First Report of Target Site Insensitivity in Pyrethroid Resistant Anopheles gambiae from Southern Guinea Savanna, Northern-Nigeria
-
Mustapha Ahmed-Yusuf
,
Hassan Vatandoost
,
Mohammad Ali Oshaghi
,
Ahmad Ali Hanafi-Bojd
,
Ahmad Ali Enayati
,
Rabiu Ibrahim Jalo
Abstract
Background: Malaria is a major public health problem and life threatening parasitic vector-borne disease. For the first time, we established and report the molecular mechanism responsible for Anopheles gambiae s.l. resistance to pyrethroids and DDT from Yamaltu Deba, Southern Guinea Savanna, Northern-Nigeria.
Methods: The susceptibility profile of An. gambiae s.l. to four insecticides (DDT 4%, bendiocarb 0.1%, malathion 5% and deltamethrin 0.05%) using 2–3 days old females from larvae collected from study area between August and November, 2018 was first established. Genomic DNA was then extracted from 318 mosquitoes using Livak DNA extraction protocol for specie identification and kdr genotyping. The mosquitoes were identified to species level and then 96 genotyped for L1014F and L1014S kdr target site mutations.
Results: The mosquitoes were all resistant to DDT, bendiocarb and deltamethrin but fully susceptible to malathion. An. coluzzii was found to be the dominant sibling species (97.8%) followed by An. arabiensis (1.9%) and An. gambiae s.s (0.3%). The frequency of the L1014F kdr mutation was relatively higher (83.3%) than the L1014S (39%) in the three species studied. The L1014F showed a genotypic frequency of 75% resistance (RR), 17% heterozygous (RS) and 8% susceptible (SS) with an allelic frequency of 87% RR and 13% SS while the L1014S showed a genotypic frequency of RR (16%), RS (38%) and SS (46%) with an allelic frequency of 40% RR and 60% SS, respectively.
Conclusion: This study reveals that both kdr mutations present simultaneously in Northern-Nigeria, however contribution of L1014F which is common in West Africa was more than twice of L1014S mutation found in East Africa.
1. Mohammed BR, Abdulsalam YM, Deeni YY (2015) Insecticide resistance to Anopheles spp. mosquitoes (Diptera: Culicidae) in Ni¬geria. A Review. Inter J Mosq Res. 2(3): 56–63.
2. Brown G, Nossal G (1986) Malaria, Yester-day, Today, and Tomorrow. Perspect Biol Med. 30(1): 65–76.
3. William GB, Janet C (1997) Heme peroxi-dase activity measured in single mosqui-toes identifies individuals expressing an elevated oxidase for insecticide re-sistance. J Am Mosq Control Assoc. 13(3): 233–237.
4. Scott JA (1995) The molecular genetics of resistance: resistance as a response to stress. Fla Entomol. 78(3): 399–404.
5. Weill M, Lutfalla G, Mogensen K, Chandre F, Berthomieu A, Berticat C, Pasteur N, Philips A, Fort P, Raymond M (2003) Comparative genomics: Insecticide re-sistance in mosquito vectors. Nature. 423 (6936): 136–140.
6. Davari B, Vatandoost H, Oshaghi MA, La-donni H, Enayati AA, Shaeghi M, Basse¬ri HR, Rassi Y, Hanafi-Bojd AA (2007) Selection of Anopheles stephensi with DDT and dieldrin and cross-resistance spec¬trum to pyrethroids and fipronil. Pest Biochem Physiol. 89(2): 97–103.
7. Limoee M, Enayati AA, Ladonni H, Vatan-doost H, Baseri H, Oshaghi MA (2007) Various mechanisms responsible for per-methrin metabolic resistance in seven field-collected strains of the German cock¬roach from Iran, Blattella germanica (L.) (Dictyoptera: Blattellidae). Pest Bio¬chem Physiol. 87 (2): 138–146.
8. Du W, Awolola T, Howell P, Koekemoer L, Brooke B, Benedict M, Coetzee M (2005) Independent mutations in the Rdl locus confer dieldrin resistance to Anopheles gambiae and An. arabiensis. Insect Mol Biol. 14(2): 179–183.
9. Hemingway J, Ranson H (2000) Insecticide resistance in insect vectors of human dis-ease. Annu Rev Entomol. 45(1): 371–391.
10. Kwiatkowska RM, Platt N, Poupardin R, Irving H, Dabire RK, Mitchell S, Jones CM (2013) Dissecting the mechanisms responsible for the multiple insecticide re¬sistance phenotype in Anopheles gam-bi¬ae s.s, M form, from Vallee du Kou, Burki¬na Faso. Gene. 519(1): 98–106.
11. Martinez Torres D, Chandre F, William¬son M, Darriet F, Berge JB, Devonshire AL, Guillet P, Pasteur N, Pauron D (1998) Molecular characterization of pyrethroid knockdown resistance (kdr) in the major malaria vector Anopheles gambiae s.s. Insect Mol Biol. 7(2): 179–184.
12. Ranson H, Abdallah H, Badolo A, Guelbeogo WM, Kerah-Hinzoumbé C, Yangalbé-Kal¬noné E, Falé Sagnon N, Simard F, Coet¬zee M (2009) Insecticide resistance in Anoph¬eles gambiae: data from the first year of a multi-country study highlight the extent of the problem. Malar J. 8(1): 299.
13. Habibu, Yayo A, Yusuf Y (2017) Suscep-ti¬bil¬ity status of Anopheles gambiae com¬plex to insecticides commonly used for malaria control in northern Nigeria. Int J Sci Technol Res. 6(6): 2277–8616.
14. Ibrahim SS, Manu YA, Tukur Z, Irving H, Wondji CS (2014) High frequency of kdr L1014F is associated with pyrethroid re¬sistance in Anopheles coluzzii in Sudan savannah of northern Nigeria. BMC In¬fect Dis. 14(1): 441–448.
15. Oduola AO, Idowu ET, Oyebola MK, Adeogun AO, Olojede JB, Otubanjo OA, Awolola TS (2012) Evidence of car¬ba¬mate resistance in urban populations of Anopheles gambiae ss mosquitoes re¬sistant to DDT and deltamethrin insecticides in Lagos, South-Western Nigeria. Parasite Vector. 5(1): 116.
16. Onyabe DY, Conn JE (2001) The distri¬bu-tion of two major malaria vectors, Anopheles gambiae and Anopheles arabiensis, in Ni¬geria. Mem Inst Oswaldo Cruz. 96(8): 1081–1084.
17. Coluzzi M, Sabatini A, Petrarca V, Di Deco M (1979) Chromosomal differentiation and adaptation to human environments in the Anopheles gambiae complex. Trans Roy
Soc Trop Med Hyg. 73(5): 483–497.
18. Safiyanu M, Alhassan A, Yayo A, Ib¬ra¬him S, Imam A, Abdullahi H (2019) Detec-tion of KDR l1014f mutation in pyre-throids susceptible Anopheles gambiae s.l. from Ladanai, Kano state, northwest Nigeria. Int J Mosq Res. 6(3): 10–15.
19. Ibrahim SS, Mukhtar MM, Datti JA, Ir-ving H, Kusimo MO, Tchapga W, Lawal N, Sambo F, Wondji CS (2019) Tem-poral escalation of pyrethroid resistance in the major malaria vector Anopheles coluzzii from Sahelo-Sudanian region of north¬ern Nigeria. Sci Rep. 9(1): 7395.
20. Mathias DK, Ochomo E, Atieli F, Ombok M, Bayoh MN, Olang G, Muhia D (2011) Spatial and temporal variation in the kdr allele L1014S in Anopheles gambiae s.s and phenotypic variability in suscep¬ti¬bil¬ity to insecticides in Western Kenya. Ma¬lar J. 10(1): 10.
21. Stump AD, Atieli FK, Vulule JM, Besan-sky NJ (2004) Dynamics of the pyre-throid knockdown resistance allele in western Kenyan populations of Anopheles gam¬biae in response to insecticide-treated bed net trials. Am J Trop Med Hyg. 70(6): 591–596.
22. Draw the map of nigeria showing the veg-etation zones. Available at: https://maps-nigeria.com/draw-the-map-of-nigeria-showing-vegetation-zone
23. Gombo state in Nigeria. Avialable at: https://gombestate.gov.ng/local-governments/
24. World Health Organization (1998) Test pro¬cedures for insecticide resistance moni¬tor¬ing in malaria vectors, bio-efficacy and persistence of insecticides on treated sur¬faces: report of the WHO informal con¬sul¬tation, Geneva: World Health Organ¬iza¬tion. p. 46.
25. World Health Organization (2016) Test procedures for insecticide resistance mon¬itoring in malaria vector mosquitoes. WHO, Geneva, p. 54.
26. Scott TW, Takken W, Knols BG, Boëte C (2002) The ecology of genetically modi-fied mosquitoes. Science. 298(5591): 117–119.
27. Livak KJ (1999) Allelic discrimination using fluorogenic probes and the 5′ nuclease assay. Genetic analysis: Biomol Eng. 14 (5–6): 143–149.
28. Gillies MT, De Meillon B (1968) The Anophe¬linae of Africa south of the Sa-hara. Publ S Afr Inst Med Res. 54: 1–343.
29. Gillies M, Coetzee M (1987) A supple-ment to the Anophelinae of Africa South of the Sahara. Publ S Afr Inst Med Res. 55: 1–143.
30. Ranson H, Jensen B, Vulule JM, Wang X, Hemingway J, Collins FH (2000) Identi-fcation of a point mutation in the volt-age-gated sodium channel gene of Ken-yan Anoheles gambiae associated with resistance to DDT and pyrethroids. In-sect Mol Biol. 9: 491–497
31. Abbott W (1987) A method of computing the effectiveness of an insecticide. J Am Mosq Control Assoc. 3(2): 302–326.
32. Olatunbosun-Oduola A, Abba E, Adelaja O, Taiwo-Ande A, Poloma-Yoriyo K, Sam¬son-Awolola T (2019) 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. 13(1): 50–61.
33. Baffour-Awuah S, Annan AA, Maiga-Ascofare O, Dieudonné SD, Adjei-Kusi P, Owusu-Dabo E (2016) Insecticide re-sistance in malaria vectors in Kumasi, Ghana. Parasite Vector. 9(1): 633.
34. Umar A, Kabir B, Amajoh C, Inyama P, Ordu D, Barde A, Misau A. Sambo ML, Babuga U, Kobi M, Jabbdo MA (2014) Susceptibility test of female Anopheles mosquitoes to ten insecticides for indoor residual spraying (IRS) baseline data col¬lection in Northeastern Nigeria. J Entomol Nematol. 6(7): 98–103.
35. Safiyanu M, Alhassan A, Abubakar A (2016) Detoxification enzymes activities in del¬tamethrin and bendiocarb resistant and susceptible malarial vectors (Anopheles gambiae) breeding in Bichi agricultural and residential sites, Kano state, Nige¬ria. Bayero J Pur Appl Sci. 9(1): 142–149.
36. Habibu A, Andrew JS, Hapca S, Mukhtar MD, Yusuf YD (2017) Malaria vectors resistance to commonly used insecti¬cides in the control of Malaria in Bichi, North-ern Nigeria. Bayero J Pur Appl Sci. 10 (1): 1–6.
37. 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 Niger Republic. Malar J. 18(1): 181.
38. Kabbale FG, Akol AM, Kaddu JB, Ma-tovu E, Kazibwe A, Yadouleton A, Ona¬pa A (2016) Molecular identification of Anopheles gambiae sensu stricto Giles (formerly Anopheles gambiae Savannah Form) in Kamuli District, Uganda. Afr J Biotechnol. 15(39): 2124–2131.
39. Oyewole I, Ogunnowo A, Ibidapo C, Okoh H, Awolola T, Adedayo M (2011) Epi¬de¬miology of malaria and insecticide resistance burden in Nigeria. J Public Health Epidemiol. l3(1): 6–12.
40. Lynd A, Weetman D, Barbosa S, Egyir Yawson A, Mitchell S, Pinto J, Hastings I (2010) Field, genetic, and modeling ap¬proaches show strong positive selection acting upon an insecticide resistance mu¬tation in Anopheles gambiae s.s. Mol Biol Evol. 27(5): 1117–1125.
41. Czeher C, Labbo R, Arzika I, Duchemin JB (2008) Evidence of increasing Leu-Phe knockdown resistance mutation in Anopheles gambiae from Niger follow-ing a nationwide long-lasting insecti-cide-treated nets implementation. Malar J. 7(1): 189.
42. Sharp BL, Ridl FC, Govender D, Kuklin-ski J, Kleinschmidt I (2007) Malaria vec-tor control by indoor residual insecticide spraying on the tropical island of Bioko, Equatorial Guinea. Malar J. 6(1): 52.
43. Awolola T, Brooke B, Koekemoer L, Coet¬zee M (2003) Absence of the kdr muta¬tion in the molecular ‘M’form suggests different pyrethroid resistance mecha¬nisms in the malaria vector mosquito Anophe¬les gambiae s.s. Trop Med Int Health. 8(5): 420–422.
44. Protopopoff N, Verhaeghen K, Van Bortel W, Roelants P, Marcotty T, Baza D, D'Ales¬sandro U, Coosemans MA (2008) A significant increase in kdr in Anophe¬les gambiae is associated with an inten¬sive vector control intervention in Bu¬rundi highlands. Trop Med Int Health. 13(12): 1479–1487.
45. Verhaeghen K, Van Bortel W, Roelants P, Okello PE, Talisuna A, Coosemans M (2010) Spatio-temporal patterns in kdr frequency in permethrin and DDT re-sistant Anopheles gambiae s.s from Ugan¬da. Am J Trop Med Hyg. 82(4): 566–573.
46. Gorouhi MA, Vatandoost H, Oshaghi MA, Raeisi A, Enayati AA, Mirhendi H, Hanafi-Bojd AA, Abai MR, Salim-Abadi Y, Rafi F (2016) Current Susceptibility Status of Anopheles stephensi (Diptera: Culicidae) to Different Imagicides in a Malarious Area, Southeastern of Iran. J Arthropod Borne Dis. 10(4): 493–500.
2. Brown G, Nossal G (1986) Malaria, Yester-day, Today, and Tomorrow. Perspect Biol Med. 30(1): 65–76.
3. William GB, Janet C (1997) Heme peroxi-dase activity measured in single mosqui-toes identifies individuals expressing an elevated oxidase for insecticide re-sistance. J Am Mosq Control Assoc. 13(3): 233–237.
4. Scott JA (1995) The molecular genetics of resistance: resistance as a response to stress. Fla Entomol. 78(3): 399–404.
5. Weill M, Lutfalla G, Mogensen K, Chandre F, Berthomieu A, Berticat C, Pasteur N, Philips A, Fort P, Raymond M (2003) Comparative genomics: Insecticide re-sistance in mosquito vectors. Nature. 423 (6936): 136–140.
6. Davari B, Vatandoost H, Oshaghi MA, La-donni H, Enayati AA, Shaeghi M, Basse¬ri HR, Rassi Y, Hanafi-Bojd AA (2007) Selection of Anopheles stephensi with DDT and dieldrin and cross-resistance spec¬trum to pyrethroids and fipronil. Pest Biochem Physiol. 89(2): 97–103.
7. Limoee M, Enayati AA, Ladonni H, Vatan-doost H, Baseri H, Oshaghi MA (2007) Various mechanisms responsible for per-methrin metabolic resistance in seven field-collected strains of the German cock¬roach from Iran, Blattella germanica (L.) (Dictyoptera: Blattellidae). Pest Bio¬chem Physiol. 87 (2): 138–146.
8. Du W, Awolola T, Howell P, Koekemoer L, Brooke B, Benedict M, Coetzee M (2005) Independent mutations in the Rdl locus confer dieldrin resistance to Anopheles gambiae and An. arabiensis. Insect Mol Biol. 14(2): 179–183.
9. Hemingway J, Ranson H (2000) Insecticide resistance in insect vectors of human dis-ease. Annu Rev Entomol. 45(1): 371–391.
10. Kwiatkowska RM, Platt N, Poupardin R, Irving H, Dabire RK, Mitchell S, Jones CM (2013) Dissecting the mechanisms responsible for the multiple insecticide re¬sistance phenotype in Anopheles gam-bi¬ae s.s, M form, from Vallee du Kou, Burki¬na Faso. Gene. 519(1): 98–106.
11. Martinez Torres D, Chandre F, William¬son M, Darriet F, Berge JB, Devonshire AL, Guillet P, Pasteur N, Pauron D (1998) Molecular characterization of pyrethroid knockdown resistance (kdr) in the major malaria vector Anopheles gambiae s.s. Insect Mol Biol. 7(2): 179–184.
12. Ranson H, Abdallah H, Badolo A, Guelbeogo WM, Kerah-Hinzoumbé C, Yangalbé-Kal¬noné E, Falé Sagnon N, Simard F, Coet¬zee M (2009) Insecticide resistance in Anoph¬eles gambiae: data from the first year of a multi-country study highlight the extent of the problem. Malar J. 8(1): 299.
13. Habibu, Yayo A, Yusuf Y (2017) Suscep-ti¬bil¬ity status of Anopheles gambiae com¬plex to insecticides commonly used for malaria control in northern Nigeria. Int J Sci Technol Res. 6(6): 2277–8616.
14. Ibrahim SS, Manu YA, Tukur Z, Irving H, Wondji CS (2014) High frequency of kdr L1014F is associated with pyrethroid re¬sistance in Anopheles coluzzii in Sudan savannah of northern Nigeria. BMC In¬fect Dis. 14(1): 441–448.
15. Oduola AO, Idowu ET, Oyebola MK, Adeogun AO, Olojede JB, Otubanjo OA, Awolola TS (2012) Evidence of car¬ba¬mate resistance in urban populations of Anopheles gambiae ss mosquitoes re¬sistant to DDT and deltamethrin insecticides in Lagos, South-Western Nigeria. Parasite Vector. 5(1): 116.
16. Onyabe DY, Conn JE (2001) The distri¬bu-tion of two major malaria vectors, Anopheles gambiae and Anopheles arabiensis, in Ni¬geria. Mem Inst Oswaldo Cruz. 96(8): 1081–1084.
17. Coluzzi M, Sabatini A, Petrarca V, Di Deco M (1979) Chromosomal differentiation and adaptation to human environments in the Anopheles gambiae complex. Trans Roy
Soc Trop Med Hyg. 73(5): 483–497.
18. Safiyanu M, Alhassan A, Yayo A, Ib¬ra¬him S, Imam A, Abdullahi H (2019) Detec-tion of KDR l1014f mutation in pyre-throids susceptible Anopheles gambiae s.l. from Ladanai, Kano state, northwest Nigeria. Int J Mosq Res. 6(3): 10–15.
19. Ibrahim SS, Mukhtar MM, Datti JA, Ir-ving H, Kusimo MO, Tchapga W, Lawal N, Sambo F, Wondji CS (2019) Tem-poral escalation of pyrethroid resistance in the major malaria vector Anopheles coluzzii from Sahelo-Sudanian region of north¬ern Nigeria. Sci Rep. 9(1): 7395.
20. Mathias DK, Ochomo E, Atieli F, Ombok M, Bayoh MN, Olang G, Muhia D (2011) Spatial and temporal variation in the kdr allele L1014S in Anopheles gambiae s.s and phenotypic variability in suscep¬ti¬bil¬ity to insecticides in Western Kenya. Ma¬lar J. 10(1): 10.
21. Stump AD, Atieli FK, Vulule JM, Besan-sky NJ (2004) Dynamics of the pyre-throid knockdown resistance allele in western Kenyan populations of Anopheles gam¬biae in response to insecticide-treated bed net trials. Am J Trop Med Hyg. 70(6): 591–596.
22. Draw the map of nigeria showing the veg-etation zones. Available at: https://maps-nigeria.com/draw-the-map-of-nigeria-showing-vegetation-zone
23. Gombo state in Nigeria. Avialable at: https://gombestate.gov.ng/local-governments/
24. World Health Organization (1998) Test pro¬cedures for insecticide resistance moni¬tor¬ing in malaria vectors, bio-efficacy and persistence of insecticides on treated sur¬faces: report of the WHO informal con¬sul¬tation, Geneva: World Health Organ¬iza¬tion. p. 46.
25. World Health Organization (2016) Test procedures for insecticide resistance mon¬itoring in malaria vector mosquitoes. WHO, Geneva, p. 54.
26. Scott TW, Takken W, Knols BG, Boëte C (2002) The ecology of genetically modi-fied mosquitoes. Science. 298(5591): 117–119.
27. Livak KJ (1999) Allelic discrimination using fluorogenic probes and the 5′ nuclease assay. Genetic analysis: Biomol Eng. 14 (5–6): 143–149.
28. Gillies MT, De Meillon B (1968) The Anophe¬linae of Africa south of the Sa-hara. Publ S Afr Inst Med Res. 54: 1–343.
29. Gillies M, Coetzee M (1987) A supple-ment to the Anophelinae of Africa South of the Sahara. Publ S Afr Inst Med Res. 55: 1–143.
30. Ranson H, Jensen B, Vulule JM, Wang X, Hemingway J, Collins FH (2000) Identi-fcation of a point mutation in the volt-age-gated sodium channel gene of Ken-yan Anoheles gambiae associated with resistance to DDT and pyrethroids. In-sect Mol Biol. 9: 491–497
31. Abbott W (1987) A method of computing the effectiveness of an insecticide. J Am Mosq Control Assoc. 3(2): 302–326.
32. Olatunbosun-Oduola A, Abba E, Adelaja O, Taiwo-Ande A, Poloma-Yoriyo K, Sam¬son-Awolola T (2019) 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. 13(1): 50–61.
33. Baffour-Awuah S, Annan AA, Maiga-Ascofare O, Dieudonné SD, Adjei-Kusi P, Owusu-Dabo E (2016) Insecticide re-sistance in malaria vectors in Kumasi, Ghana. Parasite Vector. 9(1): 633.
34. Umar A, Kabir B, Amajoh C, Inyama P, Ordu D, Barde A, Misau A. Sambo ML, Babuga U, Kobi M, Jabbdo MA (2014) Susceptibility test of female Anopheles mosquitoes to ten insecticides for indoor residual spraying (IRS) baseline data col¬lection in Northeastern Nigeria. J Entomol Nematol. 6(7): 98–103.
35. Safiyanu M, Alhassan A, Abubakar A (2016) Detoxification enzymes activities in del¬tamethrin and bendiocarb resistant and susceptible malarial vectors (Anopheles gambiae) breeding in Bichi agricultural and residential sites, Kano state, Nige¬ria. Bayero J Pur Appl Sci. 9(1): 142–149.
36. Habibu A, Andrew JS, Hapca S, Mukhtar MD, Yusuf YD (2017) Malaria vectors resistance to commonly used insecti¬cides in the control of Malaria in Bichi, North-ern Nigeria. Bayero J Pur Appl Sci. 10 (1): 1–6.
37. 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 Niger Republic. Malar J. 18(1): 181.
38. Kabbale FG, Akol AM, Kaddu JB, Ma-tovu E, Kazibwe A, Yadouleton A, Ona¬pa A (2016) Molecular identification of Anopheles gambiae sensu stricto Giles (formerly Anopheles gambiae Savannah Form) in Kamuli District, Uganda. Afr J Biotechnol. 15(39): 2124–2131.
39. Oyewole I, Ogunnowo A, Ibidapo C, Okoh H, Awolola T, Adedayo M (2011) Epi¬de¬miology of malaria and insecticide resistance burden in Nigeria. J Public Health Epidemiol. l3(1): 6–12.
40. Lynd A, Weetman D, Barbosa S, Egyir Yawson A, Mitchell S, Pinto J, Hastings I (2010) Field, genetic, and modeling ap¬proaches show strong positive selection acting upon an insecticide resistance mu¬tation in Anopheles gambiae s.s. Mol Biol Evol. 27(5): 1117–1125.
41. Czeher C, Labbo R, Arzika I, Duchemin JB (2008) Evidence of increasing Leu-Phe knockdown resistance mutation in Anopheles gambiae from Niger follow-ing a nationwide long-lasting insecti-cide-treated nets implementation. Malar J. 7(1): 189.
42. Sharp BL, Ridl FC, Govender D, Kuklin-ski J, Kleinschmidt I (2007) Malaria vec-tor control by indoor residual insecticide spraying on the tropical island of Bioko, Equatorial Guinea. Malar J. 6(1): 52.
43. Awolola T, Brooke B, Koekemoer L, Coet¬zee M (2003) Absence of the kdr muta¬tion in the molecular ‘M’form suggests different pyrethroid resistance mecha¬nisms in the malaria vector mosquito Anophe¬les gambiae s.s. Trop Med Int Health. 8(5): 420–422.
44. Protopopoff N, Verhaeghen K, Van Bortel W, Roelants P, Marcotty T, Baza D, D'Ales¬sandro U, Coosemans MA (2008) A significant increase in kdr in Anophe¬les gambiae is associated with an inten¬sive vector control intervention in Bu¬rundi highlands. Trop Med Int Health. 13(12): 1479–1487.
45. Verhaeghen K, Van Bortel W, Roelants P, Okello PE, Talisuna A, Coosemans M (2010) Spatio-temporal patterns in kdr frequency in permethrin and DDT re-sistant Anopheles gambiae s.s from Ugan¬da. Am J Trop Med Hyg. 82(4): 566–573.
46. Gorouhi MA, Vatandoost H, Oshaghi MA, Raeisi A, Enayati AA, Mirhendi H, Hanafi-Bojd AA, Abai MR, Salim-Abadi Y, Rafi F (2016) Current Susceptibility Status of Anopheles stephensi (Diptera: Culicidae) to Different Imagicides in a Malarious Area, Southeastern of Iran. J Arthropod Borne Dis. 10(4): 493–500.
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| Issue | Vol 14 No 3 (2020) | |
| Section | Original Article | |
| DOI | https://doi.org/10.18502/jad.v14i3.4556 | |
| Keywords | ||
| Anopheles gambiae s Insecticide resistance Northern Nigeria Voltage-gated sodium channels (VGSC) | ||
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How to Cite
1.
Ahmed-Yusuf M, Vatandoost H, Oshaghi MA, Hanafi-Bojd AA, Enayati AA, Jalo RI. First Report of Target Site Insensitivity in Pyrethroid Resistant Anopheles gambiae from Southern Guinea Savanna, Northern-Nigeria. J Arthropod Borne Dis. 2020;14(3):228–238.
