|Year : 2019 | Volume
| Issue : 1 | Page : 25-31
Some considerable issues concerning malaria elimination in India
ICMR–National Institute of Malaria Research, Field Unit, Panaji, Goa, India
|Date of Submission||31-Mar-2019|
|Date of Web Publication||7-May-2019|
Dr Ashwani Kumar
Scientist ‘G’ & Officer Incharge, ICMR-National Institute of Malaria Research, Field Unit, Campal, Panaji–403 001, Goa
Source of Support: None, Conflict of Interest: None
Malaria elimination is a health priority of India for the national development and to meet UN sustainable development goals. In this article, an attempt has been made to highlight some of the key issues that need attention and consideration. These include addressing the gaps in malaria burden and adopting District Health Information System (DHIS) for real time data gathering, transfer and analysis for rapid response. The article highlights threat to malaria elimination from human migration, asymptomatic malaria, P. malariae as a neglected species, need for updating vector information and devising strategies to control relay vector species especially in the high burden states of India. Additionally, scale-up of vector control interventions, integrated vector management and enhancement of vector control capacity and capability have been emphasized. It is suggested that process, performance and progress indicators for malaria elimination may be clearly spelt out and disseminated. What are the data needs for malaria elimination certification, must be well-understood? Lessons learnt by the countries that have eliminated malaria recently shall be of great value to malaria elimination efforts in India.
Keywords: Asymptomatic malaria; integrated vector management; malaria elimination; migration; national programme; Plasmodium malariae
|How to cite this article:|
Kumar A. Some considerable issues concerning malaria elimination in India. J Vector Borne Dis 2019;56:25-31
| Introduction|| |
Being seventh largest country in the world by geographical area, India is the second most populous country with 1.339 billion people. According to UN estimates, about 1.251 billion (93.4%) population is at risk of malaria in India. Of this, 162.45 million (12.1%) is at high to very high risk of malaria. India is world’s most culturally, linguistically, and genetically diverse geographical entity, after the African continent. India’s urban population has increased 11 fold during the 20th century which created problem of malaria in urban areas. The migrants from rural areas brought in malaria parasites and seeded transmission via local Anopheles (Diptera: Culicidae) vectors, viz. Anopheles stephensi in urban and An. culicifacies in the peri-urban settings, where migrants usually settle in the slums. Besides these two major vectors in India, An. fluviatilis (in the foothills), An. minimus (foothills of Himalayas), An. dirus and An. baimaii (in the northeastern states) and An. sundaicus (in the Andamans) are the other primary vectors. Additionally, An. annularis, An. barbirostris and An. philippinensis are three secondary vectors. With three prevalent human Plasmodium species, viz. Plasmodium falciparum, P. vivax and P. malariae, diverse weather conditions, human ethnicity, ongoing urbanization and population movement, the disease epidemiology is quite complex in India.
India contributed 4% to the global burden of malaria in terms of malaria incidence and deaths according to World Malaria Report. On February 11, 2016 National Framework for Malaria Elimination (NFME) was unveiled by the Union Minister for Health and Family Welfare, Govt. of India with an aim to eliminate malaria in three phases 2020, 2022 and 2027 followed by three years of sustenance of zero indigenous transmission and attainment of malaria-free status by the year 2030. This fits well into WHO’s Global Technical Strategy for Malaria Elimination 2016–2030 wherein, it has been envisaged to eliminate malaria in 35 countries by the year 2030. In this article, the author has attempted to raise some critical issues that need attention and consideration while achieving elimination of malaria for national development and for the overall achievement of the UN sustainable development goals.
True malaria burden and its implication on malaria elimination targets
National Vector Borne Disease Control Programme (NVBDCP) of India has an extensive surveillance network throughout the country by which about 10% of 1.3 billion population is being screened for malaria annually either by microscopy or rapid diagnostic test (RDT) methods. This by far is the largest surveillance network for any disease in the world. According to the World Malaria Report 2018 published by WHO, the reported incidence of malaria in India was 844,558 cases, of which 306,768 and 537,790 were diagnosed by microscopy and RDTs, respectively in the year 2017. Besides, there were 194 deaths due to malaria in 2017. However, during the same period WHO estimated 9.59 (95% UI: 6.965–13.26) million malaria cases and 16,733 (95% UI: 1200–31900) deaths attributable to malaria in India.
Earlier, global malaria mortality trends published have suggested 46,970 (95% UI: 14,757–94,945) deaths for individuals of all ages in India in the year 2010. A committee constituted by the Government of India arrived at an estimate of 9.751 million malaria cases and 40,297 deaths due to malaria (95% UI: 30,014–48,660) in the year 2010.
Having said, both reported and estimated cases and deaths have shown steady decline in the past decade. Reported number of malaria cases have declined from 1,599,968 in 2010 to 844,558 in 2017 and deaths from 1018 to 194, respectively. The WHO estimated cases have correspondingly reduced from 20.4 (95% UI 15.08–28.3) million to 9.59 (95% UI 6.95–13.2) million, i.e. by 53%. Similarly, estimated number of deaths due to malaria have also declined from 30,930 (95% UI 2770–58,600) in 2010 to 16,733 (95% UI 1200–31,900) in 2017, i.e. by 54%. In the World Malaria Report 2018, India has been complimented for reporting 3 million fewer cases in the year 2017, a reduction in malaria incidence by 24% compared to 2016.
The significant gap between reported and estimated cases and deaths has bearing on the basis on which the progress of malaria elimination is to be measured over time with respect to the baseline data. Hence, there is need to explain, debate and account for malaria cases that might have remained out of the ambit of national statistics for various reasons. If and when the revised figures of malaria incidence and deaths are agreed upon, the states and union territories of India would have to be reclassified under each of the four categories proposed on the basis of API as a primary criterion in the National Malaria Elimination Framework document. Similar exercise will be needed in the National Strategic Plan for Malaria Elimination (2017–2022) to re-categorize districts of India on the basis of revised API.
Real-time data gathering, transfer, analysis and rapid response for malaria elimination
India is progressively becoming digital under the recent initiatives of the Government of India. It is time to move away from cumbersome, slow and paper-based data gathering, reporting and documentation and adopt a system of real-time data gathering and dissemination in malaria programme. In this regard, use of cell phones offers a huge advantage in disease surveillance, intervention, monitoring and evaluation. Backed by an extensive network of transmission towers and multiple service providers, India has one of the highest densities of cell phones in the world. This offers a great opportunity for data acquisition and transfer directly from the field to the server, e.g. after diagnosing and treating malaria cases with their geographical coordinates. In this regard, District Health Information System (DHIS) which is freely available software, enables real-time data transfer and hot spot/cluster mapping of cases, decision making for investigation and intervention in 1, 3, 7 mode (https://district-health-information-system.soft112.com/). DHIS is recommended by Global Fund to fight against AIDS, Tuberculosis and Malaria and UNICEF. DHIS is an open source software platform for reporting, analysis and dissemination of data for health programmes and is at present used in more than 60 countries. The latest version 2.27 of DHIS covers aggregated data, e.g. routine health facility data, staffing, equipment, infrastructure, population estimates, and event data like disease outbreaks, survey/audit data, patient satisfaction surveys, longitudinal patient records, etc. The system is flexible and supports the capture of data linked to any level in an organisational hierarchy, any data collection frequency, a high degree of customization at both the input and output sides. DHIS-2 comes with easy to use analytics through tailored dashboards, charts, pivot tables and maps, thus enables easy data analysis and hot spot mapping. Introducing DHIS in India, in true letter and spirit, offers several advantages, viz. greater transparency, real-time data gathering, faster data analysis followed by prompt malaria control interventions, all of which are necessary for the success of malaria elimination programme. Additionally, DHIS will be a useful tool for case-based investigations and follow-up to effectively deal with residual transmission and for mounting rapid response in case of any unexpected event occurring during the sustenance phase.
Human migration and malaria elimination
Human migration has been implicated in seeding transmission of malaria in India,,. It is also a cause of spreading drug resistant and virulent strains. Human migration is a dynamic and complex phenomenon. People move for various reasons—(i) economic activity, e.g. labour movement for project work, agriculture, gem/metal mining, etc; (ii) under distress due to famines, floods, earthquakes, conflicts, etc. and (iii) for recreation and tourism. Migration may affect structure of native population permanently or temporarily/seasonally. In addition, there are communities such as nomads and tribes who are constantly on the move and may constitute a reservoir of malaria infection and, therefore, pose a threat to malaria elimination efforts. These communities are marginalized and generally detached from the national mainstream and rarely access health services. There is, therefore, need to frame a policy which is inclusive in nature to test, treat and track mobile ethnic groups to shrink this mobile malaria reservoir.
In India, many cities have seen influx of large contingent of migrant workers from rural areas in search of work especially in the construction sector. Mumbai, Goa, Mangalore, Kolkata and many other cities of India have experienced severe outbreaks of malaria and dengue in the last three decades, all of which were linked to human migration for construction activities and water storage practices,,. Migrants not only bring in different Plasmodium strains but also live in environment highly conducive to malaria transmission. Studies have shown that within and around construction complexes in the developing cities, malaria vector An. stephensi breeds merrily especially in the curing waters, cisterns and waterlogged basements. This proximity of human malaria reservoir and the vectors have resulted in several explosive malaria outbreaks in the past,,,. Similarly, other developmental projects such as railways, bridges, roads, irrigation systems and dams employ large contingents of migrant workers who would not only pose threat to the ongoing efforts to eliminate malaria but also might reintroduce malaria in the post-elimination phase. Hence, introduction of malaria infections through migrants will remain a threat to the cluster of states and UTs in the category 0 and 1 that are aiming to achieve malaria elimination by 2020 from the moderate to high burden states where malaria elimination is targeted in 2022 and 2027. During and post-malaria elimination scenario, reintroduction of malaria through human migration from within India and transnational borders would be a major challenge to deal with. Hence, special emphasis may be laid on to keeping track of human migration and taking timely steps to prevent transmission from introduced cases of malaria. It is proposed to use long-lasting insecticidal nets (LLINs) as front line vector control intervention amongst migrant workers both in the rural and urban developmental sites. Introducing and supplementing LLINs to the ongoing antilarval interventions in the urban developmental sites will be highly effective and beneficial for elimination of urban malaria and hence may be considered by the programme.
Asymptomatic malaria elimination
In malaria endemic areas, continuous exposure to Plasmodium parasites leads to asymptomatic carriers that provide a fundamental reservoir of parasites, contributing to the persistence of malaria transmission. In Chhattisgarh state of India, prevalence of asymptomatic malaria in tribal population was found to be 20 and 22.8% while overall prevalence was 27.6 and 27.7% in the years 2013 and 2014, respectively. In this study, prevalence rate of asymptomatic malaria was significantly higher in children ≤14 years (34%) compared to adults (15–18%). Of the total 103 malaria positive patients, 77% were afebrile. PCR detected significantly higher number of P. falciparum and P. vivax as compared to RDTs and microscopy.
In Thailand, despite a great decline in malaria incidences in recent years, transmission is going on at levels undetectable by microscopy, which is traditionally used. The authors, on the basis of serosurveillance with protein array methods, concluded that current routine methods used for surveillance will not be able to detect and treat asymptomatic and submicroscopic infections which will be a threat to malaria elimination in that country.
Similarly, in Iran, Zoghi et al carried out study in 3 provinces with negligible prevalence of malaria with microscopy, PCR and seroprevalence with suitable serological markers. In each province, 500 afebrile persons were randomly screened for malaria. No case of asymptomatic malaria was detected with microscopy and PCR. However, low seroprevalence of 0.45% P. vivax and 0.2% P. falciparum was detected. In Myanmar, prevalence of asymptomatic malaria infection was 2.3% (11/485) detected by Real-Time PCR which included 8 (72.7%) P. vivax cases and 3 (27.3%) P. falciparum cases. Men were at greater risk than women. In conclusion, the asymptomatic malaria may show high geographic variability depending upon the intensity of transmission and stability of malaria in a particular region.
In general, the problem of asymptomatic malaria is not well-researched and understood in India although, it forms a silent parasite reservoir that will continue to drive transmission especially during high transmission season and in the high burden states of the country. Therefore, asymptomatic malaria is perceived as a single most important threat to the elimination of malaria and must be addressed by devising appropriate policy for surveillance and treatment of asymptomatic Plasmodium carriers to deplete and eliminate asymptomatic reservoir.
Neglected species Plasmodium malariae
P. malariae is one of the five currently recognized human malaria parasite species. It is distinct from other species by being highly benign and quartan in rhythm. In the endemic regions, prevalence of P. malariae ranged from <4 to > 20% but there are several reports indicating that P. malariae cases are under-reported,,,,,,. Clinical presentation of quartan malaria is generally mild because of low parasitaemia, chronicity of infection and high host immunity. P. malariae is notorious for its persistence in the blood, often for the entire lifetime of an infected person. In malaria high burden areas, mix infection of P. malariae was detected with other species, viz. P. vivax (Pm + Pv), P. falciparum (Pm + Pf) and both these species (Pm + Pv + Pf). Although, P. malariae alone has low morbidity rate, it does contribute to the overall morbidity caused by concomitant Plasmodium species, as manifested in the incidences of anaemia, low birth weight and reduced resistance to other infections. A case in point is the reporting of several cases of complicated malaria and renal failure treated at the Ispat General Hospital in Rourkela Steel city where mix infection of P. malariae and P. falciparum was present [Table 1].
|Table 1: Increasing trend of complicated malaria and Acute Renal Failure (ARF) cases observed in Ispat General Hospital (IGH) Rourkela, Odisha|
Click here to view
Several Anopheles species have shown competence to transmit P. malariae in India as well as globally. Indian vector species that have been implicated are An. culicifacies, An. stephensi, An. aconitus, An. jeyporiensis, An. fluviatilis, An. minimus, An. splendidus, An. varuna and An. annularis. Since, all listed vector species are amenable to currently recommended control methods in areas targeted for malaria elimination, no special strategy would be necessary. Mass drug administration with chloroquine may be considered for clearing reservoir in humans to curtail transmission. However, the worry is that the presence of P. malariae is not even recognized and the species does not figure in either global or national malaria elimination agenda which is focused primarily on P. falciparum and P. vivax elimination. The problem is that reliable and complete statistics on P. malariae prevalence is not readily available as very limited studies have been undertaken. In that sense, P. malariae is a neglected species in both the Indian and global context. Hence, there is need to broaden scope of malaria elimination agenda by including P. malariae as one of the target species. Since routine diagnosis may not be appropriate to detect P. malariae, more sensitive method (PCR for example) may be used in its surveillance followed by treatment. Since P. malariae infection is usually asymptomatic, the overall policy recommended to address asymptomatic malaria may also be adequate to address this problem.
Updating vector information and addressing relay vector species
Although, several primary and secondary vector species have been recognised, there is need to discern role played by each of the sympatric vector species in local disease transmission. As an example, An. culicifacies, An. fluviatilis and An. annularis transmit malaria in forested areas during different seasons in the malaria high burden states of India. Similarly, An. minimus and An. dirus (and also An. baimaii) transmit malaria in the northeastern states of India. Studies are needed to identify weak links or bottleneck in the populations of these vector species for strategizing vector control tool selection and appropri time of intervention so as to squeeze and break malaria transmission chain. Operational research is, therefore, needed on relative abundance and incrimination of relay vector species to understand their seasonality and relative role in malaria transmission in the high burden states of the country. Also, true potential of certain Anopheles species such as An. annularis and An. subpictus (sibling species B) in malaria transmission is not fully understood and appreciated, although several reports have emerged recently implicating these species as malaria vectors,,,,.
Outdoor biting and resting species such as An. dirus and An. baimaii are the sibling vector species in many countries of South East Asia including in the northeastern states of India,,,. Being primarily exophilic and exophagic, the populations of these vectors are refractory to IRS. The extent of outdoor transmission of malaria attributed to An. dirus species complex needs to be discerned as this has implications for malaria elimination in India and South East Asia.
Scale-up of vector control interventions
One of the aims of the National Strategic Plan for Malaria Elimination 2017-2022 (NSP) put out by NVBDCP is to achieve near universal coverage of population at risk of malaria with appropriate vector control tools (www.nvbdcp.gov.in/Doc/nsp_2017–2022.pdf). As per the World Malaria Report (2018), indoor residual spraying (IRS) and LLINs were the two major vector control interventions used in India in 2017. These interventions were however, selectively used as indicated by population coverage of 39,341,409 (3.14%) residents under IRS out of 1.251 billion population at risk of malaria. Similarly, 16,340,000 LLINs were distributed covering additional 40,850,000 (3.26%) population of the country. Considering half of the population residing in areas at a very high to high risk of malaria lacks any of these two key interventions, there is an urgent need to scale-up IRS and LLINs in these areas.
As and when it appears, development of pyrethroid resistance in Indian vectors, especially in the moderate and high malaria burden states, will be a major threat to malaria elimination. Pyrethroid resistance will make IRS and LLINs, the two major vector control interventions redundant. Many African nations are currently grappling with problem of pyrethroid resistance in their major vectors, An. gambiae and An. funestus forcing the introduction of PBO nets, at a much higher cost as compared to the simple LLINs. Hence, concurrent assessment of pyrethroid resistance in major malaria vectors and a sound resistance management strategy are necessary for evidence-based decision making by the programme.
Integrated vector management
There is room for intervention mix in the form of integrated vector management (IVM) advocated by WHO (www.who.int/neglected_diseases/vector_ecology/ ivm_concept/en/). IVM approach is flexible and can be tailored to suit local vectors and epidemiological situation by selecting appropriate vector control tools among those advocated by the programme especially for the urban and peri-urban areas. The national programme has formulated and issued guidelines in this regard in 2015 (http:// www.nvbdcp.gov.in/Doc/IVM10_March_2016.pdf). Urban malaria which has been a major worry for the municipal bodies can be effectively tackled with environmental management (vector source reduction) and manipulations (vector source modification, e.g. mosquito proofing of water cisterns); larvicides (Biological/ chemical/IGRs); biological control with larvivorous fishes (Gambusia affinis and Lebistes reticulatus), thermal and cold fogging for vector knockdown and focal IRS in slums. As emphasized elsewhere, there is great scope and justification for protecting the migrant population with LLINs which is at high risk of malaria especially in labour hutments and slums in the developing cities which have been witnessing large influx of migrant populations from endemic areas of the country.
Vector control capacity and capability
A high quality, recurrent vector surveillance is of utmost importance for evidence-based vector control and for monitoring and evaluation of the interventions for delivery and impact assessment. WHO’s Global Vector Control Response 2017–2030 (GVCR 2017) endorsed by the World Health Assembly in 2017, recognises enhanced vector control capacity and capability as one of the foundations of GVCR which envisages increase in the number of entomologists and appropriate field and laboratory capacity to strengthen vector surveillance and control (https://www.who.int/neglected_diseases/vector_ecology/ resources/WHO_HTM_GVCR_2017.01/en/).
Malaria elimination process and performance indicators
As envisaged in NFME 2016–2030 and NSP 2017–2022 documents, there is time frame in which malaria elimination must be achieved in different states and UTs of the country. To track success of malaria elimination efforts over time, both performance and outcome indicators need to be clearly identified and spelt out. For example, if the outcome indicator is the reduction in malaria incidence, then states and UTs need to understand that at what rate and time frame, progressive reduction in malaria incidence is to be achieved so that by the end of the deadline ‘0’-transmission’ is evident and can be demonstrated. Also, the process indicators to achieve various milestones must be clearly known. Additionally, what evidence would be necessary for malaria elimination certification, e.g. entomological (vector numbers, EIR), parasitological (ABER, SPR and API), immunological (seropositivity in different ages) and number of deaths. Also, the methods and interventions used to achieve these milestones must be quantified and documented. There is scope for training of the senior state health officials by the management experts on how to manage the end of malaria and sustenance of ‘0’-transmission. It is believed that the last mile will be the most difficult to cover. Finally, lessons learnt by the countries, viz. Sri Lanka, Kyrgyzstan, Armenia, Maldives, Morocco, Turkmenistan and United Arab Emirates (UAE) which have eliminated malaria recently, would be of great value for the success of Indian malaria elimination programme.
| Acknowledgements|| |
Author is grateful to the Director General, ICMR for the initiative and to ICMR-National Institute of Malaria Research, New Delhi for providing facilities.
| References|| |
Murray CJL, Rossenfeld LC, Lim SS, Andrew KG, Foreman KJ, Haring D, et al
. Global malaria mortality between 1980 and 2010: A systematic analysis. The Lancet
|5.|Report of Expert Committee for estimating malaria mortality in the country
. Delhi: Ministry of Health and Family Welfare, Govt. of India 2011; p. 1-53.
Kumar A, Sharma VP, Thavaselvam D. Malaria related to constructions in Panaji, India. Indian J Malariol
Dash AP, Valecha N, Anvikar AR, Kumar A. Malaria in India: Challenges and opportunities. J Biosci
Sharma P. Malaria cases rise in Mumbai: BMC blames migrants DNA
Prothero R. Population movements and problems of malaria eradication in Africa. Bull World Health Organ
Louis P. Marginalization of tribals. Economic Political Wkly
2000; 35(47): 4087-91.
Kumar A, Thavaselvam D. Breeding habitats and their contribution to Anopheles stephensi
in Panaji. lndian J Malariol
Adsul BB, Payal SL, Prashant VH, Ramesh MC. Health problems among migrant construction workers: A unique public–private partnership project. Indian J Occup Environ Med
2011; 15(1): 29-32. doi: 10.4103/0019-5278.83001.
Dayanand KK, Punnath K, Chandrashekar V, Achur RN, Kakkilaya SB, Ghosh SK, et al
. Malaria prevalence in Mangaluru City area in the southwestern coastal region of India. Malar J
492. doi: 10.1186/s12936-017-2141-0
Chourasia MK, Raghavendra K, Bhat RM, Swain DK, Valecha N, Kleinschmidt I. Burden of asymptomatic malaria among a tribal population in a forested village of central India: A hidden challenge for malaria control in India. Public Health
Baum E, Sattabongkot J, Sirichaisinthop J, Kiattibutr K, Jain A, Taghavian O, et al
. Common asymptomatic and submicroscopic malaria infections in Western Thailand revealed in longitudinal molecular and serological studies: A challenge to malaria elimination. Malar J 2016; 15: 333. doi: 10.1186/s12936-016-1393-4.
Zoghi S, Mehrizi AA, Raeisi A, Haghdoost AA, Turki H, Safari R, et al
. Survey for asymptomatic malaria cases in low transmission settings of Iran under elimination programme. Malar J
2012; 11:126. doi: 10.1186/1475-2875-11-126.
Zaw MT, Thant M, Hlaing TM, Aung NZ, Thu M, Phumchuea K, et al
. Asymptomatic and sub-microscopic malaria infection in Kayah State, eastern Myanmar. Malar J
2017; 16(1): 138. doi: 10.1186/s12936-017-1789-9.
Beljaev AE, Brohult JA, Sharma GK, Haque MA, Samantaray KC. Studies on the detection of malaria at primary health centres. Part I. Reliability of parasitological diagnosis by decentralized laboratories. Indian J Malariol
1985; 22(2): 85-103.
Beljaev, AE, Brohult JA, Sharma GK, Haque MA, Samantaray KC. Studies on the detection of malaria at primary health centres. Part III. Parasitological profile of population surveyed for malaria through passive case detection. Indian J Malariol
1987; 24(2): 97-106.
Raichowdhuri AN, Choudhury DS, Regis ML. Simultaneous propagation of P. malariae
and P. falciparum
in a continuous culture. Indian J Med Res
William EC, Jeffery GM. Plasmodium malariae:
Parasite and disease. Clinical Microb Rev
2007; 20(4): 579-92.
Yadav RS, Ghosh SK, Chand SK, Kumar A. Quartan malaria–An investigation on the incidence of Plasmodium malariae
in Bisra PHC, District Sundergarh, Orissa. Indian J Malariol
Yadav RS, Ghosh SK, Chand SK, Kumar A. Prevalence of malaria and economic loss in two major iron ore mines in Sundergarh district Orissa. Indian J Malariol
1991; 28(2): 105-13.
Rutledge GG, Böhme U, Sanders M, Reid AJ, Maiga-Ascofare O, Abdoulaye A, et al. Plasmodium malariae
and P. ovale
genomes provide insights into malaria parasite evolution. Nature
Panicker K, Bai MG, Rao UB, Viswam K, Murthy US. Anopheles subpictus
, vector of malaria in coastal villages of south-east India. Curr Sci
Kumari S, Parida SK, Marai N, Tripathy A, Hazra RK, Kar SK, et al
. Vectorial role of Anopheles subpictus
Grassi and Anopheles culicifacies
Giles in Angul district, Orissa, India. South East Asian J Trop Med Public Health
Surendran SN, Singh OP, Jude PJ, Ramaswamy R. Genetic evidence for malaria vectors of the Anopheles sundaicus
complex in Sri Lanka with morphological characteristics attributed to Anopheles subpictus
species B. Malar J
Sinka ME, Bangs MJ, Manguin S, Chareonviriyaphap T, Patil AP,Temperley WH, et al
. The dominant Anopheles
vectors of human malaria in the Asia-Pacific region: Occurrence data, distribution maps and bionomic précis. Parasit Vectors
89. doi: 10.1186/1756-3305-4-89.
Kumar A, Hosmani R, Jadhav S, DeSouza T, Mohanty A, Naik M, et al. Anopheles subpictus
carry human malaria parasites in an urban area of western India and may facilitate perennial malaria transmission. Malar J
Tananchai C, Tisgratog R, Juntarajumnong W, Grieco JP, Manguin S, Prabaripai A, et al
. Species diversity and biting activity of Anopheles dirus
and Anopheles baimaii
(Diptera: Culicidae) in a malaria prone area of western Thailand. Parasit Vectors
2012; 5: 211. 5-211.
Obsomer V, Defourny P, Coosemans M. The Anopheles dirus
complex: Spatial distribution and environmental drivers. Malar J
Pimnon S, Bhumiratana A. Adaptation of Anopheles
vectors to anthropogenic malaria-associated rubber plantations and indoor residual spraying: Establishing population dynamics and insecticide susceptibility. Canadian J Infect Dis Med Micro
2018. Article ID 9853409; p. 17.
Hancock PA, Wiebe A, Gleave KA, Bhatt S, Cameron E, Trett A, et al
. Associated patterns of insecticide resistance in field populations of malaria vectors across Africa. Proc Nat Acad Sci
2018; 115(23): 5938-43.