Impact of Irrigation System on Malaria Transmission in Jazan Region, Saudi Arabia

Introduction: Jazan Region, in the Southwestern Saudi Arabia is known as the mostly affected region with malaria. Malaria occurs at hypo-to hyperendimic level where P. falciparum is the commonest parasite and An. arabiensis is the principal vector. Different types of crop irrigation systems were often blamed for aggravating the health risks of local communities. Reservoirs, irrigation canals, and dams are closely associated with vector-borne parasitic diseases. Thus, seasonal transmission period of a disease such as malaria may be extended as a result of these irrigation systems. The present study is meant to investigate vector breeding and transmission sites associated with the irrigation system in Jazan area for malaria through vector sampling and direct observation. Methods: The study was conducted in three villages in irrigated and three villages in non-irrigated areas in Jazan Region. Entomological surveys were conducted over 12 months from January to December 2004. Larvae were sampled by standard dipping technique and adults were sampled by pyrethrum knockdown collection and CDC light traps. Anopheline mosquitoes were morphologically identifi ed and further verifi ed at the Natural History Museum, London, UK. Mosquito blood meals were tested by direct enzyme linked immune sorbent assay technique for source identifi cation. Results: Of the 3498 anophelines larvae collected, during this study, 53.2% were from the irrigated sites. The total collection of larvae revealed the prevalence of 7 Anopheles spp., of these An. d`thali and An. pretoriensis were the most abundant, and comprised about 50.77 % and 36.91%, of the total collection, respectively. Larvae of the known malaria vector, An. arabiensis comprised 9.43% (330), of which, 69.4% were harvested from habitats at the irrigated area. A total of 2938 adult anophelines were caught from both areas and 1539 (52.4%) were An. d`thali, An. multicolor and An. arabiensis from irrigated area. A total of 106 blood-meal specimens from An. d`thali and An. arabiensis females, were examined and 95.3% were of human origin. Discussion and Conclusion: Of the seven anopheline species encountered, An. sergentii, An. multicolor and An. fl uviatilis are fi rst record in Jazan Region. The study showed no signifi cant difference between irrigated and non-irrigated areas can provide mosquitoes with various breeding habitat types. The known malaria vector in the region, An. arabiensis were more abundant in irrigated areas as larvae (69.3%) and as adults (69.4%) and together with An. d`thali showed high tendency towards anthropophagic behaviour (95.33%). Research Article Impact of Irrigation System on Malaria Transmission in Jazan Region, Saudi Arabia Mohammed Hassan Alzahrani1, Philip McCall2, Amir Hassan2, Abdiasiis Ismael Omar1* and Abdelmohsin Mohammed Abdoon1 1Disease Vectors Departments, Public Health Directorate, Ministry of Health, Kingdom of Saudi Arabia 2Liverpool School of Tropical Medicine, Liverpool, United Kingdom Dates: Received: 21 March, 2017; Accepted: 27 May, 2017; Published: 29 May, 2017 *Corresponding author: Abdiasiis Ismael Omar, Disease Vectors Departments, Public Health Directorate, Ministry of Health, Kingdom of Saudi Arabia, Tel: 00966560359993; E-mail:


Introduction
Environmental changes and ecological disturbances, due to both natural phenomena and human intervention, have exerted and continue to exert a marked infl uence on the emergence and proliferation of parasitic diseases [1,2]. Many diseases are associated with water either directly, such as the diarrhoeal diseases transmitted by ingestion of infected water, or indirectly, where a disease's intermediate hosts or vectors depend on water for their development. In the latter case, the abundance and the consequent prevalence of the disease are often inadvertently increased when water resources are developed. Health Impact Assessment (HIA) is an approach that aims to identify, predict, safeguard and mitigate the impact of development projects on health; the assessment procedure involves identifi cation of health hazards, interpretation of the health hazards as health risks attributable to the project and fi nally health risk management [3][4][5][6], conducted studies for predicting when vector-borne diseases might increase following water resource development and [7], Investigated changes in parasitic diseases in the same situations [8].
Mentioned that several case studies showed that dams may Following the extensive malaria control program in Saudi Arabia, malaria is now restricted to the southwestern part of the country (Tihama lowlands). About 5% of the national population of Saudi Arabia are at risk (1.04 million). Jazan region is in the SW of Saudi Arabia and bordering Yemen (the most malarious country in the region) accounting on average for 60-70% of all locally acquired malaria cases recorded during the period from 1983 to 2001 [11]. In wadis (valleys) and villages at the foothills of Sarawat Mountains in Jazan region where P. falciparum is common (over 90% of cases) and where rainfall is relatively abundant, malaria occurs as meso-to hyperendemic level [12,13].

Jazan region is divided into four zones with regard to malaria endemicity
Malaria free zone: malaria is absent in mountain areas at 1500 meter above sea level, e. g. Feifa and Al Hasa areas. It is also absent in the Farasan Islands.
Low endemicity zone: transmission in this zone is unstable and the area is subject to malaria epidemics. Periodic rains in the hills can lead to fl ooding in the wadis. This can leave water pockets suitable for breeding of mosquitoes on the coastal plain. In the past the spleen rate in this zone was found to be less than 10% [14,15].

Moderate endemicity zone: Malaria incidence in this zone
is also unstable. Most the inhabitants in this zone are exposed to malaria transmission during periods of up to six months every year, depending on the pattern and amount of rain. This zone includes the interior plains and foothills. This is also where most of the population of Jazan reside, especially along the wadis. The spleen rate in this zone was 10-50% [14,15].
High endemicity zone: Malaria in the Yemeni border areas is stable. Malaria cases reported from this zone constitute more than 50%of all cases reported in Jazan. Water suitable for mosquito breeding is available throughout the whole year. This persists in most areas despite repeated control measures. The malaria transmission season in Jazan extends from October to April with a prominent peak in January. The major factor that infl uences the extent and intensity of transmission season is rain [15].
The present study aims to investigate vector breeding and transmission sites associated with the irrigation system in Jazan region for malaria through vector sampling and direct observation. Most of these villages of 50-500 people are scattered in remote areas, without ease of access. Jazan is one of the Kingdom's richest agricultural regions. Topographically, it is divided into three zones: the mountains in the east (2,500 meters above sea level), the foothills (400-600 meters above sea level) and the extensive plains (less than 400 meters) occupying the area between the foothills and the Red Sea [15]. The region is drained by several permanent wadis, which play a crucial role in providing perennial habitats for mosquitoes and several intermittent wadis, which are wet except in the dry season and which are important in increasing the surface water providing many favourable breeding habitats and directly infl uence abundance of anopheline vectors. These wadis maintain a continuous steady fl ow into the foothill area [15,16]. During the period of heavy rains, the wadis may fl ood and water is carried along the entire wadis to the Red Sea. Thus water fl ow in these wadis is not stable and is subjected to various fl uctuations depending on the amount of rainfall in the mountains. Water run off these wadis ranges from steady fl ow, excessive fl ow or sweeping fl ood. Under these situations the breeding places are not constant or stable and continuously depend on the water fl ow in the wadi. Twenty major wadis that drain rainwater from the mountains into the Red Sea traverse Jazan and have hundreds of tributaries in the foothill areas [15].

Study area
The area for study is divided into two; irrigated and nonirrigated sites as follows:  all water bodies were examined for mosquitoes. All potential mosquito breeding places were visited and checked for the presence of water on each visit and those with water were examined for mosquitoes. Standard dippers of 350 ml volume were used to collect larvae. Collections were made following the protocols described by [17,18]. Hence, pools of one square meter or less in size were dipped fi ve times while pools of larger size were sampled with more than 5 and number of dips were recorded for each sample to calculate the larval density. Blood meal analysis: A Direct Enzyme Linked Immuno-Sorbent Assay (ELISA) [21], was used to identify the source of blood meals of mosquitoes collected by PKD. Each sample was tested for reactions to anti-sera for human, cattle, goat,   (Table 4). * These species have been recorded in Saudi Arabia before [19], but this is the fi rst record in Jazan Region.  A total of 2938 anopheline adults were collected during the study period (Table 5). In adult collections, 53% were An. d`thali
arabiensis. Of all anopheline mosquitoes collected in this study, two species, An. arabiensis and An. d`thali are known vectors of malaria elsewhere. An. fl uviatalis was collected as adult but not as larvae. This was the fi rst record of this species in Jazan Region.
In all study villages the larval density of Anopheles spp.
was closely associated with rainfall pattern. Peaks of rainfall amount was mostly followed by increased larval density (Figures 1-3). An. d`thali was found in all study villages and was observed to occur between June and February, with the highest peak in September. This period coincides with peaks of rainfall recorded (Figure 1) Blood-meal analysis; A total of 106 anopheline (An. d`thali and An. arabiensis) blood meal specimens were stored from PKD collections from both irrigated (78) and non-irrigated (28) areas and assayed by ELISA. In both irrigated and nonirrigated sites human was the most common blood meal source in all species (Table 6). In the irrigated site, more than 90% of the blood meal specimens of An. d`thali were of human origin, while only 64% of An. arabiensis fed on human. In nonirrigated site both species relied entirely on human as a source of blood (94% -100% human feeding rate). The human blood feeding rates were approximately the same for anopheline species 82% (n-64) in irrigated site with 96.4 % (n-27) in non-irrigated site.

Discussion
This study was conducted following the extensive use of pesticides during the 2000 epidemic of RVF in Saudi Arabia that consequently led to rapid decline in malaria cases reports the following years as was noticed during this study. The entomological surveys of the present study indicated that Anopheles spp., including vectors of malaria, breed readily in both irrigated and non-irrigated sites, and the signifi cance t test shows that there is no signifi cant difference between irrigated and non-irrigated sites. However, irrigated sites were found to provide more water surface area, and hence many more suitable breeding places. Most of the anopheline larvae were obtained from the irrigated site, but the difference is not signifi cant compared to those from non-irrigated site. In the middle reaches of Wadis at irrigated and non-irrigated sites, 389 anopheline larvae were collected from Rawan Alabeed (upper Jazan dam in the irrigated area) compared to the few collected from Alkarboos in the non-irrigated site (Table 3).
This can most likely be attributed to the number of breeding sites available at each site: at Rawan Alabeed there was Jazan Dam Lake and Jazan Wadi providing perennial sources for    breeding but at Alkarboos, the non-irrigated site, there was only one perennial wadi (Khulab Wadi) which remained dry until the seasonal rains. Seasonal rain usually increases the numbers of mosquito breeding places, while higher relative humidity and growth of vegetation cover provided a cool shaded environment for the development of aquatic stages and aided the survival of young adults [22][23][24]. Most of the sources of breeding places in the area of study were wadis, although, they were dry during much of study period due to the low rainfall.
The total amount of rainfall recorded in the study period (Jan.  (Figure 3c). This was most likely because the dam lake and the irrigation project created additional suitable breeding places for this species. A study in Jazan Region to determine the vectors of RVF found that more breeding sites were found in the Jazan dam area providing good mosquito larval habitats (Jupp et al., 2002).
In addition to the widespread use of insecticides, the shortage in rain during the study period (as compared with previous four years) was one of the limitations of adult vector density in both irrigated and non-irrigated sites. Clearly, the amount of rain in both sites and the creation of additional breeding places by irrigation in irrigated site can infl uence the quantity and quality of breeding sites available for breeding of An. arabiensis. In the dry savanna of Africa, vector species can have seasonal fl uctuations in abundance, declining to low levels in dry seasons [25][26][27][28]. ELISA test conducted in the present study showed that An. d`thali and An. arabiensis rely  predominantly on human blood. The other blood meals were taken from cattle, mainly by An. arabiensis in the irrigated site.
The domestic animals found in both areas were mainly goats, sheep, cattle, camel and donkey. Although cows were available in both areas, there were more cows in irrigated site (estimated at 250 compared to 30 cows or less in the non-irrigated site).
The presence of domestic animals has been associated with a decrease in malaria transmission rates due to zoophilic deviation [29]. In some parts of Africa, zooprophylaxis is used and cattle are intentionally kept near or inside houses to divert mosquitoes from humans to cattle [30]. It was suggested that cattle could play a role in reducing transmission of malaria by An. arabiensis by distracting the prints create more breeding sites. In East Africa, An. arabiensis shows a preference for feeding on cattle, sheep, goats and donkeys [31,32]. All these hosts were common in our study in the irrigated area. In Kenya An. arabiensis has been reported to move into houses after feeding outside on cattle [1,33,34]. Also showed that a high proportion of An. arabiensis resting inside human habitations in northern Tanzania had fed on cattle. For control measures, preventing mosquito feeding on animals by application of insecticide on domestic animals might also be useful [35,36].