First record of Anopheles stephensi in Sri Lanka: a potential challenge for prevention of malaria reintroduction

Sri Lanka, an island in the Indian Ocean, achieved zero transmission of locally acquired malaria cases in November 2012. Following completion of three consecutive malaria-free years, Sri Lanka received the certification of elimination of malaria from the World Health Organization in September 2016. In the past few decades, malaria was a major public health problem, being endemic in 22 districts of the intermediate and dry zones of the country [1]. In Sri Lanka, the major vector of malaria is reported to be Anopheles culicifacies, and Anopheles subpictus, Anopheles annularis and Anopheles varuna are considered as potential vectors [2, 3].

With the cessation of local malaria transmission in the country, disease surveillance along with entomological surveillance have been strengthened to prevent the re-introduction of malaria. The largest threat for re-introduction of malaria into the country is the importation of malaria cases from endemic countries [4]. The influx of malaria parasites into the country are through security personnel returning from United Nations peace missions, asylum seekers coming through United Nations High Commissioner for Refugees (UNHCR), foreign workforces in different trades, and local migrants going to malarious countries on travel, business or pilgrimage. The abundance of local malaria vectors in the formerly malarious areas, even in the absence of malaria transmission, has made the country both vulnerable and receptive to the re-introduction of malaria [5].

Sri Lanka has a strong entomological surveillance system, since the 1930s, which has evolved based on the changing epidemiology of malaria transmission in the country. Apart from the period 2008–2014, during which a private organization (Tropical Environmental Diseases and Health Associates Pvt. Ltd (TEDHA)) assisted in several of the conflict-affected districts in Northern Province, including Mannar, the entomological activities on malaria vectors are conducted by the Anti Malaria Campaign (AMC), Sri Lanka.

Anopheles stephensi, belonging to the subgenus Cellia and Neocellia series, had never been reported from Sri Lanka until the current study first revealed evidence for its occurrence in two localities in Mannar District in December 2016. The latest available taxonomic key for the identification of Anopheles fauna of Sri Lanka published in 2016 described 23 Anopheles species [6]. This most recent identification key, nor those previously published by Carter [7], Amerasinghe [8], Amerasinghe [9], or Gunathilaka [10] included An. stephensi as a species found in Sri Lanka. However, An. stephensi is found in Afghanistan, Bangladesh, China, India, Indochina, Iran, Iraq, Myanmar, Pakistan, Taiwan, and Thailand [11]. This species is considered an important vector of Plasmodium falciparum and Plasmodium vivax throughout its natural range and is the main urban malaria vector of India, Pakistan, Iran, and Iraq [12‐14].

Considering the importance of An. stephensi as an urban vector of falciparum and vivax malaria in other countries, its breeding on Mannar Island could pose a serious threat to preventing the re-introduction of malaria and its transmission in Sri Lanka. Therefore, in December 2016, entomological surveillance in Mannar District was intensified for four consecutive months with special focus on six selected sampling blocks on Mannar Island. Larval and adult surveys were conducted with the primary aim of confirming the presence and bionomics of An. stephensi in Sri Lanka.

Anopheles stephensi is an important urban malaria vector in neighbouring countries, such as India and Pakistan, but has not before been reported from Sri Lanka. This is the first report of its presence in Sri Lanka based on the entomological surveillance studies that detected larvae and adults of the species Mannar Island, located in the dry zone area of the country. Presence of An. stephensi was confirmed on morphological identification and molecular evidence based on the DNA barcoding approach using the COI gene.

There is limited information on malaria vector surveillance studies carried out in the Northern Province of Sri Lanka prior to 2010, including in Mannar District, because of the 30-year war in that area. This lack of information is a major constraint in determining in absolute terms the absence of this particular species in the area. The most recent vector surveillance study in Mannar District was during 2010–2012, where Gunathilaka et al. studied Anopheles species composition and breeding habitat diversity, however, the presence of An. stephensi in Mannar District was not revealed in that study [26]. The Sri Lankan mosquito checklist has not been updated, following the attempts made by Jayasekara and Chelliah [27] and the dichotomous key prepared by Amerasinghe, until more recent attempts in 2014 and 2016; none of these studies reported An. stephensi in the country [6, 8‐10]. Because of this gap in knowledge it is unclear whether An. stephensi has been undetected on Mannar Island or whether this is a recent invasion. Invasion from a neighbouring Indian state may be a possibility since An. stephensi has been incriminated as the main vector of urban malaria in India, and has shown a southwards spread on the mainland due to rapid urbanization and water storage practices. Anopheles stephensi has caused malaria outbreaks in Kerala State, India where such epidemics were not reported until 1996, and it is now reported breeding in water storage tanks in Lakshadweep islands off the coast of Kerala, indicating possibilities of invasion of islands [11, 28, 29].

Similarly, An. stephensi in Mannar Island breeds in water storage containers, mainly in domestic wells with cemented walls, where the highest percentage of breeding was recorded. Further co-existence of An. stephensi with An. culicifacies and An. varuna was also observed in wells. Anopheles stephensi breeding with other mosquito vectors such as Aedes aegypti, Aedes albopictus, Culex quinquefasciatus, and Culex vishnui has also been observed in studies in India [11]. In the absence of a continuous supply of water throughout the year, villagers, new settlers returning from India, and workforces involved in construction work and fishing depend on well water which has become an ideal breeding site for An. stephensi. Domestic wells with cemented walls appear to be permanent water bodies with the potential for breeding even in the dry season. It was also apparent that plastic barrels used by the local population for water storage were another potential breeding site which adds complexity to the situation. This container breeding habit of An. stephensi predominantly in wells, overhead or ground level water tanks, cisterns, tanks, coolers, roof gutters, curing pits in construction areas, fountains and ornamental tanks in urban areas has been observed in other countries [30]. Use of other small containers may be expected during the wet season.

Anopheles stephensi is considered an invasive species, which enters new towns and settlements. There is evidence of An. stephensi-related urban malaria in the African country, Djibouti due to introduction of An. stephensi from Asia. Suspected routes for this introduction were through transportation of goods of refugee returnees from the nearest geographically endemic peninsula [31]. Therefore, it is possible that the presence of An. stephensi is an invasion into Sri Lanka from India. The distance between Dhanushkodi in India and Talaimannar (Block B) in Sri Lanka is only 50 km, through the Palk Strait. There have been various attempts by fishermen of both countries to cross the borders for fishing. In Pesalai (Block A) the Sri Lanka Navy had informed the Regional Malaria Officer to carry out vector surveillance and vector control in the fishing boats of Indian fishermen who had in three instances crossed the border. Intersectoral collaboration with security personnel for vector surveillance activities in Mannar is an example of a recent initiative taken by the Ministry of Health in its efforts to keep Sri Lanka malaria free. Water storage utensils of the fishing boats may be potential breeding grounds for An. stephensi and the inside wall surfaces of these boats may harbour adult mosquitoes.

Anopheles stephensi control on Mannar Island by antilarval measures was initiated using 1% Temephos granules 1 mg/l and larvivorous fish Poecilia reticulata [32], and the resettled population in this area were provided with long-lasting insecticidal nets, Yorkool^®. In planning appropriate chemical-based vector control, knowledge of bionomics and biology of a vector species is an essential requirement. It must be a national priority to prevent further establishment of An. stephensi on Mannar Island and to curtail its spread to other parts of the country. A rigorous vector control strategy should be implemented with the support of other sectors to increase the awareness of local people of the potential threat of malaria re-introduction by this dangerous vector species. Closing abandoned wells, covering wells to prevent mosquito egg laying, and introduction of larvivorous fish can be carried out by the local population if a behavioural change awareness campaign were to be introduced. In addition to the health sector, the support of local authorities, the environmental sector and non-governmental organizations is of paramount importance in practising control interventions.

This paper describes the first confirmed report of An. stephensi in Sri Lanka. The post-war resettlement taking place in Northern Province, coupled with invasion of malaria vectors with or without parasites, may cause a serious threat to sustaining malaria-free status in Sri Lanka. Because An. stephensi is known to be a vector of urban malaria, if this species spreads to urban areas of Sri Lanka, it will have important implications for transmission of malaria as urban malaria has not previously been observed in Sri Lanka.

Urban malaria is quite a different situation to rural malaria in terms of transmission of the disease and disease risk assessments due to diversity of ecologies, exposure patterns and prevention opportunities, etc. [29]. Increasing numbers of people becoming residents of urban environments may cause prevention and control of malaria activities to be location specific. To minimize this risk of malaria transmission by An. stephensi in what appears to be an urban malaria situation on Mannar Island, not only should its further spread be controlled through vector control measures, its distribution should be monitored throughout Sri Lanka through active entomological surveillance. In mitigation of the present situation, the Ministry of Health needs to initiate a solid action plan to prevent the re-introduction of malaria into the country considering the potential of spread and establishment of An. stephensi into other areas of the country, and particularly considering the possible role it could play in transmission of urban malaria.