Prevalence and Seasonal Distribution of Dengue Mosquito, Aedes aegypti (Diptera: Culicidae) in Al-Madinah Al-Munawwarah, Saudi Arabia

MATERIALS AND METHODS

Study Area
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°46‘N, 39°61‘E and 631 m above sea level. It is a semi-cultivated desert area.

Mosquito Collection
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 Hoyer’s medium for taxonomic identification. Females Aedes mosquitoes were examined for feeding (the presence or absence of blood in each female’s 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 Hoyer’s medium and taxonomically identified using several keys (Edwards, 1941; Mattingly and Knight, 1956; Hopkins, 1952; Jupp, 1996; Rueda, 2004).

Statistical Analysis
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).

RESULTS

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).

Table 1:	Aedes aegypti population collected in Al-Madinah Al-Munawwarah from July 2008 to June 2009

Fig. 1:	Seasonal variation of Ae. aegypti population collected in Al-Madinah Al-Munawwarah from July 2008 to June 2009

Fig. 2:	Indoor and outdoor Ae. aegypti collected in Al-Madinah Al-Munawwarah from July 2008 to June 2009

Table 2:	Results of Ae. aegypti female mosquitos' examination for feeding status and parity, collected in Al-Madinah Al-Munawwarah from July 2008 to June 2009

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).

DISCUSSION

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 Al-Munawwarah.

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 man’s 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, 1993).

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 and Makkah.

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.

ACKNOWLEDGMENT

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.