Widespread Report of Multiple Insecticide Resistance in Anopheles gambiae s.l. Mosquitoes in Eight Communities in Southern Gombe, North-Eastern Nigeria
-
Adedayo Olatunbosun Oduola
,
Ezra Abba
,
Olukayode Adelaja
,
Adeolu Taiwo Ande
,
Kennedy Poloma Yoriyo
,
Taiwo Samson Awolola
Abstract
Background: Timely entomological and insecticide resistance monitoring is a key to generating relevant data for vector management. We investigated the insecticide susceptibility status of Anopheles gambiae s.l. in eight rural farming communities in Southern Gombe, Nigeria.
Methods: Overall, 3–5 days-old adult female Anopheles mosquitoes reared from field-collected immature stages between September and November, 2014 were exposed to the diagnostic doses of pyrethroids, organophosphate and carbamate insecticides using the Center for Disease Control Bottle bioassay. The observatory knockdown time from exposure to each insecticide was recorded up to two hours. The dead mosquitoes were then identified morphologically and by molecular assays.
Results: Mortality results showed resistance in An. gambiae s.l. populations to bendiocarb (2.3–100%), deltamethrin (39–70%), pirimiphos-methyl (65-95%), dichloro-diphenyl-trichloroethane (0–38.1%), permethrin (0–46.3%) and lambda-cyhalothrin (42.5–86.4%). The few cases of full susceptibility were observed from lamdacyhalothrin exposed population of An. gambiae s.l. in Banbam and Pantami respectively. An. gambiae 177 (45%) was significantly higher (P< 0.05) than An. arabiensis 64 (16.3%), An. coluzzii 34 (8.7%) and An. gambiae/An. coluzzii hybrid 78 (19.8%).
Conclusion: A strong evidence of widespread resistance in the major malaria vector species in Southern Gombe to all common classes of insecticides is a justification for the State Malaria Elimination Programme to consciously consider incorporating insecticide resistance management strategies into control programs in order to sustain the future of current control interventions.
1. National Population Commission (Nige-ria). Federal Ministry of Health of Ni-geria, National Bureau of Statistics (Nigeria), and Institute for Internation-al Programs at Johns Hopkins Bloom-berg School of Public Health. A ver¬bal/ social autopsy study to improve es-timates of the causes and determinants of neonatal and child mortality in Ni-geria (2014) Abuja, Nigeria, and Bal-timore, Maryland, USA.
2. World Health Organization (2012) World Malaria Report 2012.
3. Oduola AO, Olojede JB, Ashiegbu CO, Adeogun AO, Otubanjo OA, Awolola TS (2010) High Level of DDT Re-sistance in the Malaria Mosquito: Anopheles gam¬biae s.l. from Rural, Semi Urban and Ur¬ban Communities in Nigeria. J Rural and Trop Pub Health. 9: 114–120.
4. Ibrahim KT, Popoola KO, Adewuyi OR, Adeogun AO, Oricha AK (2013) Sus-ceptibility of Anopheles gambiae sensu lato to permethrin, deltamethrin and ben¬diocarb in Ibadan city, southwest Nigeria. Curr Res J Bio Sci. 5(2): 42–44.
5. Okorie PN, Ademowo OG, Irving H, Kelly-Hope LA, Wondji CS (2015) In-sec¬ti¬cide Susceptibility of Anopheles coluzzii and Anopheles gambiae Mos-quitoes in Ibadan, Southwest Nigeria. Med Vet Entomol. 29: 44–50.
6. Djouaka RJ, Atoyebi SM, Tchigossou GM, Riveron JM, Irving H, Akoton R, Kusi¬mo MO, Bakare AA, Wondji CS (2016) Evidence of a multiple insecti-cide resistance in the malaria vector Anopheles funestus in South West Ni-geria. Malaria J. 15: 565.
7. Nwankwo EN, Okorie PN, Acha CT, Okonk¬wo OE, Nwangwu UC, Ezihe EK (2017) Insecticide resistance in Anopheles gambiae s.l. mosquitoes in Awka, Anambra State, Southeast Nige-ria. J Mosq Res. 7(5): 32–37.
8. Adeogun AO, Popoola KO, Oduola AO, Olakiigbe AK, Awolola TS (2017) High level of DDT resistance and re-duced susceptibility to deltamethrin in Anoph¬e¬les gambiae, Anopheles coluzzi, and Anopheles arabiensis from Urban Com¬munities in Oyo State, South-West Nigeria. J Mosq Res. 7(16): 125–133.
9. Ibrahim SS, Yayo AM, Tukur Z, Irving H, Wondji CS (2014) High frequency of kdr L1014F is associated with pyre-throid resistance in Anopheles coluzzii in Sudan savannah of northern Nigeria. BMC Infectious Diseases. 14: 441.
10. Alhassan AJ, Sule MS, Dan Gambo MA, Yayo AM, Safiyanu M, Sulaiman D (2015) Detoxification Enzymes Activi-ties in DDT and Bendiocarb resistant and susceptible malarial vector (Anoph-eles gambiae) breed in Auyo residential and irrigation sites, north¬west Nigeria European Sci Journal. 11: 9.
11. Abdu HU, Manu YA, Deeni YY (2017) Susceptibility status of Anopheles gam-biae complex to insecticides com¬mon¬ly used for malaria control in Northern Nigeria. Int J Scientific Tech Res. 6(6): 47–54.
12. Gillies M, De Meillon B (1968) The Anophe¬linae of Africa South of the Sa-hara (Ethiopian zoogeographical re-gion). Pub South Afr Inst for Med Res. 54: 343.
13. Gillies MT, Coetzee M (1987) A Sup¬ple-ment to the Anophelinae of Africa South of the Sahara. A Pub South Afr Inst for Med Res. 55: 33–81.
14. Scott JA, Brogon WG, Collins FH (1993) Identification of Single Speci-men of the Anopheles Complex by Pol-ymerase Chain Reaction. Am J Trop Med Hyg.
49: 520–529.
15. Fanello C, Santolamazza F, Della Torre A (2002) Simultaneous identification of species and molecular forms of the Anopheles gambiae complex by PCR-RFLP. Med Vet Entomol. 16(4): 461–464.
16. WHO (2013) Test procedures for insec-ticide resistance monitoring in malaria vector mosquitoes. Geneva: World Health Organization; 2013.
17. Abuelmaali SA, Elaagip AH, Basheer MA, Frah EA, Ahmed FTA, Elhaj HFA, Sei¬dahmed OME, David Weet-man D, Ha¬mid MMA (2013) Correc-tion: Impacts of Agricultural Practices on Insecticide Resistance in the Malar¬ia Vector Anoph¬eles arabiensis in Khar-toum State, Sudan. PLoS One. 8(12): 10.137.
18. Trape JF, Tall A, Diagne N, Ndiath O, Ly AB, Faye J, Dieye-Ba F, Roucher C, Bouganali C, Badiane A, Sarr FD, Mazenot C, Touré-Baldé A, Raoult D, Druilhe P, Mercereau-Puijalon O, Rogier C, Sokhna C (2011) Malaria morbidity and pyrethroid resistance af-ter the introduction of insecticide-treated bednets and artemisinin-based combination therapies: a longitudinal study. Lancet Infect Dis. 11(12): 925–932.
19. West Africa Agricultural Productivity Pro¬gramme (2013) Report of a baseline study on status of use, registration and regulations of pesticides in Nigeria. Available at: https://www.slideshare.net/waapp-nigeria/final-version-of-baseline-studies-on-pestticide-use-submiited-to-waapp2013a1.
20. World Health Organization (2016) World Malaria Report. Geneva: World Health Organization.
21. Kamau L, Agai D, Matoke D, Wachira L, Gikandi G, Vulule JM (2007) Status of Insecticide Susceptibility in Anoph-eles gambiae sensu lato and Anopheles fu¬nes¬tus Mosquitoes from Western Kenya.
J Insect Sci. 8: 11.
22. Seidahmed OME, Abdelmajed MA, Mus¬tafa MS, Mnzava AP (2012) Insec-ti¬cide Susceptibility Status of the Ma-lar¬ia Vector Anopheles arabiensis in Khar¬toum City, Sudan: Differences be-tween Urban and Periurban Areas. Eastern Medit Health J. 18(7): 769–776.
23. Protopopoff N, Matowo J, Malima R, Kavishe R, Kaaya R, Wright A, West PA, Kleinschmidt I, Kisinza W, Mosha, FW, Rowland M (2013) High Level of Resistance in the Mosquito Anopheles gambiae to Pyrethroids In-secticides and Reduced Susceptibility to Bendi¬o¬carb in North-western Tan-zania. Malaria J. 12: 149.
24. Umar A, Kabir BGJ, Amajoh CN, Inya-ma PU, Ordu DA, Barde, AA, Misau AA, Sambo ML, Babuga U, Kobi M, Jabbdo MA (2014) Susceptibility Test of Female Anopheles Mosqui¬toes to Ten Insecticides for Indoor Re¬sidual Spraying (IRS) Baseline Data Collec-tion in Northeastern Nigeria. J Entomol Nematology. 6(7): 98–103.
25. Aïkpon R, Sezonlin M, Ossè R, Akogbe-to M (2014) Evidence of Multiple Mechanisms Providing Carbamate and Organophosphate Resistance in Field A. gambiae Population from Atacora in Benin. Parasit Vect. 7: 568.
26. Aïzoun N, Ossè R, Azondekon R, Alia Oussou O, Gnanguenon V, Aikpon R, Padonou GG, Akogbéto M (2013) Com¬parison of the Standard WHO Susceptibility Tests and the CDC Bot-tle Bioassay for the Determination of Insecticide Susceptibility in Malaria Vectors and their Correlation with Bio-chemical and Molecular Biology As-says in Benin, West Africa. Parasit Vect. 6: 147.
27. Aïkpon R, Ossè R, Govoetchan R, Sovi A, Oké-Agbo F, Akogbéto MC (2013) Entomological Baseline Data on Ma¬lar-ia Transmission and Susceptibility of Anopheles gambiae to Insecticides in Preparation for Indoor Residual Spray-ing (IRS) in Atacora, (Benin). Global J Acarology. Parasit Vect Biol. 1(1): 035–044.
28. Coetzee M (2004) Distribution of the Af-rican malaria vectors of the Anophe¬les gambiae complex. Am J Trop Med Hyg. 70: 103–104.
29. Oduola AO, Adelaja OJ, Aiyegbusi ZO, Tola M, Obembe A, Ande AT, Awolo-la S (2016) Dynamics of Anopheline vector species composition and report-ed malaria cases during rain and dry seasons in two selected communities of Kwara State. Nig J Parasitol. 37(2): 157–163.
30. Abdu HU, Spiers AJ, Simona H, Dauda MM, Deeni YY (2017) Malaria vectors resistance to commonly used insecti-cides in the control of Malaria in Bichi, Northern Nigeria. Bayero J Pure and App Sci. 10(1): 1–6.
31. Onyabe DY, Conn JE (2001) The distri-bution of two major malaria vectors, Anopheles gambiae and Anopheles arabiensis, in Nigeria. Mem Inst Os-waldo Cruz. 96(8): 1081–1084.
32. Awolola TS, Oyewole IO, Amajoh CN, Idowu ET, Ajayi MB, Oduola A, Manafa OU, Ibrahim K, Koekemoer LL (2005) Distribution of the molecu-lar forms of Anopheles gambiae and pyrethroid knock¬down resistance gene in Nigeria. Acta Trop. (95): 204–209.
2. World Health Organization (2012) World Malaria Report 2012.
3. Oduola AO, Olojede JB, Ashiegbu CO, Adeogun AO, Otubanjo OA, Awolola TS (2010) High Level of DDT Re-sistance in the Malaria Mosquito: Anopheles gam¬biae s.l. from Rural, Semi Urban and Ur¬ban Communities in Nigeria. J Rural and Trop Pub Health. 9: 114–120.
4. Ibrahim KT, Popoola KO, Adewuyi OR, Adeogun AO, Oricha AK (2013) Sus-ceptibility of Anopheles gambiae sensu lato to permethrin, deltamethrin and ben¬diocarb in Ibadan city, southwest Nigeria. Curr Res J Bio Sci. 5(2): 42–44.
5. Okorie PN, Ademowo OG, Irving H, Kelly-Hope LA, Wondji CS (2015) In-sec¬ti¬cide Susceptibility of Anopheles coluzzii and Anopheles gambiae Mos-quitoes in Ibadan, Southwest Nigeria. Med Vet Entomol. 29: 44–50.
6. Djouaka RJ, Atoyebi SM, Tchigossou GM, Riveron JM, Irving H, Akoton R, Kusi¬mo MO, Bakare AA, Wondji CS (2016) Evidence of a multiple insecti-cide resistance in the malaria vector Anopheles funestus in South West Ni-geria. Malaria J. 15: 565.
7. Nwankwo EN, Okorie PN, Acha CT, Okonk¬wo OE, Nwangwu UC, Ezihe EK (2017) Insecticide resistance in Anopheles gambiae s.l. mosquitoes in Awka, Anambra State, Southeast Nige-ria. J Mosq Res. 7(5): 32–37.
8. Adeogun AO, Popoola KO, Oduola AO, Olakiigbe AK, Awolola TS (2017) High level of DDT resistance and re-duced susceptibility to deltamethrin in Anoph¬e¬les gambiae, Anopheles coluzzi, and Anopheles arabiensis from Urban Com¬munities in Oyo State, South-West Nigeria. J Mosq Res. 7(16): 125–133.
9. Ibrahim SS, Yayo AM, Tukur Z, Irving H, Wondji CS (2014) High frequency of kdr L1014F is associated with pyre-throid resistance in Anopheles coluzzii in Sudan savannah of northern Nigeria. BMC Infectious Diseases. 14: 441.
10. Alhassan AJ, Sule MS, Dan Gambo MA, Yayo AM, Safiyanu M, Sulaiman D (2015) Detoxification Enzymes Activi-ties in DDT and Bendiocarb resistant and susceptible malarial vector (Anoph-eles gambiae) breed in Auyo residential and irrigation sites, north¬west Nigeria European Sci Journal. 11: 9.
11. Abdu HU, Manu YA, Deeni YY (2017) Susceptibility status of Anopheles gam-biae complex to insecticides com¬mon¬ly used for malaria control in Northern Nigeria. Int J Scientific Tech Res. 6(6): 47–54.
12. Gillies M, De Meillon B (1968) The Anophe¬linae of Africa South of the Sa-hara (Ethiopian zoogeographical re-gion). Pub South Afr Inst for Med Res. 54: 343.
13. Gillies MT, Coetzee M (1987) A Sup¬ple-ment to the Anophelinae of Africa South of the Sahara. A Pub South Afr Inst for Med Res. 55: 33–81.
14. Scott JA, Brogon WG, Collins FH (1993) Identification of Single Speci-men of the Anopheles Complex by Pol-ymerase Chain Reaction. Am J Trop Med Hyg.
49: 520–529.
15. Fanello C, Santolamazza F, Della Torre A (2002) Simultaneous identification of species and molecular forms of the Anopheles gambiae complex by PCR-RFLP. Med Vet Entomol. 16(4): 461–464.
16. WHO (2013) Test procedures for insec-ticide resistance monitoring in malaria vector mosquitoes. Geneva: World Health Organization; 2013.
17. Abuelmaali SA, Elaagip AH, Basheer MA, Frah EA, Ahmed FTA, Elhaj HFA, Sei¬dahmed OME, David Weet-man D, Ha¬mid MMA (2013) Correc-tion: Impacts of Agricultural Practices on Insecticide Resistance in the Malar¬ia Vector Anoph¬eles arabiensis in Khar-toum State, Sudan. PLoS One. 8(12): 10.137.
18. Trape JF, Tall A, Diagne N, Ndiath O, Ly AB, Faye J, Dieye-Ba F, Roucher C, Bouganali C, Badiane A, Sarr FD, Mazenot C, Touré-Baldé A, Raoult D, Druilhe P, Mercereau-Puijalon O, Rogier C, Sokhna C (2011) Malaria morbidity and pyrethroid resistance af-ter the introduction of insecticide-treated bednets and artemisinin-based combination therapies: a longitudinal study. Lancet Infect Dis. 11(12): 925–932.
19. West Africa Agricultural Productivity Pro¬gramme (2013) Report of a baseline study on status of use, registration and regulations of pesticides in Nigeria. Available at: https://www.slideshare.net/waapp-nigeria/final-version-of-baseline-studies-on-pestticide-use-submiited-to-waapp2013a1.
20. World Health Organization (2016) World Malaria Report. Geneva: World Health Organization.
21. Kamau L, Agai D, Matoke D, Wachira L, Gikandi G, Vulule JM (2007) Status of Insecticide Susceptibility in Anoph-eles gambiae sensu lato and Anopheles fu¬nes¬tus Mosquitoes from Western Kenya.
J Insect Sci. 8: 11.
22. Seidahmed OME, Abdelmajed MA, Mus¬tafa MS, Mnzava AP (2012) Insec-ti¬cide Susceptibility Status of the Ma-lar¬ia Vector Anopheles arabiensis in Khar¬toum City, Sudan: Differences be-tween Urban and Periurban Areas. Eastern Medit Health J. 18(7): 769–776.
23. Protopopoff N, Matowo J, Malima R, Kavishe R, Kaaya R, Wright A, West PA, Kleinschmidt I, Kisinza W, Mosha, FW, Rowland M (2013) High Level of Resistance in the Mosquito Anopheles gambiae to Pyrethroids In-secticides and Reduced Susceptibility to Bendi¬o¬carb in North-western Tan-zania. Malaria J. 12: 149.
24. Umar A, Kabir BGJ, Amajoh CN, Inya-ma PU, Ordu DA, Barde, AA, Misau AA, Sambo ML, Babuga U, Kobi M, Jabbdo MA (2014) Susceptibility Test of Female Anopheles Mosqui¬toes to Ten Insecticides for Indoor Re¬sidual Spraying (IRS) Baseline Data Collec-tion in Northeastern Nigeria. J Entomol Nematology. 6(7): 98–103.
25. Aïkpon R, Sezonlin M, Ossè R, Akogbe-to M (2014) Evidence of Multiple Mechanisms Providing Carbamate and Organophosphate Resistance in Field A. gambiae Population from Atacora in Benin. Parasit Vect. 7: 568.
26. Aïzoun N, Ossè R, Azondekon R, Alia Oussou O, Gnanguenon V, Aikpon R, Padonou GG, Akogbéto M (2013) Com¬parison of the Standard WHO Susceptibility Tests and the CDC Bot-tle Bioassay for the Determination of Insecticide Susceptibility in Malaria Vectors and their Correlation with Bio-chemical and Molecular Biology As-says in Benin, West Africa. Parasit Vect. 6: 147.
27. Aïkpon R, Ossè R, Govoetchan R, Sovi A, Oké-Agbo F, Akogbéto MC (2013) Entomological Baseline Data on Ma¬lar-ia Transmission and Susceptibility of Anopheles gambiae to Insecticides in Preparation for Indoor Residual Spray-ing (IRS) in Atacora, (Benin). Global J Acarology. Parasit Vect Biol. 1(1): 035–044.
28. Coetzee M (2004) Distribution of the Af-rican malaria vectors of the Anophe¬les gambiae complex. Am J Trop Med Hyg. 70: 103–104.
29. Oduola AO, Adelaja OJ, Aiyegbusi ZO, Tola M, Obembe A, Ande AT, Awolo-la S (2016) Dynamics of Anopheline vector species composition and report-ed malaria cases during rain and dry seasons in two selected communities of Kwara State. Nig J Parasitol. 37(2): 157–163.
30. Abdu HU, Spiers AJ, Simona H, Dauda MM, Deeni YY (2017) Malaria vectors resistance to commonly used insecti-cides in the control of Malaria in Bichi, Northern Nigeria. Bayero J Pure and App Sci. 10(1): 1–6.
31. Onyabe DY, Conn JE (2001) The distri-bution of two major malaria vectors, Anopheles gambiae and Anopheles arabiensis, in Nigeria. Mem Inst Os-waldo Cruz. 96(8): 1081–1084.
32. Awolola TS, Oyewole IO, Amajoh CN, Idowu ET, Ajayi MB, Oduola A, Manafa OU, Ibrahim K, Koekemoer LL (2005) Distribution of the molecu-lar forms of Anopheles gambiae and pyrethroid knock¬down resistance gene in Nigeria. Acta Trop. (95): 204–209.
| Files | ||
| Issue | Vol 13 No 1 (2019) | |
| Section | Original Article | |
| DOI | https://doi.org/10.18502/jad.v13i1.932 | |
| Keywords | ||
| Multiple Insecticide resistance Anopheles gambiae Gombe south Nigeria | ||
| Rights and permissions | |
|
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
How to Cite
1.
Oduola AO, Abba E, Adelaja O, Ande AT, Yoriyo KP, Awolola TS. Widespread Report of Multiple Insecticide Resistance in Anopheles gambiae s.l. Mosquitoes in Eight Communities in Southern Gombe, North-Eastern Nigeria. J Arthropod Borne Dis. 2018;13(1):50.
