Prevalence and Seasonal Distribution of Dengue Mosquito, Aedes aegypti (Diptera: Culicidae) in Al-Madinah Al-Munawwarah, Saudi Arabia
Aedes aegypti (Ae. aegypti) is a cosmo-tropical, urban, peri-domestic mosquito, was established as the primary indigenous vector of recent urban dengue virus outbreaks in Jeddah and Makkah, Saudi Arabia. Dengue virus activity has never been reported in Al-Madinah. An entomological survey was carried out to document prevalence and seasonal distribution of Aedes mosquitoes for the first time in Al-Madinah Al-Munawwarah, Western Saudi Arabia. Adult Aedes were collected for a year from July 2008 to June 2009, using standardized sampling with overnight; Black Hole UV trap produces CO2 and morning; knockdown Spray-sheet method. Ae. aegypti was the only identified Aedes mosquito species in all surveyed residential areas in Al-Madinah. A total of 463 Ae. aegypti adult mosquitoes were identified; 300 (64.8%) females and 163 (35.2%) males. It was abundant year round with varying density among months; it peaked at April. Density of Ae. aegypti intra-domiciliary was higher than extra-domiciliary stations and inflated by a greater proportion of female mosquitoes. Non-fed females were significantly out numbered blood-fed females. These results necessitate further epidemiological surveillance and implicate regular strict monitoring of Ae. aegypti in Al-Madinah Al-Munawwarah, to overrule the possibility of Ae. aegypti establishment in Al-Madinah.
Aedes aegypti (Linnaeus. Diptera: Culicidae) is of considerable public
health importance in the tropics and subtropics. Ae. aegypti mosquitoes
are the most important and the primary domestic vector of urban dengue and yellow
fever viruses (Gubler, 1988, 1998).
It can transmit Chikungunya (Sam and Baker, 2006), Murrary
Valley encephalitis and Ross River (Lee et al., 1987)
viruses in addition to Chandipura virus (Rhabdoviridae) experimentally
(Mavale et al., 2005). Aedes aegypti can
also transmit filarial infections of Wuchereria bancrofti and Dirofilaria
immitis (Russell et al., 2005), avian parasite
Plasmodium gallinaceum (Alavi et al., 2003).
It can mechanically transmit Lumpy Skin Disease Virus (LSDV) from infected to
susceptible cattle (Chihota et al., 2001).
It is a cosmo-tropical, domestic mosquito, considered to be an urban mosquito
exists inside and near human habitation and favor densely populated areas, but
it also breeds in rural areas. Females are day biters have also been taken in
lesser numbers at night (Christophers, 1960; Clements,
1999). They enter buildings to feed and prefer to lay their eggs in artificial
water containers such as flower pots, vases, gutters, roof guttering, tires,
bottles, tins, cans, pot plant saucers, plastic bags, water storage drums, subterranean
waters and refuse filled with rain (Christophers, 1960;
Lee et al., 1987; Gubler, 2002).
However, Ae. aegypti is able to utilize natural available breeding sites
as tree holes and leaf axils of bromeliads (Lee et al.,
1987). Aedes aegypti preferred breeding sites and its means of transmission
studied in many areas, in USA and Puerto Rico discarded automotive tires were
found to be an ideal sites (Tinker, 1964; Moore
et al., 1978; Chambers et al., 1986)
and large drums were their preferred sites in Colombia (Nelson
et al., 1984) overhead tanks and cement tanks in addition to tires
in India (Sharma et al., 2005).
Aedes introduction to new focus in a geographical area occurs via transportation
of dormant viable eggs through transported and stored used tires and/or transfer
of adult in different transportation vehicles (Reiter, 1993).
Aedes mosquito was involved in many recorded epidemics in Saudi Arabia
of arboviruses (Godsey et al., 2003; Rathor,
1996), Rift Valley Fever (Jupp et al., 2002;
Miller et al., 2002; Moutailler
et al., 2008) and Dengue (Ghaznawi et al.,
1997; Fakeeh and Zaki, 2001).
Aedes aegypti was established as the primary indigenous vector of recent urban dengue virus outbreaks in Jeddah and Makkah, Saudi Arabia, nearby cities to Al-Madinah Al-Munawwarah. Dengue virus activity has never been reported in Al-Madinah. We succeeded to report. Aedes aegypti through an entomological survey for 2 months (May-June 2008) in Al-Madinah which was an impetus to conduct an entomological survey for a year from July 2008 to detect Aedes prevalence and fully document their seasonal variations and populations diversity in Al-Madinah geographical region of the kingdom which is of importance to implement and designing effective vector control strategies.
MATERIALS AND METHODS
An entomologic survey were carried out in the Al-Madinah Al-Munawwarah central
region and surrounding province in housing areas as Aedes is known as
a domestic mosquito. Al-Madinah Al-Munawwarah is located approximately 420 km
North of Jeddah and Makkah. It is situated at 24°46N, 39°61E
and 631 m above sea level. It is a semi-cultivated desert area.
Adult mosquitoes were collected twice weekly to include basement of 10 building
under constructions surrounded by inhabited buildings and 10 inhabited buildings
in and surrounding central area, also 10 housed farms around the central area
of Al-Madinah Al-Munawwarah where 46 areas were surveyed once monthly. They
were collected for a year, from July 2008-June 2009, using Black Hole UV trap
produces CO2 indoor and in yards and gardens close to the human dwellings
and farms overnight and knockdown spray-sheet procedure indoors at morning (Service,
1993). After collection, the captured insects were kept in a humid and cool
environment and rapidly transported to the laboratory. In laboratory they were
observed with a dissecting microscope to separate the Aedes from other
insects and sorted by sex. Male Aedes were stored in 1.5 mL vials containing
95% ethanol, latter were mounted in Hoyers medium for taxonomic identification.
Females Aedes mosquitoes were examined for feeding (the presence or absence
of blood in each females midgut) and the status of any blood (digested
or not). Also, they were examined for parity (as being gravid or not) by analyzing
their ovarian development according to Christophers (1960).
Then examined female were pooled according to date and site of collection and
stored at -80°C.
Aedes Mosquitoes Identification
Aedes mosquitoes were mounted in Hoyers medium and taxonomically
identified using several keys (Edwards, 1941; Mattingly
and Knight, 1956; Hopkins, 1952; Jupp,
1996; Rueda, 2004).
All the results were tabulated and presented by figures and histograms;
descriptive statistics were performed using Statistical Package for the Social
Sciences (SPSS for Windows Version 13, 2005).
A total of 463 Aedes mosquitoes were identified, all of them were Ae. aegypti; 300 (64.8%) females and 163 (35.2%) males (Table 1). The mosquitoes were collected from inside homes and farms and in the area surrounding them. The distribution and seasonal variation of collected Ae. aegypti mosquitoes showed in Table 1 and Fig. 1.
Domiciliary distribution of Ae. aegypti collected in Al-Madinah Al-Munawwarah
from July 2008 to June 2009 was represented in Table 1 and
Fig. 2. Most of caught females were intradomicilary 217/300
(72.33%), 134 from inside buildings and 74 from inside farms while males were
dominant extardomicilary 99/163 (60.74%), 26 and 73 from outside of buildings
and farms, respectively (Table 1, Fig. 2).
Aedes aegypti population collected in Al-Madinah
Al-Munawwarah from July 2008 to June 2009
variation of Ae. aegypti population collected in Al-Madinah Al-Munawwarah
from July 2008 to June 2009
and outdoor Ae. aegypti collected in Al-Madinah Al-Munawwarah from
July 2008 to June 2009
of Ae. aegypti female mosquitos' examination for feeding status
and parity, collected in Al-Madinah Al-Munawwarah from July 2008 to June
Females were examined for feeding status and parity and their results were
presented in Table 2. Most of examined females were not blood
fed (63%), 70.9% of them were non-parous (Table 2).
Aedes aegypti was the primary established indigenous domestic vector
of recent outbreaks of urban dengue in Saudi Arabia (Ghaznawi
et al., 1997). To our knowledge, it was detected for the first time
in Al-Madinah Al-Munawwarah, Western of Saudi Arabia by the authors at the beginning
of 2008. Al-Madinah showed recent human-environmental changes in addition to
continuity of dengue sporadic cases in nearby cities, Jeddah and Makkah (Fakeeh
and Zaki, 2001, 2003; Ayyub
et al., 2006; Khan et al., 2008) led
us to conduct an entomological survey during which adult Aedes mosquitoes
were collected from areas in Almadinah Al-Munawwarah region, throughout a period
of a year from July 2008 to June 2009. Determination of adult mosquitoes population
size of value to direct and guide control measures. The entemological survey
is an important tool to get entemological data required for proper and effective
designing of control programs and to create an early warning system. The mosquitoes
were classified by sex, parity and feeding (for females). This study reports
for the first time the prevalence and seasonality of Aedes in Al-Madinah
Ae. aegypti was the only identified Aedes mosquito species. It
was detected year round with minimal seasonality; it peaked at April. Seasonal
variation in population density and distribution is common for Ae. aegypti
since, it is sensitive to changes in temperature and available moisture,
it decrease in density in dry and cool seasons and they increase when temperatures
increase and the wet season begins (Schultz, 1993).
Human-environmental changes are responsible for establishment and proliferation of Ae. aegypti population, this facilitates Ae. aegypti contact with humans. Al-Madinah showed recent human-environmental changes with growing in construction projects with the presence of many buildings under constrictions, rapid urbanization, the presence of farms around Al-Madinah and different life style with wide use of air conditioners and evaporative coolers, which provide manmade breeding sites suitable for establishment and proliferation of Aedes mosquitoes. Also, the presence of few old buildings with two- to three-floor flats, housing four to six families which provide dark, cool, humid microclimatic sites ideal for Aedes. The growing urban population (both local and migration) and the increasing population mobility with rapid and development of transportation in Al-Madinah also are added risk factors that may contribute to further geographic expansion and density of Ae. aegypti.
The existence of this species throughout the year in Al-Madinah Al-Munawwarah
is probably due to the arid climate and manmade breeding sites as the subterranean
sites in building under-construction, watering practices and subsequent behavior
by local residents, in addition farms in Al-Madinah Al-Munawwarah have to be
watered more frequently to maintain vegetation, but this practice may serve
to create and support sustained, suitable breeding sites for Aedes. These
available Aedes breeding sites apparently not affected by rains and sustain
year round existence of Aedes in Al-Madinah. Similar distribution was
also reported by Russell et al. (1996) in sesmi-arid
area of Australia. Ae. aegypti habitats vary almost as greatly as mans
habitats, for their primary requirement is the presence of man. From the results
of this comprehensive collection, in Al-Madinah Ae aegypti was anthrophilic
and endophilic. It was evident that the mosquitoes were more abundant indoor
followed by sheltered housing area (Table 1). Aedes aegypti
was identified in all surveyed residential areas in Al-Madinah, its urban;
peri-domestic and anthropophilic nature has also been shown in many studies
(MacDonald, 1956; Surtees, 1969;
Harrison et al., 1972; Trpis
and Hausermann, 1978; Jupp, 1996; Schultz,
It was also noted that the number of total positive buildings was more in February-May
2009 and peaked at April to decline in August-September 2008. Although, climatic
conditions and water availability may be the reason for this difference as Al-Madinah
showed flooding event by rainfall days preceding Aedes surge in February-April,
as Aedes eggs enter diapauses state during dry seasons, with lifetime
ranging from weeks to few years until a flooding such as extreme tide or rainfall
occurs which indicates the breeding habitats (Bicout et
al., 2002) this difference also may be due to the nature of Aedes
breeding sites and habitats in Al-Madinah Al-Munawwarah and is more likely to
be related to favorable cooler temperatures of these months. In addition these
months showed and preceeded by the growing intensive traffic between Jeddah
As expected, collected female mosquitoes outnumbered the males in the examined
buildings because females are the blood-feeders of these insects. Anautogenous
female Aedes mosquitoes imbibe vertebrate blood for oogenesis (Clements,
1992) except female Ae. Aegypti, it feed exclusively on human blood
and very rarely on sugar (Harrington et al., 2001).
This explain more abundance of female mosquitoes indoors (Table
1). Regarding mosquito density in the examined sites, it was found that
the highest was in February-May 2009 (Fig. 1). The feeding
and gravidity of the collected female mosquites revealed a difference in the
number of fed and non-fed collected mosquitoes (Table 2) the
non-fed females were much higher in number in some months. This is unlikely
to represent a clue to their feeding habits but is possibly a coincidence having
to do with the fact that there is no way to control the number or ration of
fed vs non-fed mosquitoes falling into the traps used to collect them. Regarding
parity and fecundity, none of the collected females were parous in September
and October 2008. This had also been preceded by a surge in parity in the previous
months and followed by a decline in parity in the next months. This is likely
to shed light on the mating season habits of Aedes mosquitoes in Almadinah
region and can may be implemented to design control strategies.
It is believed that the arrival of adult Aedes mosquitoes to Al-Madinah has been favored by the growing intensive traffic between both Jeddah and Makkah especially there is a major motorway among them. It seems that the main mode of transmission of Aedes by transport of viable, dormant eggs through transported and stored used tires do not apply here but needs to be fully investigated.
In conclusion, the recent human-environmental changes in Al-Madinah Al-Munawwarah provided manmade breeding sites that facilitate Ae. aegypti introduction, maintenance and establishment with possibility of population proliferation. Moreover, rapid transport developments are risk factors augmented by tourism and trade links. The obtained results clearly determined Ae. aegypti distribution and seasonality in Al-Madinah Al-Munawwarah. The obtained few number of Aedes mosquitoes in this study, were due to the successful implementation of control programs by local health authority. These results necessitate further epidemiological surveillance and implicate regular strict monitoring of Ae. aegypti in Al-Madinah Al-Munawwarah, to overrule the possibility of Ae. aegypti establishment in Al-Madinah, with the potential risk of dengue transmission also, they are of importance to local health authority to successfully plan and implement their proper effective control programs.
The study was funded by King Abdul Aziz City for Science and Technology (KACST) as one of the KACST grants program, grant No. AT: 27-34. We are grateful to staff of laboratories and Vector Control Unit, Primary Health Care, Ministry of Health, Al-Madinah Al-Munwarah, KSA. for collaboration in the field work.
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