Current Status of Insecticide Susceptibility in the Principal Malaria Vector, Anopheles gambiae in Three Northern States of Nigeria
-
Mustapha Ahmed Yusuf
,
Mohammad Ali Oshaghi
,
Hassan Vatandoost
,
Ahmad Ali Hanafi-Bojd
,
Ahmadali Enayati
,
Rabiu Ibrahim Jalo
,
Akande Oyebanji Azeez Aliyu Aminu
,
Isa Muhammad Daneji
Abstract
Background: Malaria is a major public health problem in Nigeria with 97% of its population with high morbidity and mortality. Mosquitoes play an important role in the transmission of malaria parasites. This study was conducted to evaluate the current resistance status of Anopheles gambiae to insecticides.
Methods: Larvae of An. gambiae was collected from three zones; A, B and C differentiated on the basis of variation in agricultural ecosystems between August and November, 2018 in the northeast and northwestern parts of Nigeria. They were carefully reared to adult stage and insecticidal susceptibility tests were conducted.
Results: The mosquitoes tested showed high levels of resistance to all the insecticides used with the exception of malathion. Study zone A, recorded 74% mortality after 24h to deltamethrin compared to 81% from zone B and 82% from zone C, respectively. Mosquitoes from zone B exposed to DDT had the highest level of resistance at 37% compared to 40% and 53% from zones A and C, respectively. Resistant to bendiocarb was also observed, with zone A having the lowest mortality of 44% compared to 48% from zone C and 55% from Zone B, respectively. According to the results of knockdown tests, mosquitoes from Zone A exposed to deltamethrin recorded the lowest knockdown across the study locations while zone B recorded the lowest knockdown for DDT.
Conclusion: The results of the study provide an insight into the current status of An. gambiae to four major insecticides in northern Nigeria as guideline for mosquitocontrol.
1. World Health Organization (2020) World malaria report. p. 125.
2. World Health Organization (2017) Achiev-ing and maintaining universal cov¬erage with long-lasting insecticidal nets for ma¬laria control. p. 156.
3. World Health Organization (2018) World malaria report. p. 125.
4. Nigeria Malaria Indicator Survey (2015) Fact Sheet. p. 12.
5. Sheet NMF (2011) United States Embassy in Nigeria Publication. Retrieved from http//photos. State. gov//libraries/nigeria/231771/public
6. Ibrahim SS, Mukhtar MM, Datti JA, Irving H, Kusimo MO, Tchapga W, Lawal N, Sambo F, Wondji CS (2019) Temporal escalation of pyrethroid resistance in the major malaria vector Anopheles coluzzii from Sahelo-Sudanian region of north-ern Nigeria. Sci Rep. 9(1): 7395.
7. Olatunbosun-Oduola A, Abba E, Adelaja O, Taiwo-Ande A, Poloma-Yoriyo K, Samson-Awolola T (2019) Wide¬spread re¬port of multiple insecticide re¬sistance in Anopheles gambiae s.l. mosquitoes in eight communities in southern Gom¬be, North-Eastern Nigeria. J Arthropod Borne Dis. 13(1): 50–61.
8. Coetzee M (2004) Distribution of the Af-rican malaria vectors of the Anopheles gambiae complex. Am J Trop Med Hyg. 70(2): 103–104.
9. Yakob L (2011) Epidemiological conse-quenc¬es of a newly discovered cryptic sub¬group of Anopheles gambiae. Biol Lett. 7(6): 947–949.
10. Williams M, Contet A, Hou C-FD, Levash¬ina EA, Baxter RH (2019) Anopheles gambiae TEP1 forms a complex with the coiled-coil domain of LRIM1/ APL1C following a conformational change in the thioester domain. PLoS One. 14(6): 10–14.
11. Lawniczak M, Emrich S, Holloway A, Regier A, Olson M, White B, Red¬mond S, Fulton L, E Appelbaum, Godfrey J, Farmer C, Chinwalla A, Yang SP, Minx P, Nelson J, Kyung K, Walenz BP, Gar-cia-Hernandez E, Aguiar M, Viswa-nathan LD, Rogers YH, Strausberg RL, Saski CA, Lawson D, Collins FH, Kafa-tos FC, Christophides GK, Clifton SW, Kirkness EF, Besansky NJ (2010) Wide-spread di¬vergence between incipient Anoph¬eles gam¬biae species revealed by whole genome sequences. Science. 330(6003): 512–514.
12. Derua YA, Alifrangis M, Magesa SM, Kisin¬za WN, Simonsen PE (2015) Sibling spe¬cies of the Anopheles funestus group, and their infection with malaria and lym¬phatic filarial parasites, in archived and newly collected specimens from north¬eastern Tanzania. Malar J. 14(1): 104–110.
13. Ibrahim SS, Manu YA, Tukur Z, Irving H, Wondji CS (2014) High frequency of kdr L1014F is associated with py¬re-throid re¬sistance in Anopheles coluzzii in Sudan savannah of northern Ni¬ge¬ria. BMC In¬fect Dis. 14: 441.
14. Habibu U, Yayo A, Yusuf Y (2017) Sus-ceptibility status of Anopheles gam¬bi¬ae complex to Insecticides commonly used for malaria control in northern Ni¬geria. Int J Sci Technol Res. 6(6): 47–54.
15. Wondji CS, Coleman M, Kleinschmidt I, Mzilahowa T, Irving H, Ndula M, Rehman A, Morgan J, Barnes KG, Hem¬ingway J (2012) Impact of pyrethroid resistance on operational malaria con¬trol in Malawi. Proc Natl Acad Sci U S A. 109(47): 19063–19070.
16. Habibu A, Andrew JS, Hapca S, Mukhtar MD, Yusuf YD (2017) Malaria vec¬tors resistance to commonly used in¬sec¬ti-cides in the control of Malaria in Bichi, North¬ern Nigeria. Bayero J Pur Appl Sci. 10 (1): 1–6.
17. Kolade T, Kehinde O, Oluwatobi R, Ade-dapo O, Audu K (2013) Susceptibility of Anopheles gambiae sensu lato to per-me¬thrin, deltamethrin and ben¬dio¬carb in Iba¬dan City, southwest Nigeria. Curr Res J Biol Sci. 5(2): 42–48.
18. Mohammed BR, Abdulsalam YM, Deeni YY (2015) Insecticide resistance to Anoph¬eles spp. mosquitoes (Diptera: Cu¬licidae) in Nigeria. A Review. Inter J Mosq Res. 2(3): 56–63.
19. World Health Organization (2006) Pes¬
ticides and their application: for the con-trol of vectors and pests of public health importance. p. 125.
20. Charlwood J, Qassim M, Elnsur E, Don-nelly M, Petrarca V, Billingsley PF (2001) The impact of indoor residual spraying with malathion on malaria in refugee camps in eastern Sudan. Acta Trop. 80 (1): 1–8.
21. WHO (2016) Test procedures for insecti-cide resistance monitoring in malaria vec¬tor mosquitoes. p. 56.
22. Safiyanu M, Alhassan A, Abubakar A (2016) Detoxification enzymes activi¬ties in del¬tamethrin and bendiocarb re¬sistant and susceptible malarial vectors (Anopheles gambiae) breeding in Bichi agricultural and residential sites, Kano state, Ni¬ge¬ria. Bayero J Pur Appl Sci. 9(1): 142–149.
23. Nutifafa GG, Hanafi-Bojd AA, Oshaghi M, Dadzie S, Vatandoost H, Koosha M (2017) Insecticide Susceptibility sta¬tus of An. gambiae s. l. (Culicidae: Giles) from selected in-land and coastal agricultural areas of Ghana. J Entomol Zool Stud. 5 (1): 701–707.
24. Baffour-Awuah S, Annan AA, Maiga-Asco¬fare O, Dieudonné SD, Adjei-Kusi P, Owusu-Dabo E (2016) Insecticide re-sistance in malaria vectors in Kumasi, Ghana. Parasit Vector. 9 (1): 633–640.
25. Map of Nigeria Https://maps-nige-ria.com/draw-the-map-of-nigeria-showing-vegetation-zone
26. National Population Comission, Federal Capiatal Territory Abuja (2006) Na¬tion-al Population Census.
27. Humanitarian Bulletin of Nigeria. Https://tukool.com/know-nigeria/know-about-gombe-state/know-about-yamaltu-deba
28. Adetifa IM, Adamu AL, Karani A, Waitha¬-ka M, Odeyemi KA, Okoromah CA (2018) Nasopharyngeal Pneumococcal Car¬riage in Nigeria: a two-site, popu¬la¬tion-based survey. Sci Rep. 8(1): 3509.
29. World Health Organization (1998) Test pro¬cedures for insecticide resistance mon¬itoring in malaria vectors, bio-ef-ficacy and persistence of insecticides on treated surfaces: report of the WHO informal consultation. Available at: https://apps.who.int/iris/handle/10665/64879
30. Abbott W (1987) A method of computing the effectiveness of an insecticide. J Am Mosq Control Assoc. 3(2): 302–326.
31. World Health Organization (1998) Test procedures for insecticide resistance mon¬itoring in malaria vector mosqui¬toes. 2nd WHO,Geneva, p. 54.
32. Oduola AO, Idowu ET, Oyebola MK, Adeogun AO, Olojede JB, Otubanjo OA, Awolola TS (2012) Evidence of carba¬mate resistance in urban pop¬u¬la-tions of Anopheles gambiae ss mos¬qui-toes re¬sistant to DDT and del¬tame¬thrin insecti¬cides in Lagos, South-West¬ern Nigeria. Parasit Vectors. 5(1): 116.
33. Umar A, Kabir B, Amajoh C, Inyama P, Ordu D, Barde A (2014) Susceptibility test of female Anopheles mosquitoes to ten insecticides for indoor residual spraying (IRS) baseline data collection in Northeastern Nigeria. J Entomol Nematol. 6(7): 98–103.
34. Ibrahim SS, Mukhtar MM, Irving H, Lab-bo R, Kusimo MO, Mahamadou I, Wondji CS (2019) High Plasmodium infection and multiple insecticide resistance in a major malaria vector Anopheles coluzzii from Sahel of Ni¬ger Republic. Malar J. 18(1): 181–190.
35. Alhassan A, Sule M, Dangambo M, Yayo A, Safiyanu M, Sulaiman D (2015) Detoxification enzymes activities in DDT and Bendiocarb resistant and suceptible malarial vector (Anopheles gambiae) breed in Auyo residential and irrigation sites Northwest Nigeria. Europe Sci J. 11(9): 315–326.
2. World Health Organization (2017) Achiev-ing and maintaining universal cov¬erage with long-lasting insecticidal nets for ma¬laria control. p. 156.
3. World Health Organization (2018) World malaria report. p. 125.
4. Nigeria Malaria Indicator Survey (2015) Fact Sheet. p. 12.
5. Sheet NMF (2011) United States Embassy in Nigeria Publication. Retrieved from http//photos. State. gov//libraries/nigeria/231771/public
6. Ibrahim SS, Mukhtar MM, Datti JA, Irving H, Kusimo MO, Tchapga W, Lawal N, Sambo F, Wondji CS (2019) Temporal escalation of pyrethroid resistance in the major malaria vector Anopheles coluzzii from Sahelo-Sudanian region of north-ern Nigeria. Sci Rep. 9(1): 7395.
7. Olatunbosun-Oduola A, Abba E, Adelaja O, Taiwo-Ande A, Poloma-Yoriyo K, Samson-Awolola T (2019) Wide¬spread re¬port of multiple insecticide re¬sistance in Anopheles gambiae s.l. mosquitoes in eight communities in southern Gom¬be, North-Eastern Nigeria. J Arthropod Borne Dis. 13(1): 50–61.
8. Coetzee M (2004) Distribution of the Af-rican malaria vectors of the Anopheles gambiae complex. Am J Trop Med Hyg. 70(2): 103–104.
9. Yakob L (2011) Epidemiological conse-quenc¬es of a newly discovered cryptic sub¬group of Anopheles gambiae. Biol Lett. 7(6): 947–949.
10. Williams M, Contet A, Hou C-FD, Levash¬ina EA, Baxter RH (2019) Anopheles gambiae TEP1 forms a complex with the coiled-coil domain of LRIM1/ APL1C following a conformational change in the thioester domain. PLoS One. 14(6): 10–14.
11. Lawniczak M, Emrich S, Holloway A, Regier A, Olson M, White B, Red¬mond S, Fulton L, E Appelbaum, Godfrey J, Farmer C, Chinwalla A, Yang SP, Minx P, Nelson J, Kyung K, Walenz BP, Gar-cia-Hernandez E, Aguiar M, Viswa-nathan LD, Rogers YH, Strausberg RL, Saski CA, Lawson D, Collins FH, Kafa-tos FC, Christophides GK, Clifton SW, Kirkness EF, Besansky NJ (2010) Wide-spread di¬vergence between incipient Anoph¬eles gam¬biae species revealed by whole genome sequences. Science. 330(6003): 512–514.
12. Derua YA, Alifrangis M, Magesa SM, Kisin¬za WN, Simonsen PE (2015) Sibling spe¬cies of the Anopheles funestus group, and their infection with malaria and lym¬phatic filarial parasites, in archived and newly collected specimens from north¬eastern Tanzania. Malar J. 14(1): 104–110.
13. Ibrahim SS, Manu YA, Tukur Z, Irving H, Wondji CS (2014) High frequency of kdr L1014F is associated with py¬re-throid re¬sistance in Anopheles coluzzii in Sudan savannah of northern Ni¬ge¬ria. BMC In¬fect Dis. 14: 441.
14. Habibu U, Yayo A, Yusuf Y (2017) Sus-ceptibility status of Anopheles gam¬bi¬ae complex to Insecticides commonly used for malaria control in northern Ni¬geria. Int J Sci Technol Res. 6(6): 47–54.
15. Wondji CS, Coleman M, Kleinschmidt I, Mzilahowa T, Irving H, Ndula M, Rehman A, Morgan J, Barnes KG, Hem¬ingway J (2012) Impact of pyrethroid resistance on operational malaria con¬trol in Malawi. Proc Natl Acad Sci U S A. 109(47): 19063–19070.
16. Habibu A, Andrew JS, Hapca S, Mukhtar MD, Yusuf YD (2017) Malaria vec¬tors resistance to commonly used in¬sec¬ti-cides in the control of Malaria in Bichi, North¬ern Nigeria. Bayero J Pur Appl Sci. 10 (1): 1–6.
17. Kolade T, Kehinde O, Oluwatobi R, Ade-dapo O, Audu K (2013) Susceptibility of Anopheles gambiae sensu lato to per-me¬thrin, deltamethrin and ben¬dio¬carb in Iba¬dan City, southwest Nigeria. Curr Res J Biol Sci. 5(2): 42–48.
18. Mohammed BR, Abdulsalam YM, Deeni YY (2015) Insecticide resistance to Anoph¬eles spp. mosquitoes (Diptera: Cu¬licidae) in Nigeria. A Review. Inter J Mosq Res. 2(3): 56–63.
19. World Health Organization (2006) Pes¬
ticides and their application: for the con-trol of vectors and pests of public health importance. p. 125.
20. Charlwood J, Qassim M, Elnsur E, Don-nelly M, Petrarca V, Billingsley PF (2001) The impact of indoor residual spraying with malathion on malaria in refugee camps in eastern Sudan. Acta Trop. 80 (1): 1–8.
21. WHO (2016) Test procedures for insecti-cide resistance monitoring in malaria vec¬tor mosquitoes. p. 56.
22. Safiyanu M, Alhassan A, Abubakar A (2016) Detoxification enzymes activi¬ties in del¬tamethrin and bendiocarb re¬sistant and susceptible malarial vectors (Anopheles gambiae) breeding in Bichi agricultural and residential sites, Kano state, Ni¬ge¬ria. Bayero J Pur Appl Sci. 9(1): 142–149.
23. Nutifafa GG, Hanafi-Bojd AA, Oshaghi M, Dadzie S, Vatandoost H, Koosha M (2017) Insecticide Susceptibility sta¬tus of An. gambiae s. l. (Culicidae: Giles) from selected in-land and coastal agricultural areas of Ghana. J Entomol Zool Stud. 5 (1): 701–707.
24. Baffour-Awuah S, Annan AA, Maiga-Asco¬fare O, Dieudonné SD, Adjei-Kusi P, Owusu-Dabo E (2016) Insecticide re-sistance in malaria vectors in Kumasi, Ghana. Parasit Vector. 9 (1): 633–640.
25. Map of Nigeria Https://maps-nige-ria.com/draw-the-map-of-nigeria-showing-vegetation-zone
26. National Population Comission, Federal Capiatal Territory Abuja (2006) Na¬tion-al Population Census.
27. Humanitarian Bulletin of Nigeria. Https://tukool.com/know-nigeria/know-about-gombe-state/know-about-yamaltu-deba
28. Adetifa IM, Adamu AL, Karani A, Waitha¬-ka M, Odeyemi KA, Okoromah CA (2018) Nasopharyngeal Pneumococcal Car¬riage in Nigeria: a two-site, popu¬la¬tion-based survey. Sci Rep. 8(1): 3509.
29. World Health Organization (1998) Test pro¬cedures for insecticide resistance mon¬itoring in malaria vectors, bio-ef-ficacy and persistence of insecticides on treated surfaces: report of the WHO informal consultation. Available at: https://apps.who.int/iris/handle/10665/64879
30. Abbott W (1987) A method of computing the effectiveness of an insecticide. J Am Mosq Control Assoc. 3(2): 302–326.
31. World Health Organization (1998) Test procedures for insecticide resistance mon¬itoring in malaria vector mosqui¬toes. 2nd WHO,Geneva, p. 54.
32. Oduola AO, Idowu ET, Oyebola MK, Adeogun AO, Olojede JB, Otubanjo OA, Awolola TS (2012) Evidence of carba¬mate resistance in urban pop¬u¬la-tions of Anopheles gambiae ss mos¬qui-toes re¬sistant to DDT and del¬tame¬thrin insecti¬cides in Lagos, South-West¬ern Nigeria. Parasit Vectors. 5(1): 116.
33. Umar A, Kabir B, Amajoh C, Inyama P, Ordu D, Barde A (2014) Susceptibility test of female Anopheles mosquitoes to ten insecticides for indoor residual spraying (IRS) baseline data collection in Northeastern Nigeria. J Entomol Nematol. 6(7): 98–103.
34. Ibrahim SS, Mukhtar MM, Irving H, Lab-bo R, Kusimo MO, Mahamadou I, Wondji CS (2019) High Plasmodium infection and multiple insecticide resistance in a major malaria vector Anopheles coluzzii from Sahel of Ni¬ger Republic. Malar J. 18(1): 181–190.
35. Alhassan A, Sule M, Dangambo M, Yayo A, Safiyanu M, Sulaiman D (2015) Detoxification enzymes activities in DDT and Bendiocarb resistant and suceptible malarial vector (Anopheles gambiae) breed in Auyo residential and irrigation sites Northwest Nigeria. Europe Sci J. 11(9): 315–326.
| Files | ||
| Issue | Vol 15 No 2 (2021) | |
| Section | Original Article | |
| DOI | https://doi.org/10.18502/jad.v15i2.7489 | |
| Keywords | ||
| Malaria; Anopheles gambiae; Insecticide resistance; Susceptibility; Northern Nigeria | ||
| Rights and permissions | |
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This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
How to Cite
1.
Ahmed Yusuf M, Oshaghi MA, Vatandoost H, Hanafi-Bojd AA, Enayati A, Jalo RI, Aminu AOAA, Daneji IM. Current Status of Insecticide Susceptibility in the Principal Malaria Vector, Anopheles gambiae in Three Northern States of Nigeria. J Arthropod Borne Dis. 2021;15(2):196-206.
