Skip to main content
Top
Published in: Malaria Journal 1/2018

Open Access 01-12-2018 | Research

Microclimate variables of the ambient environment deliver the actual estimates of the extrinsic incubation period of Plasmodium vivax and Plasmodium falciparum: a study from a malaria-endemic urban setting, Chennai in India

Authors: Shalu Thomas, Sangamithra Ravishankaran, N. A. Johnson Amala Justin, Aswin Asokan, T. Maria Jusler Kalsingh, Manu Thomas Mathai, Neena Valecha, Jacqui Montgomery, Matthew B. Thomas, Alex Eapen

Published in: Malaria Journal | Issue 1/2018

Login to get access

Abstract

Background

Environmental factors such as temperature, relative humidity and their daily variation influence a range of mosquito life history traits and hence, malaria transmission. The standard way of characterizing environmental factors with meteorological station data need not be the actual microclimates experienced by mosquitoes within local transmission settings.

Methods

A year-long study was conducted in Chennai, India to characterize local temperature and relative humidity (RH). Data loggers (Hobos) were placed in a range of probable indoor and outdoor resting sites of Anopheles stephensi. Recordings were taken hourly to estimate mean temperature and RH, together with daily temperature range (DTR) and daily relative humidity range. The temperature data were used to explore the predicted variation in extrinsic incubation period (EIP) of Plasmodium falciparum and Plasmodium vivax between microhabitats and across the year.

Results

Mean daily temperatures within the indoor settings were significantly warmer than those recorded outdoors. DTR in indoor environments was observed to be modest and ranged from 2 to 6 °C. Differences in EIP between microhabitats were most notable during the hottest summer months of April–June, with parasite development predicted to be impaired for tiled houses and overhead tanks. Overall, the prevailing warm and stable conditions suggest rapid parasite development rate regardless of where mosquitoes might rest. Taking account of seasonal and local environmental variation, the predicted EIP of P. falciparum varied from a minimum of 9.1 days to a maximum of 15.3 days, while the EIP of P. vivax varied from 8.0 to 24.3 days.

Conclusions

This study provides a detailed picture of the actual microclimates experienced by mosquitoes in an urban slum malaria setting. The data indicate differences between microhabitats that could impact mosquito and parasite life history traits. The predicted effects for EIP are often relatively subtle, but variation between minimum and maximum EIPs can play a role in disease transmission, depending on the time of year and where mosquitoes rest. Appropriate characterization of the local microclimate conditions would be the key to fully understand the effects of environment on local transmission ecology.
Appendix
Available only for authorised users
Literature
2.
go back to reference Caminade C, Kovats S, Rocklov J, Tompkins AM, Morse AP, Colón-González FJ, et al. Impact of climate change on global malaria distribution. Proc Natl Acad Sci USA. 2014;111:3286–91.CrossRefPubMedPubMedCentral Caminade C, Kovats S, Rocklov J, Tompkins AM, Morse AP, Colón-González FJ, et al. Impact of climate change on global malaria distribution. Proc Natl Acad Sci USA. 2014;111:3286–91.CrossRefPubMedPubMedCentral
3.
go back to reference Zomuanpuii R, Guruswami G, Nachimuthu SK. A 3 year study on distribution and ecology of Anophelines in Thenzawl, Mizoram, India. J Environ Biol. 2014;35:369–76.PubMed Zomuanpuii R, Guruswami G, Nachimuthu SK. A 3 year study on distribution and ecology of Anophelines in Thenzawl, Mizoram, India. J Environ Biol. 2014;35:369–76.PubMed
4.
go back to reference An G. Influence of climate on malaria in China. Penn McNair Res J. 2011;3:1. An G. Influence of climate on malaria in China. Penn McNair Res J. 2011;3:1.
5.
go back to reference Grover-Kopec EK, Blumenthal MB, Ceccato P, Dinku T, Omumbo JA, Connor SJ. Web-based climate information resources for malaria control in Africa. Malar J. 2006;5:38.CrossRefPubMedPubMedCentral Grover-Kopec EK, Blumenthal MB, Ceccato P, Dinku T, Omumbo JA, Connor SJ. Web-based climate information resources for malaria control in Africa. Malar J. 2006;5:38.CrossRefPubMedPubMedCentral
6.
go back to reference Ngarakana-Gwasira ET, Bhunu CP, Masocha M, Mashonjowa E. Assessing the role of climate change in malaria transmission in Africa. Malar Res Treat. 2016;2016:7104291.PubMedPubMedCentral Ngarakana-Gwasira ET, Bhunu CP, Masocha M, Mashonjowa E. Assessing the role of climate change in malaria transmission in Africa. Malar Res Treat. 2016;2016:7104291.PubMedPubMedCentral
9.
go back to reference Cator LJ, Thomas S, Paaijmans KP, Ravishankaran S, Justin JA, Mathai MT, et al. Characterizing microclimate in urban malaria transmission settings: a case study from Chennai, India. Malar J. 2013;12:84.CrossRefPubMedPubMedCentral Cator LJ, Thomas S, Paaijmans KP, Ravishankaran S, Justin JA, Mathai MT, et al. Characterizing microclimate in urban malaria transmission settings: a case study from Chennai, India. Malar J. 2013;12:84.CrossRefPubMedPubMedCentral
11.
go back to reference Paaijmans KP, Imbahale SS, Thomas MB, Takken W. Relevant microclimate for determining the development rate of malaria mosquitoes and possible implications of climate change. Malar J. 2010;9:196.CrossRefPubMedPubMedCentral Paaijmans KP, Imbahale SS, Thomas MB, Takken W. Relevant microclimate for determining the development rate of malaria mosquitoes and possible implications of climate change. Malar J. 2010;9:196.CrossRefPubMedPubMedCentral
13.
go back to reference Nagpal BN, Srivastava A, Dash AP. Resting behaviour of Anopheles stephensi type form to assess its amenability to control malaria through indoor residual spray. J Vector Borne Dis. 2012;49:175–80.PubMed Nagpal BN, Srivastava A, Dash AP. Resting behaviour of Anopheles stephensi type form to assess its amenability to control malaria through indoor residual spray. J Vector Borne Dis. 2012;49:175–80.PubMed
14.
go back to reference Hati AK, Chatterjee KK, Biswas D. Daytime resting habits of Anopheles stephensi in an area of Calcutta. Indian J Malariol. 1987;24:85–7.PubMed Hati AK, Chatterjee KK, Biswas D. Daytime resting habits of Anopheles stephensi in an area of Calcutta. Indian J Malariol. 1987;24:85–7.PubMed
15.
go back to reference Hati AK, Chatterjee KK, Biswas DE, Mukhopadhyay AK, Saha DI. A newly discovered habitat of Anopheles stephensi in present-day Calcutta with evidence of natural malarial infection. Trop Geogr Med. 1988;40:376–7.PubMed Hati AK, Chatterjee KK, Biswas DE, Mukhopadhyay AK, Saha DI. A newly discovered habitat of Anopheles stephensi in present-day Calcutta with evidence of natural malarial infection. Trop Geogr Med. 1988;40:376–7.PubMed
16.
go back to reference Batra CP, Reuben R, Das PK. Studies of day-time resting places of Anopheles stephensi Liston in Salem (Tamil Nadu). Indian J Med Res. 1979;69:583–8.PubMed Batra CP, Reuben R, Das PK. Studies of day-time resting places of Anopheles stephensi Liston in Salem (Tamil Nadu). Indian J Med Res. 1979;69:583–8.PubMed
17.
go back to reference Beck-Johnson LM, Nelson WA, Paaijmans KP, Read AF, Thomas MB, Bjørnstad ON. The importance of temperature fluctuations in understanding mosquito population dynamics and malaria risk. R Soc Open Sci. 2017;4:160969.CrossRefPubMedPubMedCentral Beck-Johnson LM, Nelson WA, Paaijmans KP, Read AF, Thomas MB, Bjørnstad ON. The importance of temperature fluctuations in understanding mosquito population dynamics and malaria risk. R Soc Open Sci. 2017;4:160969.CrossRefPubMedPubMedCentral
18.
go back to reference Singh P, Yadav Y, Saraswat S, Dhiman RC. Intricacies of using temperature of different niches for assessing impact on malaria transmission. Indian J Med Res. 2016;144:67–75.CrossRefPubMedPubMedCentral Singh P, Yadav Y, Saraswat S, Dhiman RC. Intricacies of using temperature of different niches for assessing impact on malaria transmission. Indian J Med Res. 2016;144:67–75.CrossRefPubMedPubMedCentral
19.
go back to reference Mordecai EA, Paaijmans KP, Johnson LR, Balzer C, Ben-Horin T, Moor E, et al. Optimal temperature for malaria transmission is dramatically lower than previously predicted. Ecol Lett. 2013;16:22–30.CrossRefPubMed Mordecai EA, Paaijmans KP, Johnson LR, Balzer C, Ben-Horin T, Moor E, et al. Optimal temperature for malaria transmission is dramatically lower than previously predicted. Ecol Lett. 2013;16:22–30.CrossRefPubMed
20.
21.
go back to reference Nguyen JL, Schwartz J, Dockery DW. The relationship between indoor and outdoor temperature, apparent temperature, relative humidity and absolute humidity. Indoor Air. 2014;24:103–12.CrossRefPubMed Nguyen JL, Schwartz J, Dockery DW. The relationship between indoor and outdoor temperature, apparent temperature, relative humidity and absolute humidity. Indoor Air. 2014;24:103–12.CrossRefPubMed
22.
go back to reference Thomas S, Ravishankaran S, Justin NJ, Asokan A, Mathai MT, Valecha N, et al. Resting and feeding preferences of Anopheles stephensi in an urban setting, perennial for malaria. Malar J. 2017;16:111.CrossRefPubMedPubMedCentral Thomas S, Ravishankaran S, Justin NJ, Asokan A, Mathai MT, Valecha N, et al. Resting and feeding preferences of Anopheles stephensi in an urban setting, perennial for malaria. Malar J. 2017;16:111.CrossRefPubMedPubMedCentral
23.
go back to reference Rozendaal JA. Vector control: methods for use by individuals and communities. Geneva: World Health Organization; 1997. Rozendaal JA. Vector control: methods for use by individuals and communities. Geneva: World Health Organization; 1997.
24.
go back to reference Blanford JI, Blanford S, Crane RG, Mann ME, Paaijmans KP, Schreiber KV, et al. Implications of temperature variation for malaria parasite development across Africa. Sci Rep. 2013;3:1300.CrossRefPubMedPubMedCentral Blanford JI, Blanford S, Crane RG, Mann ME, Paaijmans KP, Schreiber KV, et al. Implications of temperature variation for malaria parasite development across Africa. Sci Rep. 2013;3:1300.CrossRefPubMedPubMedCentral
25.
go back to reference Beck-Johnson LM, Nelson WA, Paaijmans KP, Read AF, Thomas MB, Bjørnstad ON. The effect of temperature on Anopheles mosquito population dynamics and the potential for malaria transmission. PLoS ONE. 2013;8:e79276.CrossRefPubMedPubMedCentral Beck-Johnson LM, Nelson WA, Paaijmans KP, Read AF, Thomas MB, Bjørnstad ON. The effect of temperature on Anopheles mosquito population dynamics and the potential for malaria transmission. PLoS ONE. 2013;8:e79276.CrossRefPubMedPubMedCentral
26.
go back to reference Paaijmans KP, Blanford S, Bell AS, Blanford JI, Read AF, Thomas MB. Influence of climate on malaria transmission depends on daily temperature variation. Proc Natl Acad Sci USA. 2010;107:15135–9.CrossRefPubMedPubMedCentral Paaijmans KP, Blanford S, Bell AS, Blanford JI, Read AF, Thomas MB. Influence of climate on malaria transmission depends on daily temperature variation. Proc Natl Acad Sci USA. 2010;107:15135–9.CrossRefPubMedPubMedCentral
27.
go back to reference Garnham PC. Malaria parasites and other haemosporidia. Malar Parasit Other Haemosporidia. 1966;18:1114. Garnham PC. Malaria parasites and other haemosporidia. Malar Parasit Other Haemosporidia. 1966;18:1114.
28.
go back to reference Thomas S, Ravishankaran S, Justin JA, Asokan A, Mathai MT, Valecha N, et al. Overhead tank is the potential breeding habitat of Anopheles stephensi in an urban transmission setting of Chennai, India. Malar J. 2016;15:274.CrossRefPubMedPubMedCentral Thomas S, Ravishankaran S, Justin JA, Asokan A, Mathai MT, Valecha N, et al. Overhead tank is the potential breeding habitat of Anopheles stephensi in an urban transmission setting of Chennai, India. Malar J. 2016;15:274.CrossRefPubMedPubMedCentral
29.
go back to reference Glunt KD, Paaijmans KP, Read AF, Thomas MB. Environmental temperatures significantly change the impact of insecticides measured using WHOPES protocols. Malar J. 2014;13:350.CrossRefPubMedPubMedCentral Glunt KD, Paaijmans KP, Read AF, Thomas MB. Environmental temperatures significantly change the impact of insecticides measured using WHOPES protocols. Malar J. 2014;13:350.CrossRefPubMedPubMedCentral
30.
go back to reference Hodjati MH, Curtis CF. Effects of permethrin at different temperatures on pyrethroid-resistant and susceptible strains of Anopheles. Med Vet Entomol. 1999;13:415–22.CrossRefPubMed Hodjati MH, Curtis CF. Effects of permethrin at different temperatures on pyrethroid-resistant and susceptible strains of Anopheles. Med Vet Entomol. 1999;13:415–22.CrossRefPubMed
31.
go back to reference de Barros FS, Honorio NA, Arruda ME. Survivorship of Anopheles darlingi (Diptera: Culicidae) in relation with malaria incidence in the Brazilian Amazon. PLoS ONE. 2011;6:e22388.CrossRefPubMedPubMedCentral de Barros FS, Honorio NA, Arruda ME. Survivorship of Anopheles darlingi (Diptera: Culicidae) in relation with malaria incidence in the Brazilian Amazon. PLoS ONE. 2011;6:e22388.CrossRefPubMedPubMedCentral
32.
go back to reference Alemu A, Abebe G, Tsegaye W, Golassa L. Climatic variables and malaria transmission dynamics in Jimma town, South West Ethiopia. Parasit Vectors. 2011;4:30.CrossRefPubMedPubMedCentral Alemu A, Abebe G, Tsegaye W, Golassa L. Climatic variables and malaria transmission dynamics in Jimma town, South West Ethiopia. Parasit Vectors. 2011;4:30.CrossRefPubMedPubMedCentral
33.
go back to reference Mutheneni SR, Morse AP, Caminade C, Upadhyayula SM. Dengue burden in India: recent trends and importance of climatic parameters. Emerg Microbes Infect. 2017;6:e70.CrossRefPubMedPubMedCentral Mutheneni SR, Morse AP, Caminade C, Upadhyayula SM. Dengue burden in India: recent trends and importance of climatic parameters. Emerg Microbes Infect. 2017;6:e70.CrossRefPubMedPubMedCentral
Metadata
Title
Microclimate variables of the ambient environment deliver the actual estimates of the extrinsic incubation period of Plasmodium vivax and Plasmodium falciparum: a study from a malaria-endemic urban setting, Chennai in India
Authors
Shalu Thomas
Sangamithra Ravishankaran
N. A. Johnson Amala Justin
Aswin Asokan
T. Maria Jusler Kalsingh
Manu Thomas Mathai
Neena Valecha
Jacqui Montgomery
Matthew B. Thomas
Alex Eapen
Publication date
01-12-2018
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2018
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/s12936-018-2342-1

Other articles of this Issue 1/2018

Malaria Journal 1/2018 Go to the issue