Hostname: page-component-78c5997874-xbtfd Total loading time: 0 Render date: 2024-11-19T13:00:52.907Z Has data issue: false hasContentIssue false

The Plasmodium falciparum infection status of two major anopheline vectors in three hyper-, meso-, and hypoendemic districts in Odisha, India

Published online by Cambridge University Press:  28 February 2022

Nitika Pradhan
Affiliation:
KIIT School of Biotechnology, KIIT University, Bhubaneswar, Odisha, India Regional Medical Research Centre, Bhubaneswar, Odisha, India
Rajani Kanta Mahapatra
Affiliation:
KIIT School of Biotechnology, KIIT University, Bhubaneswar, Odisha, India
Rupenangshu K. Hazra*
Affiliation:
Regional Medical Research Centre, Bhubaneswar, Odisha, India
*
*Corresponding author. Email: rupenkh@yahoo.co.in

Abstract

In-depth understanding of malaria transmission dynamics in a region can be assessed by identifying the vector populations of infected mosquitoes, Anopheles spp. (Diptera: Culicidae), and by quantifying the infectiousness extent. In this study of malaria transmission dynamics relating to vector incrimination in three districts of Odisha, India – hyperendemic Kalahandi, mesoendemic Bargarh, and hypoendemic Cuttack – we examined how quality and quantity of plasmodial infection rates vary among mosquito species and their organs and among districts. The minimum infection rate of Plasmodium falciparum sporozoite for Anopheles culicifacies was highest in Kalahandi and nil in Cuttack. However, for A. annularis, the rate was highest in Cuttack, followed by Kalahandi and Bargarh. In Kalahandi, the gland-positive rate was higher for A. culicifacies, but in Cuttack, it was higher for A. annularis. To quantify plasmodium infection in salivary glands and guts of anopheline vectors, quantitative polymerase chain reaction was performed. We observed higher parasite density in glands than in guts of vector mosquitoes in the three districts. The findings demonstrate that plasmodium-infected vectors preferentially bind sporozoites to salivary glands in the three study areas. The results improve understanding of infection status within malaria vectors and how parasite population density may affect transmissibility, which will, in turn, provide baseline evidence to develop intervention measures.

Type
Research Paper
Copyright
© The Author(s), 2022. Published by Cambridge University Press on behalf of the Entomological Society of Canada

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

Subject Editor: Rayda Krell

References

Abraham, M., Massebo, F., and Lindtjorn, B. 2017. High entomological inoculation rate of malaria vectors in area of high coverage of interventions in southwest Ethiopia: implication for residual malaria transmission. Parasite Epidemiology and Control, 2: 6169.CrossRefGoogle ScholarPubMed
Adak, T., Singh, O.P., Nanda, N., Sharma, V.P., and Subbarao, S.K. 2006. Isolation of a Plasmodium vivax refractory Anopheles culicifacies strain from India. Tropical Medicine and International Health, 11: 197203.CrossRefGoogle ScholarPubMed
Amek, N., Bayoh, N., Hamel, M., Lindblade, K.A., Gimnig, J.E., Odhiambo, F., et al. 2012. Spatial and temporal dynamics of malaria transmission in rural western Kenya. Parasitite and Vectors, 5: 86.CrossRefGoogle ScholarPubMed
Barraud, P.J. 1934. The fauna of British India, including Ceylon and Burma. Diptera, Family Culicidae, Tribes Megarhinini and Culicini. Volume 5. Taylor and Francis, London, United Kingdom. Pp. 463.Google Scholar
Bereczky, S., Martensoon, A., Gil, P., and Farnert, A. 2005. Short report: rapid DNA extraction from archive blood spots on filter paper for genotyping of Plasmodium falciparum . American Journal of Tropical Medicine and Hygiene, 72: 249251.CrossRefGoogle ScholarPubMed
Bigoga, J.D., Manga, L., Titanji, V.P.K., Coetzee, M., and Leke, R.G.F. 2007. Malaria vector and transmission dynamics in coastal south-western Cameroon. Malaria Journal, 6: 5.CrossRefGoogle ScholarPubMed
Burkot, T.R., Dye, C., and Graves, P.M. 1989. An analysis of some factors determining the sporozoite rates, human blood indexes and biting rates of members of the Anopheles punctulatus complex in Papua New Guinea. American Journal of Tropical Medicine and Hygiene, 40: 229234.CrossRefGoogle ScholarPubMed
Churcher, T.S., Siden, R.E., Edwards, N.J, Poulton, I.D., Rampling, T.W., Brock, P.M., et al. 2017. Probability of transmission of malaria from mosquito to human is regulated by mosquito parasite density in naïve and vaccinated hosts. PLOS Pathogens, 13: e1006108.CrossRefGoogle Scholar
Cox, F.E.G. 2010. History of discovery of malaria parasites and their vectors. Parasites & Vectors, 3: 5.CrossRefGoogle ScholarPubMed
Das, B., Patra, A.P., Das, M., Mahapatra, N., Tripathy, H., Kar, S.K., and Hazra, R.K. 2014. Vectorial capacity and genetic diversity of Anopheles annularis (Diptera: Culicidae) mosquitoes in Odisha, India from 2009 to 2011. Acta Tropica, 137: 130139.CrossRefGoogle ScholarPubMed
Dia, I., Konate, L., Samb, B., Sarr, J.B., Diop, A., Rogerie, F., et al. 2008. Bionomics of malaria vectors and relationship with malaria transmission and epidemiology in three physiographic zones in the Senegal River Basin. Acta Tropica, 105: 145153.CrossRefGoogle ScholarPubMed
Garcia, J.E., Puentes, A., and Patarroyo, M.E. 2006. Developmental biology of sporozoite–host interactions in Plasmodium falciparum malaria: implications for vaccine design. Clinical Microbiology Reviews, 19: 686707.CrossRefGoogle ScholarPubMed
Gunasekaran, K., Sahu, S., Parida, S.K., Sadanandane, C., Jambulingam, P., and Das, P.K. 1989. Anopheline fauna of Koraput district, Odisha state, with particular reference to transmission of malaria. Indian Journal of Medical Research, 89: 340343.Google Scholar
Gunasekaran, K., Sahu, S.S., Jambulingam, P., and Das, P.K. 2005. DDT indoor residual spray, still an effective tool to control Anopheles fluviatilis–transmitted Plasmodium falciparum malaria in India. Tropical Medicine and International Health, 10: 160168.CrossRefGoogle ScholarPubMed
Harbach, R.E. 2004. The classification of genus Anopheles (Diptera:Culicidae): a working hypothesis of phylogenetic relationships. Bulletin of Entomological Research, 94: 537553.CrossRefGoogle ScholarPubMed
Hazra, R.K., Barik, S.K., Prusty, M.R., Rath, A., and Kar, S.K. 2013. A simple, rapid and very efficient protocol for DNA isolation from mosquito species. Version 1. Nature Protocol, Protocol Exchange. https://doi.org/10.1038/protex.2013.007.CrossRefGoogle Scholar
Kumar, A., Valecha, N., Jain, T., and Dash, A.P. 2007. Burden of malaria in India: retrospective and prospective view. American Journal of Tropical Medicine and Hygiene, Supplement 6: 6978.CrossRefGoogle Scholar
Kumari, S., Das, S., and Mahapatra, N. 2013. Anopheles subpictus B and its role in transmission of malaria in Odisha, India, Tropical Biomedicine, 30: 710717.Google ScholarPubMed
Lindsay, S.W. and Birley, M.H. 1996. Climate change and malaria transmission. Annals of Tropical Medicine and Parasitology, 90: 573588.CrossRefGoogle ScholarPubMed
Mohanty, A., Kar, P., Mishra, K., Singh, D.V., Mahapatra, N., Das, A.P., and Hazra, R.K. 2007. Multiplex PCR assay for the detection of Anopheles fluviatilis species complex, human host preference, and Plasmodium falciparum sporozoite presence, using a unique mosquito processing method. American Journal of Tropical Medicine and Hygiene, 76: 837843.CrossRefGoogle ScholarPubMed
Pimenta, P.F., Orfano, A.S., Bahia, A.C., Duarte, A.P., Rios-Velasquez, C.M., Melo, F.F., et al. 2015. An overview of malaria transmission from the perspective of Amazon Anopheles vectors. Memorias do Instituto Oswaldo Cruz, 110: 2347.CrossRefGoogle ScholarPubMed
Pimenta, P.F., Touray, M., and Miller, L. 1994. The journey of malaria sporozoites in the mosquito salivary gland. Journal of Eukaryotic Microbiology, 41: 608624.CrossRefGoogle ScholarPubMed
Pradhan, N., Pradhan, P., Pati, S., and Hazra, R.K. 2018. Epidemiological profile of malaria among various socio-demographic groups in a western district of Odisha, India. Infezioni in Medicinia, 1: 3745.Google Scholar
Pradhan, N., Rath, A., Mohanty, I., Pana, B.B., and Hazra, R.K. 2019. A comparative study of prevalence and spatial distribution of major anopheline vector fauna in a hyper- and a hypo-malaria endemic district of Odisha, India with special reference to onset of first wet season. Tropical Biomedicine, 30: 209223.Google Scholar
Pradhan, N., Tarai, R., and Hazra, R.K. 2020. Vector dynamics predicts transmission dynamics: a simple, realistic and sensible approach for measuring malaria endemicity. Bulletin of Entomological Research, 110: 379387.CrossRefGoogle ScholarPubMed
Raghavendra, K., Velamuri, P.S., Verma, V., Elamathi, N., Barik, T.K., Bhatt, R.M., and Dash, A.P. 2017. Temporo-spatial distribution of insecticide-resistance in Indian malaria vectors in the last quarter century: Need for regular resistance monitoring and management. Journal of Vector Borne Diseases, 54: 111130.Google ScholarPubMed
Rath, A., Prusty, M.R., Barik, S.K., Das, M., Tripathy, H.K., Mahapatra, N, and Hazra, R.K. 2017. Development, standardization and validation of molecular techniques for malaria vector species identification, trophic preferences and detection of Plasmodium falciparum . Journal of Vector Borne Diseases, 54: 2534.Google ScholarPubMed
Rodriguez, M.H. and Hernandez-Hernandez, F. de. L. 2004. Insect–malaria parasites interactions: the salivary gland. Insect Biochemistry and Molecular Biology, 34: 615624.CrossRefGoogle ScholarPubMed
Sahu, S.S., Gunasekaran, K., Krishnamoorthy, N., Vanamail, P., Mathivanan, A., Manonmani, A., and Jambulingam, P. 2017. Bionomics of Anopheles fluviatilis and Anopheles culicifacies (Diptera: Culicidae) in relation to malaria transmission in east–central India. Journal of Medical Entomology, 54: 821830.CrossRefGoogle ScholarPubMed
Sharma, S.K., Upadhyay, A.K., Haque, M.A., Singh, O.P., Adak, T., and Subbrao, S. 2004. Insecticide susceptibility status of malaria vectors in some hyper endemic tribal districts of Orissa. Current Science, 87: 17181726.Google Scholar
Singh, R.K., Haq, S., Kumar, G., and Dhiman, R.C. 2013. Bionomics and vectorial capacity of Anopheles annularis with special reference to India: a review. Journal of Communicable Diseases, 45: 116 Google ScholarPubMed
Suenaga, E. and Nakamura, H. 2005. Evaluation of three methods for effective extraction of DNA from human hair. Journal of Chromatography B, 820: 137141.CrossRefGoogle ScholarPubMed
Wang, J., Zhang, Y., Zhao, Y.O., Li, M.W., Zhang, L., Dragovic, S., Abraham, N.M., and Fikrig, E. 2013. Anopheles gambiae circumsporozoite protein-binding protein facilitates Plasmodium infection of mosquito salivary glands. Journal of Infectious Diseases, 208: 11611169.CrossRefGoogle ScholarPubMed
Wilson, M.E., Kantele, A., and Jokiranta, T.S. 2011. Review of cases with the emerging fifth human malaria parasite, Plasmodium knowlesi . Clinical Infectious Diseases, 52: 13561362.Google Scholar
World Health Organisation. 1992. Entomological field techniques for malaria control. Part I, Learners guide. World Health Organisation, Geneva, Switzerland.Google Scholar
Supplementary material: File

Pradhan et al. supplementary material

Table S1

Download Pradhan et al. supplementary material(File)
File 14.6 KB