Insecticide Resistance Profile and Detoxification Enzyme Activities of Anopheles Mosquitoes from Three Different Breeding Habitats in Sudan Savannah Region of Jigawa State, Nigeria
Malaria is a disease of global public health concern. The disease has its highest global burden and mortality in Africa while Nigeria has up to 25% of global malaria burden. Prevention is achievable through targeting mosquito vectors with insecticides. A primary concern in the global malaria control is resistance to insecticides which affects vector control interventions. It is therefore significant to know mosquitoes’ insecticide resistance profile. This study is aimed at determining insecticide resistance profile and enzyme activities of Anopheles mosquitoes from three different breeding habitats. Larval samples were collected during rainy season (August, September and October, 2019) from Hadejia and Dutse towns of Jigawa State. Larvae were reared to adults in the insectary and morphologically identified. WHO insecticide bioassay was conducted using permethrin 0.75%, deltamethrin 0.05%, bendiocarb 0.1%, and dichlorodiphenyltrichloroethane 4%. About 100 samples (20 – 25 per test per four replicates) were used for each tested insecticide. Results showed preponderance of An. gambiae complex in the three study sites. High resistant levels according to WHO protocol with mortality less than 90% were recorded for all the tested insecticides, suggesting resistances in the Anopheles mosquitoes. Highest monooxygenase, glutathione-s-transferases and esterases activities were recorded in agricultural site compared to other sites. These findings can be attributed to differences in activities that occur in the study areas. Findings of this study can serve as threat to vector control measures in the study sites.
Abdulkadir, M., Ruslan, R. and Mohammed, M. U. (2019). Free maternal healthcare programme under the successful delivery programme in Jigawa State, Nigeria. International Journal of Psychosocial Rehabiltation, 23(4):707-718.
Alhassan, A. J., Sule, M. S., Dangambo M. A, Yayo, A. M., Safiyanu, M. and Sulaiman, D. (2015). Detoxification enzymes activities in DDT and bendiocarb resistant andsuceptible malarial vector (Anopheles gambiae) breed in Auyo residential and irrigation sites Northwest Nigeria. European Scientific Journal, 11(9): 315- 326.
Awolola, S. T., Adeogun, A. O., Olojede, J. B., Oduola, A. O., Oyewole, I. O. and Amajoh, C. N. (2014). Impact of PermaNet 3.0 on entomological indices in an area of pyrethroid resistant Anopheles gambiae in south-western Nigeria. Parasites and Vectors, 7(1): 1-10.
Brogdon, W. G.and McAllister, J. C. (1998). Insecticide resistance and vector control. Emerging Infectious Diseases, 4(4): 605–613.
Boussougou-Sambe, S. T., Eyisap, W. E., TaboueTasse, G. C., Stanislas Elysee Mandeng, S. E., Mbakop, L. R., Enyong, P., Etang, J., Fokam, E. B., and Awono-Ambene, P. H. (2018). Insecticide susceptibility status of Anopheles gambiae (s.l.) in South-West Cameroon four years after long-lasting insecticidal net mass distribution. Parasites and Vectors, 11(1):1-8.
Camara, S., Koffi, A. A., Ahoua Alou, L. P., Koffi, K., Kabran, J. K. and Koné, A. (2018). Mapping insecticide resistance in Anopheles gambiae (s.l.) from Côte d’Ivoire.Parasites and Vectors, 11(1):1-11.
Clark, A. G. (1990). The glutathione s transferase and resistance to insecticides in: Hayes JD,Picket, CB, and Mantle JD (Eds.) Glutathione s Transferase and Drug Resistance London, 369-378.
Coetzee, M., Hunt, R. H., Wilkerson, R., Della Torre, A., Coulibaly, M. B. and Besansky, N. J. (2013). Anopheles coluzzii and Anopheles amharicus, new members of the Anopheles gambiae complex. Zootaxa, 3619: 246–274.
Crow, J. A., Potter, P. M., Borazjani, A., and Rose, M. K. (2007). Hydrolysis of pyretheroids byhuman and rat tissues. Examination of intestinal, liver and serum carboxylesterase. Toxicology and Applied Pharmacology, 221:1-12.
Cuamba, N., Morgan, J. C., Irving, H., Steven, A. and Wondji, C. S. (2010). High level of pyrethroid resistance in an Anopheles funestus population of the Chokwe District in Mozambique.PLoS One, 5(6): e11010.
Das, S., Garver, L. and Dimopoulos, G. (2007). Protocol for mosquito rearing (A. gambiae). Journal of Visualized Experiments, 5:221.https://doi.org/10.3791/221
Djouaka, R. F., Bakare, A. A., Coulibaly, O. N., Akogbeto, M. C., Ranson, H. and Hemingway, J. (2008). Expression of the cytochrome P450s, CYP6P3 and CYP6M2 are significantly elevated in multiple pyrethroid resistant populations of Anopheles gambiaes.s. from Southern Benin and Nigeria. BMC Genomics, 9(1):1-10.
Erhabor, O., Adias, T. C. and Hart, M. L. (2010). Effect of falciparum malaria on the indices of anaemia among pregnant women in the Niger Delta of Nigeria. Journal of Clinical Medicine and Research, 2(3):035-041.
Faiz, O. A., colak, N., Saglam, S., and Belduz, A. O. (2007). Determination and characterization of thermostableesterolytic activity from a novel thermopilic bacterium AnoxybaccilusgonesisA4.BMB Reports, 40(4): 588-594.
Gillies, M. T. and Coetzee, M. (1987). Supplement to the Anophelinae of Africa South of the Sahara (Afrotropical region). Publications of The South African Institute for Medical Research, 55:1-143.
Habig, W. H., Pabst, M. J., and Jacoby, W. B. (1974). Glutathione S-transferase: The firstenzymatic step in mercapturic acid formation. Journal of Biological Chemistry, 249:7130- 7139
Hemingway, J., Hawkes, N., Prapanthadara, L., Jayawardena, K. G., and Ranson, H. (1998). The role of gene splicing, gene amplification and regulation in mosquito insecticide resistance. Philosophical Transactions of the Royal Society of London, 29: 1695-1699.
Hemingway, J., Field, L. and Vontas, J. (2002). An overview of insecticide resistance. Science, 298: 96–97.
Ibrahim, K. T., Popoola, K. O., Adewuyi, O. R., Adeogun, A. O. and Oricha, A. K. (2013). Susceptibility of Anopheles gambiae sensulato to permethrin, deltamethrin and bendiocarb in Ibadan city, southwest Nigeria. Current Research Journal of Biological Sciences, 5(2): 42–44.
Ibrahim, S. S., Manu, Y. A., Tukur, Z., Irving, H. and Wondji, C. S. (2014). High frequency of kdr L1014F is associated with pyrethroid resistance in Anopheles coluzzii in Sudan savannah of northern Nigeria. Ibrahim et al. BMC Infectious Diseases, 14:441.
Ibrahim, S. S., Mukhtar, M. M., Datti, J. A., Irving, H., Kusimo, M. O., Tchapga, W., Lawal, N., Fatima I. Sambo, F. I. and Wondji, C. S. (2019). Temporal escalation of Pyrethroid Resistance in the major malaria vector Anopheles coluzziifrom Sahelo-Sudanian Region of northern Nigeria. Scientific Reports,9:7395https://doi.org/10.1038/s41598-019-43634-4
Jenavine O. M., Njoku, O. O., Agwu, U. N., Ijem, A. N. and Amaechi, J. N. (2015). Incidence of antenatal malaria parasitaemia and the effects on the haemoglobin profile of the pregnant women in Enugu East Local Government Area, Enugu, Nigeria. American Journal of Epidemiology and Infectious Disease, 3(5): 88-94.
Jigawa State JGS, (2015). A New World. [http://www.jigawastate.gov.ng/contentpage.php?id=82]. Accessed 02 January, 2020.
Kalilani-Phiri, L. V., Lungu, D. and Coghlan, R. (2011). Knowledge and malaria treatment practices using artemisinin combination therapy (ACT) in Malawi: survey of health professionals. Malaria Journal, 10:279.
Kemabonta, K. A., Anikwe, J. C. and Adaezeobiora, I. B. (2013). Bioefficacy of Skaeter Abateand Spintor on Anopheles gambiaeand Aedesaegypti mosquitoes from insecticides resistance areas of Lagos and Oyo State, Nigeria.Journal of Biology Agriculture and Healthcare,3:(3).
Khan, S., Uddin, M. N., Rizwan, M., Khan, W., Farooq, M., Shah, A. S., Subhan, F., Aziz, F.,Rahman, U. R., Khan, A., Ali, S., and Muhammad (2020).Mechanism of Insecticide Resistancein Insects/Pests.Polish Journal of Environmental Studies, Vol. 29,No. 3: 2023-2030. DOI: 10.15244/pjoes/108513
Liu, N., Li, M., Gong, Y., Liu, F., and Li, T. (2015). Cytochrome P450s–Their expression, regulation, and role in insecticide resistance. Pesticide Biochemistry and Physiology, 120, 77-81.
Mnzava, A. P., Knox, T. B., Temu, E. A., Trett, A., Fornadel, C. and Hemingway, J. (2015). Implementation of the global plan for insecticide resistance management in malaria vectors: progress, challenges and the way forward. Malaria Journal, 14:173.
Mulla, M. S. (1994). “Mosquito control then, now, and in the future,” Journal of the American Mosquito Control Association, 10 (4): 574-575.
Niang, E. A., Bassene, H., Fenollar, F. and Mediannikov, O. (2018). Biological Control of Mosquito-Borne Diseases: The Potential of Wolbachia-Based Interventions in an IVM Framework. Hindawi Journal of Tropical Medicine, Article ID 1470459:15
Noland, G. S., Graves, P. M., Sallau, A., Eigege, A., Emukah, E., Patterson, A.E. and Ajiji, J. (2014). Malaria prevalence, anaemia and baseline intervention coverage prior to mass net distributions in Abia and Plateau States, Nigeria.BMC Infectious Diseases, 14:168. DOI:10.1186/1471-2334-14-168.
Nwane, P., Etang, J., Chouaibu, M., Toto, J. C., Kerah – Hinzombe, C., and Mimfoundi, R.(2009). Trend in DDT and pyretheroids resistance in Anopheles gambiae ss. Population from urban and agroindustrial settings in southern Cameroon. BMC Infectious Disease, 9:(163).
Oduola, A. O., Obansa J. B., Ashiegbu, C. O., Adeogun, A. O., Otubanjo, O. A. and Awolola, T.S. (2010). High Level of DDT Resistance in the Malaria Mosquito: Anopheles gambiaes.l. from Rural, Semi Urban and Urban Communities in Nigeria. Journal Rural and Tropical Public Health, 9: 114–120.
Oduola, A. O., Idowu, E. T., Oyebola, M. K., Adeogun, A. O., Olojede, J. B., Otubanjo, O.A.and Awolola, T. S. (2012). Evidence of carbamate resistance in urban populations of Anopheles gambiaes.s.mosquitoes’ resistance to DDT and deltamethrin insecticides in Lagos, South-Western Nigeria. Parasites & Vectors, 5:116. doi: 10.1186/1756-3305-5-116
Oduola, A. O., Abba, E., Adelaja, O., Ande, A. T., Yoriyo, K. P. and Awolola, T. S. (2019). Widespread Report of Multiple Insecticide Resistance in Anopheles gambiaes. l. Mosquitoes in Eight Communities in Southern Gombe, North-Eastern Nigeria. Journal of Arthropod-Borne Diseases, 13(1): 50–61
Ononamadu, C. J, Datit, J. T. and Imam, A. A. (2020). Insecticide Resistance Profile of Anopheles gambiae Mosquitoes: A Study of a Residential and Industrial Breeding Sites in Kano Metropolis, Nigeria. Environmental Health Insights, 14: 1–9 sagepub.com/journals-permissions. DOI: 10.1177/1178630219897272
Ranson, H. and Lissenden, N. (2016). Insecticide Resistance in African Anopheles mosquitoes: A worsening situation that needs urgent action to maintain malaria control. Trends in Parasitology, 32(3): 187–196. https://doi.org/10.1016/j.pt.2015.11.010
Raymond, M., Chevillon, C., Guillemaud, T., Lenormand, T. and Pasteur, N. (1998). An overview of the evolution of overproduced esterases in the mosquito Culexpipiens. Philosophical Transactions of the Royal Society B: Biological Sciences; 353, 1707–1711.
Reid, M. C. and McKenzie, F. E. (2016). The contribution of agricultural insecticide use to increasing insecticide resistance in African malaria vectors. Malaria Journal, 15(1): 1-8.
Reyes, M., Franck, P., Olivares, J., Margaritopoulos, J., Knight, A., and Sauphanor, B. (2009). Worldwide variability of insecticide resistance mechanisms in the codling moth, Cydiapomonella L. (Lepidoptera: Tortricidae). Bulletin of Entomological Research, 99(4): 359-369.
Robert, V., Le Goff, G. and Ariey, F. A. (2002). Possible alternative method for collecting mosquito larvae in rice fields. Malaria Journal, 1(1):1-4.
Russell, R. J., Scott, C., Jackson, C. J., Pandey, R., Pandey, G., Taylor, M. C., and Oakeshott, J. G. (2011). The evolution of new enzyme function: lessons from xenobiotic metabolizing bacteria versus insecticide‐resistant insects. Evolutionary Applications, 4(2): 225-248.
Safiyanu, M., Alhassan, A. J. and Abubakar, A. B. (2016). Detoxification enzymes activities inDeltamethrin and Bendiocarb resistant and susceptible malarial vectors (Anopheles gambiae) breeding in Bichi Agricultural and Residential sites, Kano State, Nigeria. Bayero Journal of Pure and Applied Sciences, 9(1): 142 – 149.
Safiyanu, M., Alhassan, A. J., Imam, A. A. and Abdullahi, H. (2017). Pyretheroids Resistance and Detoxifying Enzymes Activities of Malaria Vector (Anopheles gambiae) Breeding in Auyo Irrigation and Residential Sites, Jigawa State, Nigeria. Annual Research & Review in Biology; 17(2): 1-8.
Safiyanu, M., Alhassan, A. J., Yayo, A. M., Ibrahim, S. S., Imam, A. A. and Abdullahi. H. (2019). Detection of KDR l1014f mutation in pyrethroids susceptible Anopheles gambiaes.l from Ladanai, Kano state, northwest Nigeria. International Journal of Mosquito Research, 6(3): 10-15.
Serebrov, V. V., Gerber, O. N., Malyarchuk, A. A. Martemyanov, V. V., Alekseev, A. A., and Glupov, V. V. (2006). Effect of entomopathogenic fungi on detoxification enzyme activity in greater wax moth Galleria mellonella L. (Lepidoptera, Pyralidae) and role of detoxification enzymes in development of insect resistance to entomopathogenic fungi. Biology Bulletin, 33(6): 581-586.
Service, M. W. (1993). Mosquito ecology. Field sampling methods.2nd edition. London: Elsevier/Chapman and Hall. pp244.
Stica, C., Jeffries, C. L., Irish, S. R., Barry, Y., Camara, D, Yansane, I, Kristan, M., Walker, T. and Messenger, L. A. (2019). Characterizing the molecular and metabolic mechanisms of insecticide resistance in Anopheles gambiaein Faranah, Guinea. Malaria Journal, 18(1):1-15.
Strode, C., Donegan, S., Garner, P., Enayati, A. A. and Hemingway, J. (2014). The impact of pyrethroid resistance on the efficacy of insecticide-treated bed nets against African anopheline mosquitoes: systematic review and meta-analysis. PLoS Medicine, 11: e1001619.
Umar, A., Kabir, B. G. J., Amajoh, C. N., Inyama, P. U., Ordu, D. A., Barde, A. A., Misau, A.A., Sambo, M. L., Babuga, U., Kobi, M. and Jabbdo, M. A. (2014). Susceptibility test of female anopheles mosquitoes to ten insecticides for indoor residual spraying (IRS) baseline data collection in Northeastern Nigeria. Journal of Entomology and Nematology, 6 (7): 98-103.
UPMI (2020). USAID President’s Malaria Initiative FY. Nigeria Malaria Operational Plan.
Weill, M., Malcolm, C., Chandre, F., Mogensen, K., Berthomieu, A., and Marquine, M. (2004). The unique mutation in ace-1 giving high insecticide resistance is easily detectable in mosquito vectors. Insect Molecular Biology, 13(1):1-7.
Wen, Z., Pan, L., Berenbaum, M. R.and Schuler, M. A. (2003). Metabolism of linear and angular furanocoumarins by Papiliopolyxenes CYP6B1 co-expressed with NADPH cytochrome P450 reductase. Insect Biochemistry and Molecular Biology, 33(9):937-947.
WHO (1998). Test procedures for insecticide resistance monitoring in malaria vectors, bioefficacy and persistence of insecticides on treated surfaces. Geneva, Switzerland: World Health Organization.WHO/CDS/MAL/98.12 Geneva: World Health Organization; 1998.
WHO (2012). Global Plan for Insecticide Resistance Management in Malaria Vectors (GPIRM). In: WHO/HTM/GMP/20125. Geneva, Switzerland: Organization WHO.
WHO (2013). World Malaria Report. 2013. World Health Organization, Geneva, Switzerland. (http://www.who.int/malaria/publications). Accessed: 7th October, 2021.
WHO (2017). World malaria report 2017. Geneva: World Health Organization; 2017. Licence: CC BY-NC-SA 3.0 IGO. ISBN 978-92-4-156552-3 © World Health Organization 2017
WHO (2018). World malaria report 2018. © World Health Organization 2018. ISBN 978-92-4-156565-3
WHO (2019). World malaria report 2019. Geneva: World Health Organization; 2019.Licence:CC BY-NC-SA 3.0 IGO. ISBN 978-92-4-156572-1
World Health Organisation World Malaria Report (2020).
https://www.who.int/malaria/publications/world-malaria-report-2020/report/en/. Accessed 29th April, 2021
World Health Organization, World Malaria Report (2021). https://www.who.int/news-room/fact-sheet/detail/malaria. Accessed 28 April 2021
Wilke, A. B. B. and Marrelli, M. T. (2015). Paratransgenesis: A promising new strategy for mosquito vector control.Parasites and Vectors, 8:1.
Wondji, C. S., Coleman, M., Kleinschmidt, I., Mzilahowa, T., Irving, H., Ndula, M., Rehman, A., Morgan J, Barnes, K. G. and Hemingway, J. (2012). Impact of pyrethroid resistance on operational malaria control in Malawi.Proceedings of the National Academy of Science U S A, 109(47):19063–19070.
Wu, G., Jiang, S., and Miyata, T. (2004). Seasonal change methamidhopos susceptibility and biochemical properties in Plutellaxylostella and it parasitoid Costelliaplutella. Journal of Economic Entomology. 97:1689-1698.
Yang, Y., Wu, Y., Chen, S., Devine, G. J., Denholm, L., and Jewes, P. (2004). The involvement of microsomal oxidases in pyretheroids resistance in Helicoverpa armigera from Asia. Insect Biochemistry and Molecular Biology, 34:763-773.
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