- ABSTRACT.
- INTRODUCTION
- MATERIALS AND METHODS
- Study site.
- Collection and culture of An. stephensi.
- Collection of P. vivax-infected blood from malaria patients.
- Microscopic and molecular detection of malaria parasites.
- Microclimate (temperature and RH) data of various roof types.
- Standard membrane feeding assay (SMFA) experiments with An. stephensi.
- Simulation of microclimate (temperature and RH) conditions of the roof types in Percival biological incubators.
- Midgut and salivary gland dissection of An. stephensi mosquitoes.
- Sporozoite detection in An. stephensi mosquitoes by CS-ELISA method.
- STATISTICAL ANALYSES
- RESULTS
- Parasite density and membrane feeding experiments of An. stephensi.
- Oocyst and sporozoite detection by dissection methods.
- Sporozoite detection by CS-ELISA and estimation of EIP.
- Statistical analysis of oocyst parameters.
- Univariate and multivariate regression models for exploring the factors influencing P. vivax development in An. stephensi.
- Univariate and multivariate regression models for exploring the factors influencing oocyst parameters.
- Survival of P. vivax-infected An. stephensi in simulated/real-time microclimatic conditions of different roof types.
- DISCUSSION
- Supplemental Materials
- ACKNOWLEDGMENTS
- REFERENCES
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
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Thomas S, Ravishankaran S, Justin JA, Asokan A, Mathai MT, Valecha N, Thomas MB, Eapen A, 2016. Overhead tank is the potential breeding habitat of Anopheles stephensi in an urban transmission setting of Chennai, India. Malar J 15: 274.
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Thomas S, Ravishankaran S, Asokan A, Johnson Amala Justin NA, Maria Jusler Kalsingh TMJ, Mathai MT, Valecha N, Eapen A, 2018. Socio-demographic and household attributes may not necessarily influence malaria: Evidence from a cross-sectional study of households in an urban slum setting of Chennai, India. Malar J 17: 4.
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Cator LJ, Thomas S, Paaijmans KP, Ravishankaran S, Justin JA, Mathai MT, Read AF, Thomas MB, Eapen A, 2013. Characterizing microclimate in urban malaria transmission settings: A case study from Chennai, India. Malar J 12: 84.
-
17.
Thomas S, Ravishankaran S, Justin NJA, Asokan A, Kalsingh TMJ, Mathai MT, Valecha N, Montgomery J, Thomas MB, Eapen A, 2018. 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. Malar J 17: 201.
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Ravishankaran S, Asokan A, Justin NA, Thomas S, Joshua V, Mathai MT, Eapen A, 2022. Does the roof type of a house influence the presence of adult Anopheles stephensi, urban malaria vector?—Evidence from a few slum settings in Chennai, India. Parasitol Res 121: 105–114.
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Kumari S, De TD, Chauhan CRJ, Tevatiya S, Sharma P, Pandey KC, Pande V, Dixit R, 2020. Salivary AsHPX12 influence pre-blood meal associated behavioral properties in the mosquito Anopheles stephensi. bioRxiv doi.org/10.1101/2020.06.12.147959.
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Kumari S et al., 2021. Genetic changes of Plasmodium vivax tempers host tissue-specific responses in Anopheles stephensi. Curr Res Immunol 2: 12–22.
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Sharma P, Rani J, Chauhan C, Kumari S, Tevatiya S, Das De T, Savargaonkar D, Pandey KC, Dixit R, 2020. Altered gut microbiota and immunity defines Plasmodium vivax survival in Anopheles stephensi. Front Immunol 11: 609.
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Shumbej T, Jemal A, Worku A, Bekele F, Weldesenbet H, 2019. Therapeutic efficacy of chloroquine for treatment of Plasmodium vivax malaria cases in Guragae zone southern Central Ethiopia. BMC Infect Dis 19: 413–416.
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Influence of Household Roof Types on the Development of Plasmodium vivax in Anopheles stephensi Mosquitoes
Sangamithra Ravishankaran
Sangamithra Ravishankaran
ICMR–National Institute of Malaria Research, Field Unit, Chennai, India;
Madras Christian College, Chennai, India;
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Madras Christian College, Chennai, India;
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Aswin Asokan
Aswin Asokan
ICMR–National Institute of Malaria Research, Field Unit, Chennai, India;
Academy of Scientific and Innovative Research (AcSIR), Ghaziabad, India;
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Academy of Scientific and Innovative Research (AcSIR), Ghaziabad, India;
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N. A. Johnson Amala Justin
N. A. Johnson Amala Justin
ICMR–National Institute of Malaria Research, Field Unit, Chennai, India;
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Janani Surya R
Janani Surya R
ICMR–National Institute of Epidemiology, Chennai, India
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Manu Thomas Mathai
Manu Thomas Mathai
Madras Christian College, Chennai, India;
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Alex Eapen
alexeapen@yahoo.com
Alex Eapen
ICMR–National Institute of Malaria Research, Field Unit, Chennai, India;
Academy of Scientific and Innovative Research (AcSIR), Ghaziabad, India;
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Academy of Scientific and Innovative Research (AcSIR), Ghaziabad, India;
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ABSTRACT.
Urbanization and microclimate variation in cities can influence mosquito behavior and parasite development, thus affecting malaria transmission. This study investigates how the impact of microclimate variations due to household roof types can aid in the survival of Anopheles stephensi and the development of Plasmodium vivax in an urban slum setting. Understanding these vital environmental interactions is essential for devising effective control strategies to achieve malaria elimination. Anopheles stephensi (F1) mosquitoes were membrane-fed with blood collected from P. vivax-infected patients before (day 0) and during (day 1) antimalarial treatment. The parasite development and mosquito survival were monitored in simulated microclimatic conditions of a variety of household roof types (thatched, asbestos, tiled) against standard laboratory conditions. Mosquito dissections were undertaken to detect oocysts and sporozoites in An. stephensi mosquitoes (oocyst: day 3–5, sporozoites: day 7–11). The maximum number of oocysts were detected in infected mosquitoes in thatched-roof conditions, whereas the largest oocyst was in the asbestos roof type. Circumsporozoite-ELISA results indicated the presence of sporozoites in infected mosquitoes for up to 29 days under standard conditions, 18 days in thatched-roof and asbestos roof conditions, and 14 days in tiled conditions. The univariate binary logistic regression model indicated a significant influence of microclimatic conditions of thatched roofs on parasite development. The Kaplan-Meier survival analysis revealed that the median survival of P. vivax-infected An. stephensi in thatched-roof conditions was 14 days, followed by asbestos (11 days) and tiled (10 days) roof conditions. In conclusion, thatched-roof houses were favorable for the development and survival of P. vivax-infected An. stephensi.
- Supplemental Materials (PDF 348.34 KB)
Author Notes
Financial support: This work was supported by the
Disclosures: Institutional ethical clearance of the project was obtained from the National Institute of Malaria Research of the Indian Council of Medical Research, New Delhi (ECR/NIMR/EC/2010/100). Informed consent was obtained from all subjects. All experiments were performed in accordance with the relevant guidelines and regulations.
The content of this manuscript is solely the responsibility of the authors and does not necessarily represent the official views of the NIH.
Current contact information: Sangamithra Ravishankaran, ICMR-National Institute of Malaria Research, Field Unit, Chennai, India, and Madras Christian College, Chennai, India, E-mail: vr.sangamithra@gmail.com. Aswin Asokan and Alex Eapen, ICMR-National Institute of Malaria Research, Field Unit, Chennai, India, and Academy of Scientific and Innovative Research (AcSIR), Ghaziabad, India, E-mails: ashwinviro@gmail.com and alexeapen@yahoo.com. N. A. Johnson Amala Justin, ICMR-National Institute of Malaria Research, Field Unit, Chennai, India, and National Center for Vector Borne Diseases Control, New Delhi, India, E-mail: johnsonamalajustin@gmail.com. Janani Surya R, ICMR-National Institute of Epidemiology, Chennai, India, E-mail: jananisurya92@gmail.com. Manu Thomas Mathai, Madras Christian College, Chennai, India, E-mail: manuthomasmcc@gmail.com.
- ABSTRACT.
- INTRODUCTION
- MATERIALS AND METHODS
- Study site.
- Collection and culture of An. stephensi.
- Collection of P. vivax-infected blood from malaria patients.
- Microscopic and molecular detection of malaria parasites.
- Microclimate (temperature and RH) data of various roof types.
- Standard membrane feeding assay (SMFA) experiments with An. stephensi.
- Simulation of microclimate (temperature and RH) conditions of the roof types in Percival biological incubators.
- Midgut and salivary gland dissection of An. stephensi mosquitoes.
- Sporozoite detection in An. stephensi mosquitoes by CS-ELISA method.
- STATISTICAL ANALYSES
- RESULTS
- Parasite density and membrane feeding experiments of An. stephensi.
- Oocyst and sporozoite detection by dissection methods.
- Sporozoite detection by CS-ELISA and estimation of EIP.
- Statistical analysis of oocyst parameters.
- Univariate and multivariate regression models for exploring the factors influencing P. vivax development in An. stephensi.
- Univariate and multivariate regression models for exploring the factors influencing oocyst parameters.
- Survival of P. vivax-infected An. stephensi in simulated/real-time microclimatic conditions of different roof types.
- DISCUSSION
- Supplemental Materials
- ACKNOWLEDGMENTS
- REFERENCES
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
World Health Organization, 2023. World Malaria Report 2023. Geneva, Switzerland: World Health Organization.
-
2.
Ministry of Health and Family Welfare, Government of India, National Center for Vector Borne Diseases Control. Available at: https://ncvbdc.mohfw.gov.in/index.php. Accessed January 10, 2024.
-
3.
Rahi M, Das P, Sharma A, 2020. COVID-19 mitigation steps provide a blueprint for malaria control and elimination. Am J Trop Med Hyg 103: 28–30.
-
4.
Wilder-Smith A, Tissera H, Ooi EE, Coloma J, Scott TW, Gubler DJ, 2020. Preventing dengue epidemics during the COVID-19 pandemic. Am J Trop Med Hyg 103: 570–571.
-
5.
Hussein MIH, Albashir AAD, Elawad OAMA, Homeida A, 2020. Malaria and COVID-19: Unmasking their ties. Malar J 19: 457.
-
6.
Parham PE et al., 2015. Climate, environmental and socio-economic change: Weighing up the balance in vector-borne disease transmission. Philos Trans R Soc Lond B Biol Sci 370: 20130551.
-
7.
Murdock CC, Sternberg ED, Thomas MB, 2016. Malaria transmission potential could be reduced with current and future climate change. Sci Rep 6: 27771–27777.
-
8.
Bordoloi B, Saharia S, 2021. Mosquito-borne diseases in Assam. Int J Mosq Res 8: 130–133.
-
9.
Ghosh SK, Rahi M, 2019. Malaria elimination in India—The way forward. J Vector Borne Dis 56: 32–40.
-
10.
Ahmad SS, Rahi M, Sharma A, 2021. Relapses of Plasmodium vivax malaria threaten disease elimination: Time to deploy tafenoquine in India? BMJ Glob Health 6: e004558.
-
11.
Wilson ML, Krogstad DJ, Arinaitwe E, Arevalo-Herrera M, Chery L, Ferreira MU, Ndiaye D, Mathanga DP, Eapen A, 2015. Urban malaria: Understanding its epidemiology, ecology, and transmission across seven diverse ICEMR network sites. Am J Trop Med Hyg 93: 110–123.
-
12.
Thomas S, Ravishankaran S, Justin JA, Asokan A, Mathai MT, Valecha N, Thomas MB, Eapen A, 2016. Overhead tank is the potential breeding habitat of Anopheles stephensi in an urban transmission setting of Chennai, India. Malar J 15: 274.
-
13.
Thomas S, Ravishankaran S, Asokan A, Johnson Amala Justin NA, Maria Jusler Kalsingh TMJ, Mathai MT, Valecha N, Eapen A, 2018. Socio-demographic and household attributes may not necessarily influence malaria: Evidence from a cross-sectional study of households in an urban slum setting of Chennai, India. Malar J 17: 4.
-
14.
Alemu A, Tsegaye W, Golassa L, Abebe G, 2011. Urban malaria and associated risk factors in Jimma town, south-west Ethiopia. Malar J 10: 173.
-
15.
Thomas S, Ravishankaran S, Justin NJA, Asokan A, Mathai MT, Valecha N, Montgomery J, Thomas MB, Eapen A, 2017. Resting and feeding preferences of Anopheles stephensi in an urban setting, perennial for malaria. Malar J 16: 111.
-
16.
Cator LJ, Thomas S, Paaijmans KP, Ravishankaran S, Justin JA, Mathai MT, Read AF, Thomas MB, Eapen A, 2013. Characterizing microclimate in urban malaria transmission settings: A case study from Chennai, India. Malar J 12: 84.
-
17.
Thomas S, Ravishankaran S, Justin NJA, Asokan A, Kalsingh TMJ, Mathai MT, Valecha N, Montgomery J, Thomas MB, Eapen A, 2018. 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. Malar J 17: 201.
-
18.
Ciota AT, Matacchiero AC, Kilpatrick AM, Kramer LD, 2014. The effect of temperature on life history traits of Culex mosquitoes. J Med Entomol 51: 55–62.
-
19.
Afrane YA, Zhou G, Lawson BW, Githeko AK, Yan G, 2007. Life-table analysis of Anopheles arabiensis in western Kenya highlands: Effects of land covers on larval and adult survivorship. Am J Trop Med Hyg 77: 660–666.
-
20.
Raghavendra K, Barik TK, Swain V, 2010. Studies on the impact of thermal stress on survival and development of adaptive thermotolerance in immature stages of Anopheles culicifacies. J Ecobiotechnol 2: 25–30.
-
21.
Ravishankaran S, Asokan A, Justin NA, Thomas S, Joshua V, Mathai MT, Eapen A, 2022. Does the roof type of a house influence the presence of adult Anopheles stephensi, urban malaria vector?—Evidence from a few slum settings in Chennai, India. Parasitol Res 121: 105–114.
-
22.
Kumari S, De TD, Chauhan CRJ, Tevatiya S, Sharma P, Pandey KC, Pande V, Dixit R, 2020. Salivary AsHPX12 influence pre-blood meal associated behavioral properties in the mosquito Anopheles stephensi. bioRxiv doi.org/10.1101/2020.06.12.147959.
-
23.
Kumari S et al., 2021. Genetic changes of Plasmodium vivax tempers host tissue-specific responses in Anopheles stephensi. Curr Res Immunol 2: 12–22.
-
24.
Sharma P, Rani J, Chauhan C, Kumari S, Tevatiya S, Das De T, Savargaonkar D, Pandey KC, Dixit R, 2020. Altered gut microbiota and immunity defines Plasmodium vivax survival in Anopheles stephensi. Front Immunol 11: 609.
-
25.
Basseri HR, Doosti S, Akbarzadeh K, Nateghpour M, Whitten M, Ladoni H, 2008. Competency of Anopheles stephensi mysorensis strain for Plasmodium vivax and the role of inhibitory carbohydrates to block its sporogonic cycle. Malar J 7: 131–138.
-
26.
Adak T, Singh OP, Das MK, Wattal S, Nanda N, 2005. Comparative susceptibility of three important malaria vectors Anopheles stephensi, Anopheles fluviatilis, and Anopheles sundaicus to Plasmodium vivax. J Parasitol 91: 79–82.
-
27.
World Health Organization, 2015. Guidelines for the Treatment of Malaria. Geneva, Switzerland: WHO.
-
28.
Baird JK, Valecha N, Duparc S, White NJ, Price RN, 2016. Diagnosis and treatment of Plasmodium vivax malaria. Am J Trop Med Hyg 95: 35–51.
-
29.
Price RN, Von Seidlein L, Valecha N, Nosten F, Baird JK, White NJ, 2014. Global extent of chloroquine-resistant Plasmodium vivax: A systematic review and meta-analysis. Lancet Infect Dis 14: 982–991.
-
30.
Shumbej T, Jemal A, Worku A, Bekele F, Weldesenbet H, 2019. Therapeutic efficacy of chloroquine for treatment of Plasmodium vivax malaria cases in Guragae zone southern Central Ethiopia. BMC Infect Dis 19: 413–416.
-
31.
Xu S et al., 2020. Efficacy of directly-observed chloroquine-primaquine treatment for uncomplicated acute Plasmodium vivax malaria in northeast Myanmar: A prospective open-label efficacy trial. Travel Med Infect Dis 36: 101499.
-
32.
Kshirsagar NA et al., 2000. A randomized, double-blind, parallel-group, comparative safety, and efficacy trial of oral co-artemether versus oral chloroquine in the treatment of acute uncomplicated Plasmodium falciparum malaria in adults in India. Am J Trop Med Hyg 62: 402–408.
-
33.
van Eijk AM et al., 2016. What is the value of reactive case detection in malaria control? A case-study in India and a systematic review. Malar J 15: 67.
-
34.
van Eijk AM et al., 2019. The burden of submicroscopic and asymptomatic malaria in India revealed from epidemiology studies at three varied transmission sites in India. Sci Rep 9: 17095.
-
35.
Nagpal BN, Sharma VP, 1995. Indian Anophelines. Lebanon, NH: Science Publishers, Inc.
-
36.
Nagpal BN, Srivastava A, Saxena R, Ansari MA, Dash AP, Das SC, 2005. Pictorial Identification Key for Indian Anophelines. Delhi: Malaria Research Center, 8–10.
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