2875-13-360.
  70. Lobo, N.F.; St Laurent, B.; Sikaala, C.H.; Hamainza, B.; Chanda, J.; Chinula, D.; Krishnankutty, S.M.; Mueller, J.D.; Deason, N.A.; Hoang, Q.T.; et al. Unexpected diversity of Anopheles species in Eastern Zambia: Implications for evaluating vector behavior and interventions using molecular tools. Rep. 2015, 5, 17952,doi:10.1038/srep17952.
  71. Okiro, E.A.; Alegana, V.A.; Noor, A.M.; Snow, R.W. Changing malaria intervention coverage, transmission and hospitalization in Kenya. J. 2010, 9, 285, doi:10.1186/1475-2875-9-285.
  72. Centers for Disease Control. CDC Activities in Kenya. 2018. Available online: https://www.cdc.gov/malaria/
    malaria_worldwide/cdc_activities/kenya.html (accessed on 25 March 2019).
  73. Macharia, P.M.; Giorgi, E.; Noor, A.M.; Waqo, E.; Kiptui4, R.; Okiro, E.A.; Snow, R.W. Spatio-temporal analysis of Plasmodium falciparum prevalence to understand the past and chart the future of malaria control in Kenya. J. 2018, 17, 340, doi:10.1186/s12936-018-2489-9.
  74. Okara, R.M.; Sinka, M.E.; Minakawa, N.; Mbogo, C.M.; Hay, S.I.; Snow, R.W. Distribution of the main malaria vectors in Kenya. J. 2010, 9, 69, doi:10.1186/1475-2875-9-69.
  75. Olanga, E.A.; Okombo, L.; Irungu, L.W.; Mukabana, W.R. Parasites and vectors of malaria on Rusinga Island, Western Kenya. Parasites Vectors 2015, 8, 250, doi:10.1186/s13071-015-0860-z.
  76. Ototo, E.N.; Mbugi, J.P.; Wanjala, C.L.; Zhou, G.; Githeko, A.K.; Yan, G. Surveillance of malaria vector population density and biting behaviour in western Kenya. J. 2015, 14, 244, doi:10.1186/s12936-015-0763-7.
  77. Ochomo, E.; Bayoh, N.M.; Kamau, L.; Atieli, F.; Vulule, J.; Ouma, C.; Ombok, M.; Njagi, K.; Soti, D.; Mathenge, E.; et al. Pyrethroid susceptibility of malaria vectors in four Districts of western Kenya. Parasites Vectors 2014, 7, 310, doi:10.1186/1756-3305-7-310.
  78. Kipyab, P.C.; Khaemba, B.M.; Mwangangi, J.M.; Mbogo, C.M. The physicochemical and environmental factors affecting the distribution of Anopheles merus along the Kenyan coast. Parasites Vectors 2015, 8, 221, doi:10.1186/s13071-015-0819-0.
  79. Mukiama, T.K.; Mwangi, R.W. Seasonal population changes and malaria transmission potential of Anopheles pharoensis and the minor anophelines in Mwea Irrigation Scheme, Kenya. Acta Trop. 1989, 4, 181–189.
  80. Degefa, T.; Yewhalaw, D.; Zhou, G.; Lee, M.; Atieli, H.; Githeko, A.K.; Yan, G. Indoor and outdoor malaria vector surveillance in western Kenya: Implications for better understanding of residual transmission. J. 2017, 16, 443, doi:10.1186/s12936-017-2098-z.
  81. Ministry of Health. The Epidemiology and Control Profile of Malaria in Kenya: Reviewing the Evidence to Guide the future Vector Control. National Malaria Control Programme, Ministry of Health. Technical support provided by the LINK Project Nairobi, Kenya, 2016. Available online: https://virtual.lshtm.ac.uk/
    wp-content/uploads/2016/11/Kenya-Epidemiological-Profile.pdf (accessed on 28 March 2019).
  82. Kweka, E.J.; Munga, S.; Himeidan, Y.; Githeko, A.K.; Yan, G. Assessment of mosquito larval productivity among different land use types for targeted malaria vector control in the western Kenya highlands. Parasites Vectors 2015, 8, 356, doi:10.1186/s13071-015-0968-1.
  83. President’s Malaria Initiative. Kenya Malaria Operational Plan FY 2019. 2019. Available online: https://www.pmi.gov/docs/default-source/default-document-library/malaria-operational-plans/fy19/fy-2019-kenya-malaria-operational-plan.pdf?sfvrsn=3 (accessed on 1 March 2019).
  84. Owino, E.A. Kenya needs cohesive policies and better strategies in its war against malaria in arid and semi arid areas. J. Mosq. Res. 2018, 5, 124–126.
  85. Bowman, D.D.; Liu, Y.; McMahan, C.S.; Nordone, S.K.; Yabsley, M.J.; Lund, R.B. Forecasting United States heartworm Dirofilaria immitis prevalence in dogs. Parasites Vectors 2016, 9, 540, doi:10.1186/s13071-016-1804-y.
  86. Labarthe, N.; Guerrero, J. Epidemiology of heartworm: What is happening in South America and Mexico? Parasitol. 2005, 133, 149–156, doi:10.1016/j.vetpar.2005.04.006.
  87. Corbet, P.S.; Williams, M.C.; Gillett, J.D. O’nyong nyong fever: An epidemic virus disease in East Africa. IV. Vector studies at epidemic sites. R. Soc. Trop. Med. Hyg. 1961, 55, 463–480.
  88. LaBeaud, A.D.; Banda, T.; Brichard, J.; Muchiri, E.M.; Mungai, P.L.; Mutuku, F.M.; Borland, E.; Gildengorin, G.; Pfeil, S.; Teng, C.Y.; et al. High Rates of O’Nyong Nyong and Chikungunya Virus Transmission in Coastal Kenya. PLoS Negl. Trop. Dis. 2015, 9, e0003436, doi:10.1371/journal.pntd.0003436.
  89. Njenga, S.M.; Mwandawiro, C.S.; Wamae, C.N.; Mukoko, D.A.; Omar, A.A.; Shimada, M.; Bockarie, M.J.; Molyneux, D.H. Sustained reduction in prevalence of lymphatic filariasis infection in spite of missed rounds of mass drug administration in an area under mosquito nets for malaria control. Parasites Vectors 2011, 4, 90, doi:10.1186/1756-3305-4-90.
  90. Njenga, S.M.; Kanyi, H.M.; Mutungi, F.M.; Okoyo, C.; Matendechero, H.S.; Pullan, R.L.; Halliday, K.E.; Brooker, S.J.; Wamae, C.N.; Onsongo, J.K.; et al. Assessment of lymphatic filariasis prior to re-starting mass drug administration campaigns in coastal Kenya. Parasites Vectors 2017, 10, 99, doi:10.1186/s13071-017-2044-5.
  91. Mwandawiro, C.S.; Fujimaki, Y.; Mitsui, Y.; Katsivo, M. Mosquito vectors of bancroftian filariasis in Kwale District, Kenya. East Afr. Med. J. 1997, 74, 288–293.
  92. Moraga, P.; Cano, J.; Baggaley, R.F.; Gyapong, J.O.; Njenga, S.M.; Nikolay, B.; Davies, E.; Rebollo, M.P.; Pullan, R.L.; Bockarie, M.J.; et al. Modelling the distribution and transmission intensity of lymphatic filariasis in sub-Saharan Africa prior to scaling up interventions: Integrated use of geostatistical and mathematical modelling. Parasites Vectors 2015, 8, 560, doi:10.1186/s13071-015-1166-x.
  93. Ogola, E.O.; Fillinger, U.; Ondiba, I.M.; Villinger, J.; Masiga, D.K.; Torto, B.; Tchouassi, D.P. Insights into malaria transmission among Anopheles funestus mosquitoes, Kenya. Parasites Vectors 2018, 11, 577, doi:10.1186/s13071-018-3171-3.
  94. Ogola, E.O.; Fillinger, U.; Isabella, M.V.; Jandouwe, M.; Daniel, K.; Torto, B.; Tchouassi, D.P. Malaria in Kakuma refugee camp, Turkana, Kenya: Facilitation of Anopheles arabiensis vector populations by installed water distribution and catchment systems. J. 2011, 10, 149, doi:10.1186/s13071-018-3171-3.
  95. Njenga, S.M.; Muita, M.; Kirigi, G.; Mbugua, J.; Mitsui, Y.; Fujimaki, Y.; Aoki, Y. Bancroftian filariasis in Kwale District, Kenya. East Afr. Med. J. 2000, 77, 245–249.
  96. Ciota, A.T.; Kramer, L.D. Vector-virus interactions and transmission dynamics of West Nile virus. Viruses 2013, 5, 3021–3047, doi:10.3390/v5123021.
  97. Burkett-Cadena, N.D.; Bingham, A.M.; Porterfield, C.; Unnasch, T.R. Innate preference or opportunism: Mosquitoes feeding on birds of prey at the Southeastern Raptor Center. Vector Ecol. 2014, 39, 21–31, doi:10.1111/j.1948-7134.2014.12066.x.
  98. Zittra, C.; Flechl, E.; Kothmayer, M.; Vitecek, S.; Rossiter, H.; Zechmeister, T.; Fuehrer, H.P. Ecological characterization and molecular differentiation of Culex pipiens complex taxa and Culex torrentium in eastern Austria. Parasites Vectors 2016, 9, 197, doi:10.1186/s13071-016-1495-4.
  99. Beji, M.; Rhim, A.; Roiz, D.; Bouattour, A. Ecophysiological characterization and molecular differentiation of Culex pipiens forms (Diptera: Culicidae) in Tunisia. Parasites Vectors 10, 3021-3047, doi:10.3390/v5123021.
  100. Scott, J.G.; Yoshimizu, M.H.; Kasai, S. Pyrethroid resistance in Culex pipiens Pestic. Biochem. Physiol. 2015, 120, 68–76, doi:10.1016/j.pestbp.2014.12.018.
  101. Centers for Disease Control. Vectors of Lymphatic Filariasis. 2018. Available online: https://www.cdc.gov/
    parasites/lymphaticfilariasis/gen_info/vectors.html (accessed on 13 March 2019).
  102. World Health Oganisation. Lymphatic Filariasis. 2018. Available online: https://www.who.int/news-room/fact-sheets/detail/lymphatic-filariasis (accessed on 26 March 2019).
  103. Turell, M.J. Members of the Culex pipiens Complex as Vectors of Viruses. Am. Mosq. Control Assoc. 2012, 28, 123–126, doi:10.2987/8756-971X-28.4.123.
  104. Rappole, J.H.; Hubalek, Z. Migratory birds and West Nile virus. Appl. Microbiol. 2003, 94, 47–58.
  105. Chancey, C.; Grinev, A.; Volkova, E.; Rios, M. The global ecology and epidemiology of west nile virus. Res. Int. 2015, 2015, 376230, doi:10.1155/2015/376230.
  106. Kopp, A.; Gillespie, T.R.; Hobelsberger, D.; Estrada, A.; Harper, J.M.; Miller, R.A.; Eckerle, I.; Müller, M.A.; Podsiadlowski, L.; Leendertz, F.H.; et al. Provenance and geographic spread of St. Louis encephalitis virus. MBio 2013, 4, e00322-13, doi:10.1128/mBio.00322-13.
  107. Deardorff, E.R.; Weaver, S.C. Vector competence of Culex (Melanoconion) taeniopus for equine-virulent subtype IE strains of Venezuelan equine encephalitis virus. J. Trop. Med. Hyg. 2010, 82, 1047–1052, doi:10.4269/ajtmh.2010.09-0556.
  108. Samy, A.M.; Elaagip, A.H.; Kenawy, M.A.; Ayres, C.F.J.; Peterson, A.T.; Soliman, D.E. Climate change influences on the global potential distribution of the mosquito Culex quinquefasciatus, vector of West Nile virus and lymphatic filariasis. PLoS ONE 2016, 11, e0163863, doi:10.1371/journal.pone.0163863.
  109. Amraoui, F.; Atyame-Nten, C.; Vega-Rúa, A.; Lourenço-De-Oliveira, R.; Vazeille, M.; Failloux, A.B. Culex mosquitoes are experimentally unable to transmit zika virus. Surveill. 2016, 21, 35, doi:10.2807/1560-7917.ES.2016.21.35.30333.
  110. Huang, Y.S.; Ayers, V.B.; Lyons, A.C.; Unlu, I.; Alto, B.W.; Cohnstaedt, L.W.; Higgs, S.; Vanlandingham, D.L. Culex Species Mosquitoes and Zika Virus. Vector-Borne Zoonotic Dis. 2016, 16, 673–676, doi:10.1089/vbz.2016.2058.
  111. Phumee, A.; Chompoosri, J.; Intayot, P.; Boonserm, R.; Boonyasuppayakorn, S.; Buathong, R.; Thavara, U.; Tawatsin, A.; Joyjinda, Y.; Wacharapluesadee, S.; et al. Vertical transmission of Zika virus in Culex quinquefasciatus Say and Aedes aegypti () mosquitoes. Sci. Rep. 2019, 9, 5257, doi:10.1038/s41598-019-41727-8.
  112. Grossi-Soyster, E.N.; Banda, T.; Teng, C.Y.; Muchiri, E.M.; Mungai, P.L.; Mutuku, F.M.; Gildengorin, G.; Kitron, U.; King, C.H.; Desiree, L.A. Rift valley fever seroprevalence in Coastal Kenya. J. Trop. Med. Hyg. 2017, 97, 115–120, doi:10.4269/ajtmh.17-0104.
  113. Harbach, R. Genus Mansonia Blanchard, 1901. Mosquito Taxonomic Inventory. 2008. Available online: http://mosquito-taxonomic-inventory.info/genus-emmansoniaem-blanchard-1901 (accessed on 1 March 2019).
  114. Islam, M.N.; ZulKifle, M.A.; Sherwani, M.K.; Ghosh, S.K.; Tiwari, S. Prevalence of malaria, dengue and chikungunya significantly associated with mosquito breeding sites. Islam. Med. Assoc. North Am. 2011, 43, 58–67, doi:10.5915/43-2-7871.
  115. Torres, R.; Samudio, R.; Carrera, J.P.; Young, J.; Maârquez, R.; Hurtado, L.; Weaver, S.; Chaves, L.F.; Tesh, R.; Caâceres, L. Enzootic mosquito vector species at equine encephalitis transmission foci in the República de Panama. PLoS ONE 2017, 12, e0185491, doi:10.1371/journal.pone.0185491.
  116. Beranek, M.D.; Gallardo, R.; Almirón, W.R.; Contigiani, M.S. First detection of Mansonia titillans (Diptera: Culicidae) infected with St. Louis encephalitis virus (Flaviviridae: Flavivirus) and Bunyamwera serogroup (Peribunyaviridae: Orthobunyavirus) in Argentina. Vector Ecol. 2018, 43, 340–343, doi:10.1111/jvec.12320.
  117. Rueanghiran, C.; Lertwatcharasarakul, P.; Ruangsittichai, J. Species-specific primers for the detection of lymphatic filariasis vectors: Mansonia bonneae and Mansonia dives. Biomed. 2017, 34, 615–621.
  118. Ughasi, J.; Bekard, H.E.; Coulibaly, M.; Adabie-Gomez, D.; Gyapong, J.; Appawu, M.; Wilson, M.D.; David, B.; Daniel, A. Mansonia africana and Mansonia uniformis are Vectors in the transmission of Wuchereria bancrofti lymphatic filariasis in Ghana. Parasites Vectors 2012, 5, 89, doi:10.1186/1756-3305-5-89.
  119. Onapa, A.W.; Pedersen, E.M.; Reimert, C.M.; Simonsen, P.E. A role for Mansonia uniformis mosquitoes in the transmission of lymphatic filariasis in Uganda? Acta Trop. 2007, 101, 159–168, doi:10.1016/j.actatropica.2007.01.003.
  120. Epelboin, Y.; Talaga, S.; Epelboin, L.; Dusfour, I. Zika virus: An updated review of competent or naturally infected mosquitoes. PLoS Negl. Trop. Dis. 2017, 11, e0005933, doi:10.1371/journal.pntd.0005933.
  121. Kinyatta, N.M. Vectorial Potential of Mansonia Species in the Transmission of Wuchereria Bancrofti and Evaluation of Mosquito Collection Methods in Tana-Delta, Coastal Kenya. Master’s Thesis, Kenyatta University of Agriculture and Technology, Nairobi, Kenya, 2010.
 

Cite this article

Xiaomin, Hu. Mosquitoes of Etiological Concern in Kenya, Encyclopedia, 2019, v1, Available online: https://encyclopedia.pub/215