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Vythilingam et al. Parasites & Vectors 2014, 7:436 http://www.parasitesandvectors.com/content/7/1/436 RESEARCH Open Access Plasmodium knowlesi malaria an emerging public health problem in Hulu Selangor, Selangor, Malaysia (2009–2013): epidemiologic and entomologic analysis Indra Vythilingam1*, Yvonne AL Lim1, Balan Venugopalan2, Romano Ngui1, Cherng Shii Leong1, Meng Li Wong1, LokeTim Khaw1, XiangTing Goh1, NanJiun Yap1, Wan Yusoff Wan Sulaiman1, John Jeffery1, Ab Ghani CT Zawiah3, Ismail Nor Aszlina4, Reuben SK Sharma5, Lau Yee Ling1 and Rohela Mahmud1 Abstract Background: While transmission of the human Plasmodium species has declined, a significant increase in Plasmodium knowlesi/Plasmodium malariae cases was reported in Hulu Selangor, Selangor, Malaysia. Thus, a study was undertaken to determine the epidemiology and the vectors involved in the transmission of knowlesi malaria. Methods: Cases of knowlesi/malariae malaria in the Hulu Selangor district were retrospectively reviewed and analyzed from 2009 to 2013. Mosquitoes were collected from areas where cases occurred in order to determine the vectors. Leucosphyrus group of mosquitoes were genetically characterized targeting the nuclear internal transcribed spacer 2 (ITS2) and mitochondrial cytochrome c oxidase subunit I (CO1). In addition, temporal and spatial analyses were carried out for human cases and vectors. Results: Of the 100 microscopy diagnosed P. knowlesi/P. malariae cases over the 5 year period in the Hulu Selangor district, there was predominance of P. knowlesi/P. malariae cases among the young adults (ages 20–39 years; 67 cases; 67%). The majority of the infected people were involved in occupations related to agriculture and forestry (51; 51%). No death was recorded in all these cases. Five hundred and thirty five mosquitoes belonging to 14 species were obtained during the study. Anopheles maculatus was the predominant species (49.5%) followed by Anopheles letifer (13.1%) and Anopheles introlatus (11.6%). Molecular and phylogenetic analysis confirmed the species of the Leucosphyrus group to be An. introlatus. In the present study, only An. introlatus was positive for oocysts. Kernel Density analysis showed that P. knowlesi hotspot areas overlapped with areas where the infected An. introlatus was discovered. This further strengthens the hypothesis that An. introlatusis is the vector for P. knowlesi in the Hulu Selangor district. Unless more information is obtained on the vectors as well as macaque involved in the transmission, it will be difficult to plan effective control strategies. The utilization of modern analytical tools such as GIS (Geographic Information System) is crucial in estimating hotspot areas for targeted control strategies. Conclusions: Anopheles introlatus has been incriminated as vector of P. knowlesi in Hulu Selangor. The cases of P. knowlesi are on the increase and further research using molecular techniques is needed. Keywords: An. introlatus, Vector, P. knowlesi, Malaysia * Correspondence: [email protected] 1Department of Parasitology, Faculty of Medicine, University of Malaya, Kuala Lumpur, Malaysia Full list of author information is available at the end of the article © 2014 Vythilingam et al.; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Vythilingam et al. Parasites & Vectors 2014, 7:436 Page 2 of 14 http://www.parasitesandvectors.com/content/7/1/436 Background coastal areas, and An. maculatus in the hilly regions of pen- Malaria still remains a serious public health challenge in insular Malaysia, An. latens and An. balabacensis the pre- the tropics. However, with improved and effective treat- dominant vectors in Sarawak and Sabah, respectively ment coupled with the use of long lasting insecticide [26-28]. The malaria eradication programme worked very treated nets, the burden of disease has decreased over well in the coastal areas and the vectors were almost elimi- the years [1]. In highly endemic countries, this disease is nated due to their resting behavior indoors [29]. However, observed to be more preponderant in infants and young in the hilly regions of peninsular Malaysia, An. maculatus children [2]. Lately, with the decline in the number of remains the primary vector of human malaria. When the cases, a contrasting observation noted that older chil- first case of P. knowlesi infection was reported in Pahang, dren and adults are more susceptible to the disease. Malaysia, the Leucosphyrus group of mosquitoes was in- Historically, malaria used to be a major health concern criminated as the vectors. The vectors incriminated were in Malaysia with >200,000 cases in the 1960s [3]. The An. hackeri (for P. knowlesi) in the coastal area of Selangor introduction of a malaria eradication programme in the [30] and An. cracens (then known as An. balabacensis)in late 1960s, which continued to the late 80s has contrib- Perlis (northern region of peninsular Malaysia) (for Plasmo- uted to the significant reduction of malaria cases in dium inui) [31]. However, An. hackeri was found to only Malaysia to approximately 43,000 cases in the early 1990s. biting monkeys, and was not reported to bite humans. In During those years, the states of Kelantan, Pahang and 2006, An. latens was incriminated as a vector of P. knowlesi Perak had the highest number of cases in peninsular in Kapit Sarawak [32,33], An. cracens in Kuala Lipis Pahang Malaysia [4]. During the eradication period, DDT residual [25,34] and An. balabacensis in Sabah [35]. house spraying was the main method used to reduce The state of Selangor consists of nine districts and the malaria vectors. With economic development and the Hulu Selangor district had the highest number of know- introduction of insecticide treated bednets, malaria was lesi/malariae malaria cases (Records from State Health further reduced to approximately 12,000 cases in 2000. In Department). For the past five years, the cases of know- 2001, 12,780 cases were reported and this was significantly lesi/malariae malaria have also increased in Hulu Se- scaled down to 4,725 cases in 2012 [5]. langor. However, the vector involved in the transmission Four species of malaria parasites (namely Plasmodium of knowlesi malaria remained unknown in this district. falciparum, P. vivax, P. malariae and P.ovale) are known The national malaria program strategy has been reor- to affect humans. In 2004, Singh et al. [6] reported the iented from control to elimination, and Malaysia is now presence of a large number of P. knowlesi cases in Sarawak, working to eliminate malaria from the peninsular by a state in Malaysian Borneo. Subsequently, P. knowlesi be- 2015 and from Malaysian Borneo by 2020 [36]. came known as the fifth malaria parasite species to infect In view of these recent events, it is imperative that a humans [7]. Various studies have shown that P. knowlesi is holistic approach is adopted in order to understand the not only present in Malaysia but has a wider presence in transmission of P. knowlesi malaria better especially in other parts of Southeast Asia as well, namely Singapore this district. Thus, the objective of this study was to ana- [8-10], Thailand [11-14], Myanmar [15,16], Philippines [17], lyse the epidemiology of knowlesi/malariae malaria in Indonesia [18,19], Vietnam [20,21] and Cambodia [22]. To Hulu Selangor in a more comprehensive manner, taking date, only Laos and Timor-Leste are devoid of any reported into consideration the human infection and vector dis- P. knowlesi cases. tribution. This study actively collected mosquitoes from Lately, it was observed that as transmission of the hu- locations with human cases and in so doing, managed man Plasmodium species declined, a significant increase to determine the vectors in Hulu Selangor. Another in- in microscopy diagnosed P. knowlesi/P. malariae cases teresting feature of the study involved the temporal and were reported [23]. A similar trend was also observed in spatial analysis utilizing advanced tools such as GIS ana- peninsular Malaysia [24]. This was confirmed in the lysis to shed some light on the association of human Ministry of Health Annual Report that in 2012, P. know- infection and mosquito distribution in order to eluci- lesi was the predominant species comprising 38% of the date the transmission of P. knowlesi malaria in Hulu malaria cases in Malaysia followed by P. vivax (31% of Selangor. cases) [5]. In Malaysian Borneo, Sabah and Sarawak con- tributed most of the cases, whereas Pahang has always Methods had a high number of P. knowlesi malaria cases [24,25] Ethical clearance in peninsular Malaysia. This study was approved by the Medical Ethics Malaria is transmitted from one person to another by Committee of University of Malaya Medical Center the bite of the female infected Anophelesmosquito.The (UMMC), Malaysia (Reference number: 890.12) and the main malaria vectors in Malaysia are Anopheles campestris National Medical Research Register (Reference number: and An. sundaicus (now known as An. epiroticus)inthe NMRR-11-1050-10619). Prior to mosquito collection, Vythilingam et al. Parasites & Vectors 2014, 7:436 Page 3 of 14 http://www.parasitesandvectors.com/content/7/1/436 volunteers who consented were provided antimalarial (SPSS Inc, Chicago, USA). Categorical variables such as in- prophylaxis. fection rate was presented as frequencies and percentages. Epidemiology aspects Entomology Study site The study was carried out in the Hulu Selangor district This study was carried out in the state of Selangor, the from 2012 to 2013. Various locations were surveyed most developed state [23.5% of Malaysia’s total GDP within the district where knowlesi malaria cases were re- (gross domestic product) in 2012; Department of Statis- ported.
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