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Submission to UNFCCC by the Nepal Health Research Council (NHRC) in collaboration
with Goethe University, Frankfurt am Main, Germany
Institute
Nepal Health Research Council (NHRC), Kathmandu, Nepal (Dr. Meghnath Dhimal, Dr.
Krishna Kumar Aryal, Dr. Khem Bahadur Karki)
Collaborating Partners
Institute of Atmospheric and Environmental Sciences, Goethe University, Frankfurt am Main,
Germany (Prof. Dr. Bodo Ahrens)
Institute of Occupational Medicine, Social Medicine and Environmental Medicine, Goethe
University, Frankfurt am Main, Germany (Dr. Ulrich Kuch, Dr. Ruth Müller, Prof. Dr. David A.
Groneberg)
Contact details for further information
Dr. Meghnath Dhimal (PhD),
Email: meghdhimal@gmail.com
Country/Countries of Focus (Nepal and other countries of the Hindu-Kush Himalayan region:
Afghanistan, Bhutan, Bangladesh, China, India, Myanmar and Pakistan)
Research on climate change and the distributions of vector-borne diseases in the Hindu-
Kush Himalayan region – the case of Nepal
Abstract
In view of increasing concern about the impacts of climate change on vector-borne diseases
(VBDs) especially in tropical highlands and temperate regions of our planet, we carried out
international collaborative research in Nepal between 2011 and 2015. Nepal is located in the
central part of the Hindu-Kush Himalayan (HKH) region where at least seven VBDs (malaria,
lymphatic filariasis, Japanese encephalitis, West Nile fever, chikungunya fever, dengue fever and
visceral leishmaniasis) are endemic, and threat of Zika virus infection expected. The pathogens
causing these diseases are transmitted to or among humans by mosquitoes or sand flies which are
sensitive to temperature and thus to climate change. Hydro-meteorological data for the HKH
region are scarce, but the available data indicate that its warming trend is more pronounced than
the global trend. A shift of disease vectors and disease transmission to higher elevations has been
predicted under observed and future climate change scenarios, however, empirical data on the
expansion of VBDs in the HKH region was largely lacking. To address this knowledge gap, we
carried out entomological, climatological, social and epidemiological studies in Nepal in an
integrated eco-bio-social framework and compared our findings with literature on the
distribution of VBDs in the HKH region published up to September 2016. Our studies highlight a
more pronounced warming in the hills and mountains of Nepal and the HKH region overall
compared to other parts of the world. We found a distinct shift of disease vectors and VBD
incidence with autochthonous cases to previously non-endemic areas including hills and
mountains. Significant relationships between climatic variables and the occurrence of VBDs and
their vectors were revealed in short-term studies. The knowledge of people on the prevention and
control of VBDs was very low among our study populations in different highland and lowland
areas of Nepal. Given the establishment of relevant vectors up to at least 2,000 m above sea
level, increasing movement of people and goods between endemic and non-endemic areas, and
urbanization and poverty, climate change can intensify the risk of VBD epidemics in the fragile
HKH region and its vulnerable populations. The wide distribution of important disease vectors in
regions that had previously been considered to be non-endemic calls for regional collaboration in
extending and upscaling surveillance and control programs in the HKH region.
Keywords: Climate change, vector-borne diseases, mountain, Himalaya, poverty
1 Introduction
The Hindu-Kush Himalayan (HKH) region spans over four million square kilometers,
constituting approximately 18% of the world’s mountainous areas. This region includes all of
Nepal and Bhutan, and the mountains of Afghanistan, Bangladesh, China, India, Myanmar and
Pakistan [1]. The HKH region is particularly vulnerable to climate change because the rate of
warming in the Himalayas has been much greater (0.06°C yr-1) than the global average in the last
three decades [2]. Over 200 million people live in the mountains, valleys, and hills of the HKH
region and an estimated 3 billion people benefit from the water and other goods and services that
originate in the mountains of this region [1]. As evidence for the varied impacts of climate
change on public health is increasing, the published literature continues to focus on the effects of
climate change in developed countries and other parts of the world while the effects on mountain
populations residing in the HKH region are grossly underreported [3,4].
Vector-borne diseases (VBDs) which are transmitted to or among humans, livestock and wildlife
by arthropod animals (in the case of the diseases discussed here: mosquitoes or sandflies) are
sensitive to temperature, rainfall and humidity and thus, ultimately, sensitive to climate change
[5,6]. Any change in the geographical distribution of a VBD due to climate change, allowing a
vector and/or pathogen to shift to new areas, will have a profound effect on the exposure of naïve
hosts to those diseases [7]. As VBDs are emerging in highlands and high-latitude regions causing
significant morbidity and mortality, the role of climate change on VBDs should be explored as a
priority in those areas and countries where disease surveillance systems and reporting efforts are
weak [8]. It is estimated that more than half of the world’s population is already now at risk of
disease from insect-borne pathogens [9] and constitute an important cause of morbidity and
mortality, diseases burden and health inequality especially in developing and poor countries [10].
At least seven major VBDs, namely malaria, lymphatic filariasis (LF), Japanese encephalitis
(JE), visceral leishmaniasis (VL, also known as kala-azar), chikungunya fever (CHIK), dengue
fever (DF) and West Nile Fever (WNF) are endemic in the HKH region which is now also facing
the threat of Zika virus.
Figure 1. Map of the Hindu-Kush Himalayan region (from Dhimal et al., submitted manuscript)
As arthropods are ‘cold-blooded’ or poikilothermic animals, the period of their life-cycle and the
pathogen development in their body is affected by climate change [7,11,12]. The duration of the
growth season will increase in many regions with climate change, which means that more
generations of vectors may be produced each year in tropical highlands and temperate regions
[7]. Therefore, the greatest effect of climate change on VBD transmission is likely to be
observed in cooler areas where the minimum temperature is limiting disease transmission, and in
warmer areas where temperatures above 34°C have a negative impact on the survival of vectors
and pathogens [13-15]. Moreover, as the warming rate is higher closer to the poles and in
highlands compared to the tropics and lowlands [16,17], vectors and pathogens are experiencing
more differential warming in high latitudes and altitudes compared to lower latitudes and
lowlands [18].
Minimum criteria that have been suggested for accepting a causal relationship between climate
change and human VBDs are evidence of biological sensitivity to climate, meteorological
evidence of climate change, and evidence of entomological and/or epidemiological change in
relation to climate change [19]. The first two criteria are obvious, and the third one needs to be
explored using empirical data. Changes in the spatiotemporal patterns of climatic variables such
as temperature, precipitation and relative humidity under different climate change scenarios
based on RCPs, affect the biology and ecology of vectors and intermediate hosts and
consequently the risk of disease transmission [14]. However, the local adaptation of disease
vectors to micro-climatic variation may modulate the effects of both short- and long-term
changes in climate [20]. Moreover, climate, vector ecology, healthcare systems and socio-
economic status vary dramatically across geographical regions and countries and therefore
demand studies at the local level in each country and region.
Methodology
We used a broad ecological-biological-social conceptual framework which is consistent with the
´One Health´ concept to explore the geographical distribution of VBDs and their associated
factors in Nepal. Our international collaborative research project provided a unique opportunity
to explore and compare climate change related risks of VBDs with clear eco-socio-medical
relevance for people in mountain regions. Both qualitative and quantitative data were collected.
We studied the distribution of vectors along an altitudinal transect using standard entomological
techniques. We used BG-Sentinel traps, CDC light traps and aspirators with the support of
flashlights to capture adult mosquitoes. Immature mosquitoes were collected using locally
constructed dippers. Mosquito eggs were collected using ovitraps. We used epidemiological
surveillance data collected by the Epidemiology and Diseases Control Division (EDCD) and
Health Management Information System (HMIS) of the Ministry of Health, Government of
Nepal. Similarly, we used observed meteorological data collected by the Department of
Hydrology and Meteorology (DHM), Government of Nepal. Surveys on the knowledge, attitude
and practice of people regarding the prevention and control of VBDs were carried out using
structured questionnaires. In order to validate and elaborate quantitative data, we assessed local
residents’ perceptions of the distribution and occurrence of mosquitoes using key informant
interview techniques. Quantitative data were analyzed using modeling techniques and qualitative
data were analyzed using thematic content analysis techniques.
2 Key Results
Analysis of observed temperature data shows a warming trend in Nepal which is influenced by
maximum temperatures with higher warming rates in the mountain regions compared to the
lowlands of Nepal [21]. Precipitation does not show a distinct trend in Nepal. However, changes
in extreme events such as heavy rainfall, drought, cold days, hot days, consistent with climate
change effects, are more significant in Nepal [21]. The review of observed and future projections
of climatic data shows a conducive environment for the transmission of VBDs in the HKH
region, especially in the highlands (mountains) which had been assumed to be free from these
diseases [2,22-24]. However, inter-modal variability and uncertainties in temperature and
precipitation have been observed over the region.
The known malaria vectors in Nepal, Anopheles fluviatilis, Anopheles annularis and Anopheles
maculatus complex members, currently have established populations at least 1800 m above sea
level (asl) [25]. The vectors of chikungunya and dengue viruses (also Zika virus), Aedes aegypti
and Aedes albopictus, the main vector of lymphatic filariasis, Culex quinquefasciatus, and the
main vector of Japanese encephalitis in Nepal, Culex tritaeniorhynchus, have established
populations at altitudes of at least 2,000 m asl [25-28]. Larvae of Anopheles, Culex and Aedes
species were found up to 2,310 m asl [25,26,28]. We also found significant relationships between
climatic variables and the abundance of disease vectors [26,28].
Our systematic review of climate change and the spatiotemporal distributions of VBDs in Nepal
and comparison of the results with those of other studies from the HKH region show a consistent
trend of VBD expansion in the HKH region [21]. Over the last decade, the distribution of these
diseases and their vectors, which were previously believed to be confined to tropical and sub-
tropical regions, is now observed to extend to the hills and mountains of the HKH region. For
example, the geographical area with autochthonous dengue virus transmission has extended to
include Bhutan and Nepal since 2004 and 2006, respectively [29,30] and the primary dengue
virus vector Aedes aegypti has already expanded its regional range to above 2,000 m altitude in
the region [26,31,32]. The first autochthonous cases of chikungunya virus infection (also
transmitted by A. aegypti) were reported in Bhutan and Nepal in 2012 and 2013, respectively
[33,34]. The presence of the principal vector of Japanese encephalitis virus (JEV), Culex
tritaeniorhynchus, and of JEV circulation itself in the mountain regions of Tibet and Nepal has
also been reported [35-37]. Despite significant declining trends of malaria in Nepal [38], malaria
hotspots have shifted to new areas which in the past had been regarded as low-risk areas so that
vector control interventions were not in place [39]. In addition, we found a significant effect of
ambient temperature on the incidence of malaria [39]. The climate and other environmental
changes are likely to affect malaria and other parasitic diseases elimination goals of Nepal and
other countries of HKH region [8,21,40-42].
The entomological findings are consistent with epidemiological findings from the region
[25,26,39]. More importantly, the knowledge of people residing in the highlands on the
prevention and control of diseases such as dengue fever is very low [43]. People living in
mountain regions reported that mosquito nuisance had started in their communities as recently as
5–10 years ago and increasingly became a problem as mosquito bites started immediately after
winter and lasted until the end of autumn. People in the lowlands reported an elongation of the
mosquito biting seasons. Participants from highland areas believed that mosquitoes had been
carried to the highlands by trucks and buses and that growing mosquito populations breeding in
the highlands had been favored by the installation of water supply pipes in communities,
domestic water storage and warming temperatures in the last years [25]. They also believed that
the replacement of biomass solid fuel by electricity promoted mosquito populations in
households because electric lights attract mosquitoes whereas smoke from kerosene lamps and
biomass fuels repels mosquitoes. In summary, community people perceived the occurrence and
distribution of mosquitoes in their mountain regions to be a recent event which coincided with
development and environmental changes including pronounced temperature increases in the
latest decade. These reported perceptions are consistent with entomological findings [25,44].
Key publications of our international collaborative study:
1. Dhimal M, Ahrens B, Kuch U (2015) Climate change and spatiotemporal
distribution of vector-borne diseases in Nepal - a systematic review of literature.
PLoS ONE, 10(6):e0129869. doi:10.1371/journal.pone.0129869
2. Dhimal M, Gautam I, Joshi HD, O’Hara RB, Ahrens B, Kuch U (2015) Risk factors
for the presence of chikungunya and dengue virus vectors (Aedes aegypti and Aedes
albopictus), their altitudinal distribution and climatic determinants of their abundance
in central Nepal. PLoS Neglected Tropical Diseases, 9(3):e0003545.
doi:10.1371/journal.pntd.0003545
3. Dhimal M, Ahrens B, Kuch U (2014) Species composition, seasonal occurrence, habitat
preference and altitudinal distribution of malaria and other disease vectors in eastern
Nepal. Parasites and Vectors, 7:540. doi:10.1186/s13071-014-0540-4
4. Dhimal M, O’Hara RB, Karki RC, Thakur GD, Kuch U, Ahrens B (2014)
Spatiotemporal distribution of malaria and its association with climatic factors and
vector control interventions in two high-risk districts of Nepal. Malaria Journal, 13:457.
doi:10.1186/1475-2875-13-457
5. Dhimal M, Ahrens B, Kuch U (2014) Altitudinal shift of malaria vectors and malaria
elimination in Nepal. Malaria Journal, 13 (Suppl.):P26. doi:10.1186/1475-2875-13-S1-
P26
6. Dhimal M, Ahrens B, Kuch U (2014) Malaria control in Nepal 1963-2012: challenges
on the path towards elimination. Malaria Journal, 13:241. doi:10.1186/1475-2875-13-
241
7. Dhimal M, Gautam I, Kreß A, Müller R, Kuch U (2014) Spatio-temporal distribution of
dengue and lymphatic filariasis vectors along an altitudinal transect in central Nepal.
PLoS Neglected Tropical Diseases, 8(7):e3035. doi:10.1371/journal.pntd.0003035
8. Dhimal M Aryal KK, Lamichhane Dhimal M, Gautam I, Singh SP, Bhusal CL, Kuch
U (2014) Knowledge, attitude and practice regarding dengue fever among the healthy
population of highland and lowland communities in central Nepal. PLoS ONE,
9(7):e102028. doi:10.1371/journal.pone.0102028
The available data indicate that the warming trend of the HKH region is more pronounced than
that of other parts of the world [2,24]. Climate change, alongside landscape change and
population dynamics is resulting in dramatic environmental changes in the HKH region [1]. This
drives a shift of disease vectors and disease transmission from tropical regions into temperate
regions and highlands, as has been predicted for both observed and future climate change
scenarios [45-48]. It has also been reported that the increasing movement of people and imported
cases of infection, in the presence of appropriate weather conditions, can initiate epidemics of
VBDs [49,50]. Hence, these factors along with the documented establishment of relevant vectors
at altitudes of at least 2,000 m above sea level can intensify the risk of VBD epidemics in the
fragile and previously non-endemic areas of HKH region and its vulnerable populations. The
wide distribution of important disease vectors in regions that had previously been considered to
be non-endemic calls for regional collaboration in extending and upscaling VBD surveillance
and control programs in the HKH region.
Challenges faced while conducting study
Multiple challenges exist for conducting research on climate change and health in the mountain
regions of developing countries [51]. As a result, research continues to focus on the effects of
climate change in developed countries, whereas effects on the most vulnerable populations
residing in least developed and developing countries are grossly underreported [3,4]. The Fourth
Assessment Report of the IPCC [4] categorized the Himalayan region as a "white spot" and
called for global, regional and national responses to fill this gap. In order to study the early
effects of climate change on the spatiotemporal distributions of VBDs, environmental and
climatic data are needed at finer resolution. However, the application of the general circulation
model (GCM) and regional climate model (RCM) data for disease mapping in complex mountain
topography is difficult owing to the spatially clustering nature of diseases and high micro-
climatic variation within short airline distances. Despite the presently low coverage of
meteorological stations in mountain regions, utilizing observed meteorological data provides
more reliable information for exploring the relationships between climatic variables and VBD
transmission.
Hence, we chose an altitudinal transect where meteorological stations were installed for our
study purposes. As the use of CO2 as an attractant for mosquito collection is difficult to
implement in remote mountain regions because of logistic and economic reasons, we collected
mosquitoes with CDC light traps without the use of CO2, and with BG-Sentinel traps using a
specific attractant (BG-Lure) designed for A. aegypti and A. albopictus mosquitoes. Medical
entomology data for mapping vector distributions was completely lacking after the 1990s in
Nepal except for a few studies of dengue virus vectors. Thus, we also collected qualitative data
using interview techniques. Epidemiological data are limited in mountain regions, hence
studying the effects of climate on vectors is of interest because such studies can detect responses
in vector populations before they cause disease and avoid confounding factors such as changes in
diagnosis and treatment regimens or public awareness of the prevention and control of diseases
[19]. In addition, entomological transect surveys along an altitudinal gradient can provide direct
evidence of the distributional shifts of disease vectors in response to climate change.
Planned Next Steps
We propose to extend such integrative, comparative and interdisciplinary entomological-
epidemiological surveys on a broad range of climate change related aspects of VBDs and their
vectors to additional areas in the HKH region where uncertainties for the altitudinal distribution
of mosquitoes, sand flies and the pathogens they transmit have remained high, and to put the
obtained results in a global context by comparing the climate change and health development of
the HKH region with that of the Andes as another major mountain region with a high diversity
and burden of VBDs. This study will also include analyses of the positive and negative effects
that climate change adaptation in other sectors has on VBD transmission, and address possible
mitigating measures.
References
1. Singh SP, Bassignana-Khadka I, Karky BS, Sharma E (2011) Climate change in the Hindu Kush-
Himalayas: The state of current knowledge. Kathmandu: International Centre for Integrated
Mountain Development (ICIMOD).
2. Shrestha UB, Gautam S, Bawa KS (2012) Widespread climate change in the Himalayas and associated
changes in local ecosystems. PLoS One 7: e36741.
3. Confalonieri U, Menne B, Akhtar R, Ebi KL, Hauengue M, et al. (2007) Human Health In: Parry ML,
Canziani OF, Palutikof JP, van der Linden PJ, Hanson CE, editors. Climate Change 2007: Impacts,
Adaptation and Vulnerability Contribution of Working Group II to the Fourth Assessment Report
of the Intergovernmental Panel on Climate Change. Cambridge, UK: Cambridge University Press.
pp. 391-431.
4. IPCC ( 2014) Climate Change 2014: Impacts, Adaptation, and Vulnerability. Part A: Global and Sectoral
Aspects. Contribution of Working Group II to the Fifth Assessment Report of the
Intergovernmental Panel on Climate Change. United Kingdom and New York, NY, USA. 1-32 p.
5. Tabachnick WJ (2010) Challenges in predicting climate and environmental effects on vector-borne
disease episystems in a changing world. J Exp Biol 213: 946-954.
6. Mills JN, Gage KL, Khan AS (2010) Potential influence of climate change on vector-borne and zoonotic
diseases: a review and proposed research plan. Environ Health Perspect 118: 1507-1514.
7. Sutherst RW (2004) Global change and human vulnerability to vector-borne diseases. Clin Microbiol
Rev 17: 136-173.
8. Dhimal M (2015) Effects of climatic and non-climatic factors on the spatiotemporal distributions of
vector-borne diseases in Nepal [Unpublished PhD disseration ]. Frankfurt am Main, Germany
Goethe Univeristy 270 p.
9. WHO (2014) A global brief on vector-borne diseases. Geneva: World Health Organization
10. Campbell-Lendrum D, Manga L, Bagayoko M, Sommerfeld J (2015) Climate change and vector-borne
diseases: what are the implications for public health research and policy? Philos Trans R Soc
Lond B Biol Sci 370.
11. Dhiman RC, Pahwa S, Dhillon GP, Dash AP (2010) Climate change and threat of vector-borne diseases
in India: are we prepared? Parasitol Res 106: 763-773.
12. Gage KL, Burkot TR, Eisen RJ, Hayes EB (2008) Climate and vectorborne diseases. Am J Prev Med 35:
436-450.
13. Rueda LM, Patel KJ, Axtell RC, Stinner RE (1990) Temperature-dependent development and survival
rates of Culex quinquefasciatus and Aedes aegypti (Diptera: Culicidae). J Med Entomol 27: 892-
898.
14. Githeko AK, Lindsay SW, Confalonieri UE, Patz JA (2000) Climate change and vector-borne diseases: a
regional analysis. Bull World Health Organ 78: 1136-1147.
15. Watts DM, Burke DS, Harrison BA, Whitmire RE, Nisalak A (1987) Effect of temperature on the vector
efficiency of Aedes aegypti for dengue 2 virus. Am J Trop Med Hyg 36: 143-152.
16. IPCC (2013) Climate Change 2013. The Physical Science Basis. Working Group I Contribution to the
Fifth Assessment Report of the Intergovernmental Panel on Climate Change-Abstract for
decision-makers. Cambridge, United Kingdom and New York, NY, USA.
17. IPCC (2007) Climate Change 2007: The Physical Science Basis. Contribution of Working Group I to the
Fourth Assessment Report of the Intergovernmental Panel on Climate Change; [Solomon S, Qin
D, Manning M, Chen Z, Marquis M et al., editors. United Kingdom and New York, NY, USA:
Cambridge University Press. 996 p.
18. Epstein P (2010) The ecology of climate change and infectious diseases: comment. Ecology 91: 925-
928; discussion 928-929.
19. Kovats RS, Campbell-Lendrum DH, McMichael AJ, Woodward A, Cox JS (2001) Early effects of climate
change: do they include changes in vector-borne disease? Philos Trans R Soc Lond B Biol Sci 356:
1057-1068.
20. Sternberg ED, Thomas MB (2014) Local adaptation to temperature and the implications for vector-
borne diseases. Trends Parasitol 30: 115-122.
21. Dhimal M, Ahrens B, Kuch U (2015) Climate change and spatiotemporal distributions of vector-borne
diseases in Nepal--A Systematic Synthesis of Literature. PLoS One 10: e0129869.
22. Shrestha AB, Aryal R (2011) Climate change in Nepal and its impact on Himalayan glaciers. Reg
Environ Change 11: S65-S77.
23. Shrestha AB, Wake CP, Mayewski PA, Dibb JE (1999) Maximum temperature trends in the Himalaya
and its vicinity: An analysis based on temperature records from Nepal for the period 1971-94. J
Climate 12: 2775-2786.
24. Kulkarni A, Patwardhan S, Kumar KK, Ashok K, Krishnan R (2013) Projected climate change in the
Hindu Kush-Himalayan region by using the high-resolution regional climate model PRECIS. Mt
Res Dev 33: 142-151.
25. Dhimal M, Ahrens B, Kuch U (2014) Species composition, seasonal occurrence, habitat preference
and altitudinal distribution of malaria and other disease vectors in eastern Nepal. Parasit Vectors
7: 540.
26. Dhimal M, Gautam I, Joshi HD, O'Hara RB, Ahrens B, et al. (2015) Risk factors for the presence of
chikungunya and dengue vectors (Aedes aegypti and Aedes albopictus), their altitudinal
distribution and climatic determinants of their abundance in central Nepal. PLoS Negl Trop Dis 9:
e0003545.
27. Dhimal M, Gautam I, Baral G, Pandey B, Karki KB (2015) Zika Virus: yet another emerging threat to
Nepal. J Nepal Health Res Counc 13: 248-251.
28. Dhimal M, Gautam I, Kress A, Muller R, Kuch U (2014) Spatio-temporal distribution of dengue and
lymphatic filariasis vectors along an altitudinal transect in Central Nepal. PLoS Negl Trop Dis 8:
e3035.
29. Dorji T, Yoon IK, Holmes EC, Wangchuk S, Tobgay T, et al. (2009) Diversity and origin of dengue virus
serotypes 1, 2, and 3, Bhutan. Emerg Infect Dis 15: 1630-1632.
30. Malla S, Thakur GD, Shrestha SK, Banjeree MK, Thapa LB, et al. (2008) Identification of all dengue
serotypes in Nepal. Emerg Infect Dis 14: 1669-1670.
31. Aditya G, Pramanik MK, Saha GK (2009) Immatures of Aedes aegypti in Darjeeling Himalayas--
expanding geographical limits in India. Indian J Med Res 129: 455-457.
32. Dhimal M, Ahrens B, Kuch U (2014) Species composition, seasonal occurrence, habitat preference
and altitudinal distribution of malaria and other disease vectors in eastern Nepal. Parasit Vectors
7: 540.
33. Pun SB, Bastola A, Shah R (2014) First report of Chikungunya virus infection in Nepal. J Infect Dev
Ctries 8: 790-792.
34. Wangchuk S, Chinnawirotpisan P, Dorji T, Tobgay T, Dorji T, et al. (2013) Chikungunya fever
outbreak, Bhutan, 2012. Emerg Infect Dis 19: 1681-1684.
35. Baylis M, Barker CM, Caminade C, Joshi BR, Pant GR, et al. (2016) Emergence or improved detection
of Japanese encephalitis virus in the Himalayan highlands? Trans R Soc Trop Med Hyg 110: 209-
211.
36. Li YX, Li MH, Fu SH, Chen WX, Liu QY, et al. (2011) Japanese encephalitis, Tibet, China. Emerg Infect
Dis 17: 934-936.
37. Bhattachan A, Amatya S, Sedai TR, Upreti SR, Partridge J (2009) Japanese encephalitis in hill and
mountain districts, Nepal. Emerg Infect Dis 15: 1691-1692.
38. Dhimal M, Ahrens B, Kuch U (2014) Malaria control in Nepal 1963-2012: challenges on the path
towards elimination. Malar J 13: 241.
39. Dhimal M, O'Hara RB, Karki R, Thakur GD, Kuch U, et al. (2014) Spatio-temporal distribution of
malaria and its association with climatic factors and vector-control interventions in two high-risk
districts of Nepal. Malar J 13: 457.
40. Mishra SR, Dhimal M, Guinto RR, Adhikari B, Chu C (2016) Threats to malaria elimination in the
Himalayas. Lancet Glob Health 4: e519.
41. Ostyn B, Uranw S, Bhattarai NR, Das ML, Rai K, et al. (2015) Transmission of Leishmania donovani in
the Hills of Eastern Nepal, an Outbreak Investigation in Okhaldhunga and Bhojpur Districts. PLoS
Negl Trop Dis 9: e0003966.
42. Dhimal M, Karki KB (2014) The hidden burden of Neglected Tropical Diseases: a call for inter-sectoral
collaboration in Nepal. J Nepal Health Res Counc 12: I-IV.
43. Dhimal M, Aryal KK, Dhimal ML, Gautam I, Singh SP, et al. (2014) Knowledge, attitude and practice
regarding dengue fever among the healthy population of highland and lowland communities in
central Nepal. PLoS One 9: e102028.
44. Chaudhary P, Bawa KS (2011) Local perceptions of climate change validated by scientific evidence in
the Himalayas. Biol Lett 7: 767-770.
45. Liu-Helmersson J, Stenlund H, Wilder-Smith A, Rocklov J (2014) Vectorial capacity of Aedes aegypti:
effects of temperature and implications for global dengue epidemic potential. PLoS One 9:
e89783.
46. Siraj AS, Santos-Vega M, Bouma MJ, Yadeta D, Ruiz Carrascal D, et al. (2014) Altitudinal changes in
malaria incidence in highlands of Ethiopia and Colombia. Science 343: 1154-1158.
47. Caminade C, Kovats S, Rocklov J, Tompkins AM, Morse AP, et al. (2014) Impact of climate change on
global malaria distribution. Proc Natl Acad Sci U S A 111: 3286-3291.
48. Chen IC, Hill JK, Ohlemuller R, Roy DB, Thomas CD (2011) Rapid range shifts of species associated
with high levels of climate warming. Science 333: 1024-1026.
49. Stoddard ST, Morrison AC, Vazquez-Prokopec GM, Paz Soldan V, Kochel TJ, et al. (2009) The role of
human movement in the transmission of vector-borne pathogens. PLoS Negl Trop Dis 3: e481.
50. Shang CS, Fang CT, Liu CM, Wen TH, Tsai KH, et al. (2010) The role of imported cases and favorable
meteorological conditions in the onset of dengue epidemics. PLoS Negl Trop Dis 4: e775.
51. Dhimal M (2008) Climate Change and health:research challenges in vulnerable mountaoinous
countries like Nepal Global Forum for Health Research, Young Voices in Research for Health.
Switzerland The Global Forum for Health Research and the Lancet pp. 66-69.