Background
Malaria, one of the most common life-threatening infectious diseases, is still a major public health problem worldwide, particularly in tropical and sub-tropical regions. According to the World Health Organization (WHO), about 229 million new cases of malaria were reported worldwide in 2019 and over 3.4 billion people are at risk of infection [
1]. Almost 94% of the malaria cases were reported in the WHO African Region (AFR), while 3.0 and 2.2% of the cases were recorded in the WHO Southeast Asia Region (SEAR) and Eastern Mediterranean Region (EMR), respectively [
1]. Moreover, approximately 409,000 malaria deaths occurred worldwide in 2019, with sub-Saharan Africa accounting for about 95% of all global malaria deaths [
1,
2].
Plasmodium falciparum is considered the most virulent and prevalent
Plasmodium species, accounting for 99.7, 69 and 62.8% of the reported malaria cases in the AFR, EMR and SEAR regions, respectively [
3]. Furthermore, it has been estimated that about 14.3 million malaria cases in 2018 were attributable to
Plasmodium vivax and that 3.3 billion people are at risk of vivax malaria infection worldwide [
4].
In Saudi Arabia, the national malaria control programme, which was established in 1948, has achieved a tremendous reduction in the annual number of malaria cases, and malaria is now restricted to the southwestern parts of the country, which includes the Aseer and Jazan regions. The number of autochthonous/indigenous (locally transmitted) malaria cases in Saudi Arabia decreased dramatically between 2000 and 2014, from 511 in 2000 to just 30 in 2014, and the country has been included in the E-2020 WHO initiative, which is focused on achieving a target of zero autochthonous cases by 2020 [
5]. However, malaria cases increased after 2014, with 5,382 malaria cases reported in 2016, including 272 locally transmitted cases (270 falciparum and two vivax malaria) [
6,
7]. In the global context, this number of cases is considered high and the country therefore remains determined to make vigorous efforts to achieve E-2020 status.
Progress toward malaria elimination in Saudi Arabia until 2014 has been investigated by several researchers [
8,
9]. However, there is a scarcity of information about the frequency and distribution of malaria cases in Jazan region after 2014. Therefore, this study aims to fill this gap in knowledge and to elucidate the situation regarding the level of residual malaria endemicity in the region, as well as to investigate associations of autochthonous malaria with selected climatic (meteorological) factors over a period of 8 years (2010–2017). In malaria elimination settings, such information is crucial to identify the challenges and further research needs towards the elimination of malaria in the targeted areas.
Discussion
The current study revealed that malaria remains a public health problem in Jazan region, with a total of 1124 confirmed cases were reported among the febrile patients presented at healthcare centres during the study period. Since the introduction of a malaria elimination strategy in 2004, the burden of malaria in Saudi Arabia has been markedly reduced, and the country has successfully decreased the burden and geographic extent of malaria nationwide [
29]. However, a limited number of malaria foci remain in Jazan and Aseer regions in southwestern Saudi Arabia [
9,
30].
In the current study, the percentage of febrile subjects found positive for malaria parasites was higher than that reported by previous studies conducted in Jazan and some other regions of the country, including the Makkah region and in the Al-Ahsa governorate in Eastern province [
30‐
33]. El Hassan et al. [
9] showed a dual trend of malaria cases in Jazan between 2000 and 2014, i.e., a significant reduction in autochthonous malaria cases (from 35.3 per 10,000 population in 2000 to the lowest rate of 0.11 cases per 10,000 population in 2014) and a constant number of imported malaria cases. A similar situation was also reported in the neighboring Aseer region [
30]. However, since 2015, a steady rise in malaria cases in both Jazan and Aseer regions has been noted [
34,
35], and this observation is supported by the findings of the current study. Compared to the very low proportion of autochthonous cases reported annually as compared to imported cases since 2014, the current study found that 4.5% (51/1124) of the cases can be considered autochthonous, with autochthonous cases reported during the outbreak in Baysh governorate were excluded. Hence, generally, it can be said that Saudi Arabia continues to make good progress toward achieving the WHO E-2020 goal [
1].
Moreover, the current study revealed that malaria transmission is still active in Jazan region with malaria cases identified in 14 governorates (out of 17) during the study period. The findings also showed that malaria in Jazan region occurs throughout the year without any obvious seasonal patterns, a finding that coincides with that reported by a previous study conducted in Aseer region [
30]. Likewise, the findings also demonstrated that the monthly number of malaria cases was consistent in all governorates, except Baysh. Indeed, an outbreak of falciparum malaria was reported in Baysh governorate from November 2018 through January 2019, with an approximately two- to three-fold increase in the number of confirmed cases relative to the mean number of cases for the same months in the five preceding years plus two times the standard deviation [
36,
37]. Despite a lack of authoritative information on its spread and determinants, this outbreak could be attributed to a combination of factors, including unusual heavy rainfall and flooding in Jazan region including Wadi Baysh (the largest perennial stream in Saudi Arabia) for 2–3 months before the onset of outbreak, which may have caused an increase in vector breeding sites as well as the arrival of new efficient vectors [
18,
21]. Moreover, the Baysh dam, built in 2009, is one of the largest dams in the country and is situated along the mainstream of Wadi Baysh [
38]. Hence, it seems that, unless there are appropriate measures in place, the construction of dams for irrigation and hydroelectric generation could intensify malaria transmission by providing breeding habitats for prominent malaria vector species, especially in areas of unstable or limited transmission [
18,
39]. In addition, increased cross-border importation of malaria [
34] and poor awareness of malaria prevention measures among the general population [
40], as well as the emerging resistance of the parasites to treatment and the resistance of the vectors to insecticides might also have contributed to this outbreak [
19]. Therefore, this malaria outbreak indicates that there is a need for rigorous impact assessments of metrological and climate change-related variables as well as dam-related environmental factors in Jazan region.
The current findings also showed that
P. falciparum was the predominant cause of malaria in Jazan which is consistent with previous reports [
35,
41]. The majority of vivax malaria cases identified by the current study were among non-Saudi patients, particularly Pakistani patients followed by Indian and Yemeni patients, as compared with only three cases among the Saudi patient group. Although
P. falciparum is the predominant species in the neighbouring endemic country, Yemen [
42,
43], the incidence of vivax malaria has been rising since 2015 [
4]. In addition, it was recently estimated that over three quarters (79·5%) of the global burden of vivax malaria in 2017 was attributable to India, Pakistan and Ethiopia [
4].
As regards the distribution of cases according to demographic factors, the current findings showed that malaria was present among all age groups including children below 5 years. However, the percentage of positive for malaria was the highest among patients aged 18–30 years, which corresponds with previous reports [
30,
32]. This finding could be explained by the higher mobility and occupation-related factors among adult individuals, which may lead to higher exposure to mosquito bites. Similarly, the higher percentage of cases reported in the current study among males could be attributed to behavioral differences and the customs and the traditions in the country. For instance, the female population wears clothes that cover the entire body, whereas the male population tends to wear lighter clothing that exposes arms and legs thereby increasing susceptibility to mosquito bites. However, it should be borne in mind that the reported difference could be attributed to the low number of female participants involved in this study. A greater likelihood of infection among the male population has been reported by previous studies undertaken in Jazan region and elsewhere [
35,
44,
45]. In contrast, other studies have demonstrated that women are 40% more likely than men to contract malaria and that pregnant women are at greater risk of malaria infection and also suffer higher morbidity and mortality [
46,
47].
In addition, the findings showed significantly higher percentage of malaria among non-Saudi patients as compared with Saudi patients, with more than half (54.2%) of the cases found among Yemeni patients. These findings are consistent with those previously reported for Jazan [
9,
35]. Moreover, among a total of 318 malaria cases reported in Makkah region between 2008 and 2011, non-Saudi patients accounted for 95%, with Pakistanis, Nigerians, and Indians accounting for 62.0% [
32]. Similarly, out of 3151 malaria cases reported in all regions of the country in 2017, 2974 (95%) were imported cases, while the remaining 177 cases were autochthonous [
3].
The porous international borders between countries represent a major challenge to the elimination of malaria, with the Saudi Arabia border with Yemen being a typical example [
34,
48]. The migration of malaria-infected humans has been shown to rapidly undermine gains made in malaria control efforts [
49]. In Saudi Arabia, imported malaria remains a major problem with a constant flow of imported malaria, mostly among immigrant workers from south Asia (Pakistan, India and Bangladesh), East Africa (Sudan and Ethiopia), and Yemen [
30,
50]. In an effort to address this problem, a collaborative Saudi Arabia and Yemen cross-border joint-programme of malaria control was launched in 2002 and remained operational until 2014 before it ceased due to the armed crisis in Yemen. As a result, the incidence of malaria in Jazan region dramatically decreased until 2014. However, between 2015 and 2017, it has been estimated that 32% of all imported infections detected in Saudi Arabia were of Yemeni origin [
34]. Coincidentally, the incidence of the locally acquired cases in Saudi Arabia increased [
9,
35]. Moreover, it should be noted that the majority of non-Saudi immigrant workers in the region reside in areas with poor housing and environmental settings that may favor mosquito breeding and malaria transmission. In general, malaria has been traditionally considered as less of a problem in urban areas compared with peri-urban slums
/settlements and rural areas [
51].
The association between climatic factors and malaria transmission has been extensively studied and the results are quite varied, thereby indicating that this association is complex. Nonetheless, such information from Saudi Arabia and Jazan region is lacking. Although rainfall is considered a critical factor that provides suitable breeding sites for mosquitoes, temperature is a key driver of many vital traits of the development and the life cycle of both the parasite and the mosquito [
52‐
54]. The current study showed that average temperature and relative humidity were the significant climatic determinants of autochthonous malaria in Jazan region. The findings on temperature are consistent with those in previous studies that demonstrated that temperature below 27 °C was associated with a high incidence rate, while a temperature over 30 °C was related to the lowest incidence rates [
55,
56]. The optimal temperature for malaria transmission ranges between 16 °C and 34 °C and peak transmission occurs at 25 °C [
53], which is 5–7 °C cooler than that estimated by other previous studies [
57,
58]. Likewise, a positive relationship between malaria and relative humidity has been demonstrated by previous studies elsewhere [
54,
55,
59]. High humidity (> 60%) is essential to enhance the lifespan of the mosquito and the development of the parasite in mosquitoes [
60].
The current study has some limitations that should be considered when interpreting the above findings. First, data on the distribution of malaria cases between April 2018 and January 2019 came from passive case detection among febrile patients presenting for healthcare at participating health facilities and this limited the ability to detect malaria infection among parasitaemic but asymptomatic individuals. It should be mentioned that according to the Saudi Ministry of Health’s statistics, 184,734 individuals were examined for malaria in Jazan region during 2018, and 1516 of them were found positive with a positivity rate of 0.82% [
36]. As a result, the current findings should be interpreted with caution and evaluated as part of the larger context of the malaria situation in the region. Second, as malaria in Jazan is mostly imported, the association between climatic variables and malaria had to rely on small monthly number of autochthonous malaria reported during the period of 2010–2017. Third, the positive cases reported in this study involved only eight out of 17 governorates of Jazan region. Indeed, Farasan Island and Fayfa highlands were reported malaria-free [
18], while all other governorates share similar epidemiological characteristics. Thus, the findings can be generalized to include those governorates; however, further studies are required to investigate this conjecture.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.