Susceptibility Status of Several Field-Collected German Cock-roaches (Blattella germanica) to a Pyrethroid Insecticide and Molecular Detection of Knockdown Resistance (kdr)
Abstract
Abstract
Background: High frequency of insecticide used to control German cockroaches may lead to insecticide resistance development. We aimed to compare the level of insecticide resistance and heterogeneity in insecticide resistance of field-collected German cockroaches in eight selected zones of Mashhad City, Razavi Khorasan Province, Iran.
Methods: The present study was conducted from October 2019 to May 2021. Adult and nymphs of German cockroaches were collected from infested restaurants or hotels in eight zones of Mashhad City and then colonized in an insectarium. The cockroaches were subjected to bioassay against cypermethrin insecticide. In addition, the genomic DNA of each cockroach population was analyzed in the region where the kdr mutations reside in the German cockroach.
Results: The LT50 values against cypermethrin in the susceptible strain (SS) and eight field-collected strains so varied from 17.52 to 95.36 min. The resistance ratio of the strains was also different in response to the insecticide. The similarity of multiple sequence alignments at the amino acid level was 97.5%-100%. An exon 20 transversion mutation and a nonsynonymous substitution were found. The L1014F substitution was detected in 83.4% of the cockroach samples.
Discussion: The field-collected strains were resistant to cypermethrin at different levels. Furthermore, the molecular study confirms the heterogeneity in the level of resistance among eight strains. Therefore, eight strains might have a different history of insecticide treatment.
1. Gore JC, Schal C (2007). Cockroach allergen biology and mitigation in the indoor en-vironment. Annu Rev Entomol, 52:439-63.
2. Mengoni SL, Alzogaray RA (2018). Deltame-thrin-resistant German cockroaches are less sensitive to the insect repellents DEET and IR3535 than non-resistant individuals. J Econ Entomol, 111(2):836-43.
3. Shahraki GH, Parhizkar S, Nejad ARS (2013). Cockroach infestation and factors affecting the estimation of cockroach population in urban communities. Int J Zool, 2013: 649089.
4. Pridgeon JW, Liu N (2003). Overexpression of the cytochrome c oxidase subunit I gene
associated with a pyrethroid resistant strain of German cockroaches, Blattella germanica
(L.). Insect Biochem Mol Biol, 33(10):1043-8.
5. Pridgeon JW, Zhang L, Liu N (2003). Over-expression of CYP4G19 associated with a
pyrethroid-resistant strain of the German cockroach, Blattella germanica (L.). Gene,
314:157–63.
6. Rahimian AA, Hanafi-Bojd AA, Vatandoost H, et al (2019). A review on the insecticide
resistance of three species of cockroaches (Blattodea: Blattidae) in Iran. J Econ
Entomol, 112(1): 1–10.
7. Do DC, Zhao Y, Gao P (2016). Cockroach allergen exposure and risk of asthma. Al-lergy, 71(4):463–74.
8. Sookrung N, Chaicumpa W (2010). A revisit to cockroach allergens. Asian Pac J Allergy
Immunol, 28(2-3):95-106.
9. Menasria T, Moussa F, El-Hamza S, et al (2014). Bacterial load of German cock-roach
(Blattella germanica) found in hospital envi-ronment. Pathog Glob Health, 108(3):141-7.
10. Solomon F, Belayneh F, Kibru G, et al (2016). Vector potential of Blattella germani-ca (L.) (Dictyoptera: Blattidae) for medi-cally important bacteria at food handling establishments in Jimma town, Southwest Ethiopia. Biomed Res Int, 2016:e3490906.
11. Gondhalekar AD, Appel AG, Thomas GM, et al (2021). A review of alternative man-agement tactics employed for the control of various cockroach species (Order: Blattodea) in the USA. Insects, 12(6): 550.
12. Zha C, Wang C, Buckley B, et al(2018). Pest prevalence and evaluation of community-wide integrated pest management for re-ducing cockroach infestations and indoor insecticide residues. J Econ Entomol, 111(2):795-802.
13. Hemingway J, Dunbar SJ, Monro AG, et al (1993). Pyrethroid resistance in German
cockroaches (Dictyoptera, Blattelidae) - Resistance levels and underlying mecha-nisms. J
Econ Entomol, 86(6):1631-8.
14. Wang C, Scharf M, Bennett G (2004). Be-havioral and physiological resistance of the
German cockroach to Gel Baits (Blat-todea: Blattellidae). J Econ Entomol, 97:2067–72.
15. Zhu F, Lavine L, O’Neal S, et al (2016). In-secticide resistance and management strategies
in urban ecosystems. Insects, 7(1):2.
16. Whalon M, Mota-Sanchez D, Hollingworth R (2008). Global Pesticide Resistance in Arthropods. CABI Publishing, Cromwell Press, Trowbridge, UK, pp 169.
17. Lee SH, Choe DH, Rust MK, et al (2022). Reduced susceptibility towards commer-cial bait insecticides in field German cockroach (Blattodea: Ectobiidae) popula-tions from california. J Econ Entomol, 115(1):259-65.
18. Umeda K, Yano T, Hirano M (1988). Pyre-throid-resistance mechanism in German cockroach, Blattella germanica (Orthop-tera: Blattellidae). Appl Entomol Zool, 23(4):373-80.
19. Wu X, Appel AG (2017). Insecticide re-sistance of several field-collected German
cockroach (Dictyoptera: Blattellidae) strains. J Econ Entomol, 110(3):1203–9.
20. Scharf ME, Neal JJ, Bennett GW (1998). Changes of insecticide resistance levels and
detoxication enzymes following insecti-cide selection in the German cockroach, Blattella
germanica (L.). Pestic Biochem Physiol, 59(2):67–79.
21. De Vries ZC, Santangelo RG, Crissman J, et al (2019). Exposure risks and ineffective-ness of total release foggers (TRFs) used for cockroach control in residential set-tings. BMC Public Health, 19(1):96.
22. Georghiou GP (1972). The evolution of re-sistance to pesticides. Annu Rev Ecol Syst,
3(1):133–68.
23. Zalucki MP, Furlong MJ (2017). Behavior as a mechanism of insecticide resistance:
evaluation of the evidence. Curr Opin Insect Sci, 21:19–25.
24. Sparks TC, Lockwood JA, Byford RL, et al (1989). The role of behavior in insecticide
resistance. Pestic Sci, 26(4):383–99.
25. Hostetler ME, Brenner RJ (1994). Behavioral and physiological resistance to insecti-cides
in the German cockroach (Dictyoptera: Blattellidae): an experimental reevaluation. J
Econ Entomol, 87(4):885–93.
26. Dong K (1997). A single amino acid change in the para sodium channel protein is
associated with knockdown-resistance (kdr) to pyrethroid insecticides in Ger-man
cockroach. Insect Biochem Mol Biol, 27(2):93–100.
27. Zahraei-Ramazani AR, Saghafipour A, Vatandoost H (2018). Control of Ameri-can cockroach (Periplaneta americana) in municipal sewage disposal system, central Iran. J Arthropod Borne Dis, 12(2):172-9.
28. Hou W, Xin J, Lu H (2021). Resistance de-velopment characteristics of reared Ger-man
cockroach (Blattodea: Blattellidae) to chlorpyrifos. Sci Rep, 11(1):3505.
29. Bloomquist JR (1996). Ion channels as tar-gets for insecticides. Annu Rev Entomol,
41(1):163–90.
30. Busvine JR (1951). Mechanism of resistance to insecticide in houseflies. Nature,
168(4266):193–5.
31. Omotayo AI, Ande AT, Oduola AO, et al (2022). Multiple insecticide resistance mechanisms in urban population of Anopheles coluzzii (Diptera: culicidae) from Lagos, South-West Nigeria. Acta Trop, 227:e106291.
32. Scharf ME, Gondhalekar AD (2021). Insec-ticide resistance: perspectives on evolu-tion, monitoring, mechanisms and man-agement. In: Biology and Management of the German Cockroach, ed, C Wang, CY Lee, M Rust , CSIRO Publishing, Ordibehesht 13, pp 231-56.
33. Liu Z, Valles SM, Dong K (2000). Novel point mutations in the German cock-roach para
sodium channel gene are associated with knockdown resistance (kdr) to pyrethroid
insecticides. Insect Biochem Mol Biol, 30(10):991–7.
34. Ladonni H (2001). Evaluation of three methods for detecting permethrin re-sistance in adult and nymphal Blattella germanica (Dictyoptera: Blattellidae). J Econ Entomol, 94(3):694-7.
35. Nasirian H, Ladonni H, Shayeghi M, et al (2006). Duration of fipronil WHO glass jar method toxicity against susceptible and feral German cockroach strains. Pa-kistan J Biol Sci, 9(10):1955-1959.
36. Fardisi M, Gondhalekar AD, Scharf ME (2017). Development of diagnostic insec-ticide concentrations and assessment of insecticide susceptibility in German Cock-roach (Dictyoptera: Blattellidae) field strains collected from public housing. J Econ Entomol, 110(3):1210-1217.
37. Wadley FM (1962). Probit Analysis: a Statis-tical Treatment of the Sigmoid Response Curve. 2nd Ed. Cambridge Univ. Press, London, UK, pp 318.
38. Gholizadeh S, Nouroozi B, Ladonni H (2014). Molecular detection of knock-down
resistance (kdr) in Blattella germanica (Blat-todea: Blattellidae) from northwestern Iran.
J Med Entomol, 51(5):976–9.
39. Sievers F, Higgins DG (2018). Clustal omega for making accurate alignments of many
protein sequences. Protein Sci, 27(1):135–45.
40. Kumar S, Stecher G, Tamura K (2016). MEGA7: Molecular evolutionary genetics
analysis version 7.0 for bigger datasets. Mol Biol Evol, 33 (7):1870–4.
41. Farmani M, Basseri HR, Norouzi B, et al (2019). Ribosomal DNA internal tran-scribed
spacer 2 sequence analysis and phyloge-netic comparison of seven cockroach species in
northwestern Iran. BMC Res Notes, 12(1):53.
42. Ghaderi A, Baniardalani M, Basseri HR (2021). Level of pyrethroid-resistance as-sociated
with cytochrome P450 expression in German cockroach Blattella germanica (Blattodea:
Ectobiidae) in the field collected strains. J Arthropod Borne Dis, 15(2):152–61.
43. Nardini L, Christian RN, Coetzer N, et al (2012). Detoxification enzymes associated with
insecticide resistance in laboratory strains of Anopheles arabiensis of different geo-graphic
origin. Parasit Vectors, 5(1):113.
44. Valles SM, Dong K, Brenner RJ (2000). Mechanisms responsible for cyperme-thrin
resistance in a strain of German cock-roach, Blattella germanica. Pestic Biochem Phys-iol,
66(3):195–205.
45. Zhai J, Robinson WH (1992). Measuring cy-permethrin resistance in the German
cockroach (Orthoptera: Blattellidae). J Econ Entomol, 85(2):348–51.
46. Valles SM (2004). Effects of cypermethrin Sselection on expression of insecticide
Resistance Mechanisms in the German Cockroach (Blattaria: Blattellidae). J Ento-mol Sci,
39(1):84–93.
47. Brengues C, Hawkes NJ, Chandre F, et al (2003). Pyrethroid and DDT cross-resistance in
Aedes aegypti is correlated with novel muta-tions in the voltage-gated sodium channel
gene. Med Vet Entomol, 17(1):87–94.
48. Chang X, Zhong D, Lo E, et al (2016). Landscape genetic structure and evolu-tionary
genetics of insecticide resistance gene mutations in Anopheles sinensis. Parasit Vec-tors,
9:228.
2. Mengoni SL, Alzogaray RA (2018). Deltame-thrin-resistant German cockroaches are less sensitive to the insect repellents DEET and IR3535 than non-resistant individuals. J Econ Entomol, 111(2):836-43.
3. Shahraki GH, Parhizkar S, Nejad ARS (2013). Cockroach infestation and factors affecting the estimation of cockroach population in urban communities. Int J Zool, 2013: 649089.
4. Pridgeon JW, Liu N (2003). Overexpression of the cytochrome c oxidase subunit I gene
associated with a pyrethroid resistant strain of German cockroaches, Blattella germanica
(L.). Insect Biochem Mol Biol, 33(10):1043-8.
5. Pridgeon JW, Zhang L, Liu N (2003). Over-expression of CYP4G19 associated with a
pyrethroid-resistant strain of the German cockroach, Blattella germanica (L.). Gene,
314:157–63.
6. Rahimian AA, Hanafi-Bojd AA, Vatandoost H, et al (2019). A review on the insecticide
resistance of three species of cockroaches (Blattodea: Blattidae) in Iran. J Econ
Entomol, 112(1): 1–10.
7. Do DC, Zhao Y, Gao P (2016). Cockroach allergen exposure and risk of asthma. Al-lergy, 71(4):463–74.
8. Sookrung N, Chaicumpa W (2010). A revisit to cockroach allergens. Asian Pac J Allergy
Immunol, 28(2-3):95-106.
9. Menasria T, Moussa F, El-Hamza S, et al (2014). Bacterial load of German cock-roach
(Blattella germanica) found in hospital envi-ronment. Pathog Glob Health, 108(3):141-7.
10. Solomon F, Belayneh F, Kibru G, et al (2016). Vector potential of Blattella germani-ca (L.) (Dictyoptera: Blattidae) for medi-cally important bacteria at food handling establishments in Jimma town, Southwest Ethiopia. Biomed Res Int, 2016:e3490906.
11. Gondhalekar AD, Appel AG, Thomas GM, et al (2021). A review of alternative man-agement tactics employed for the control of various cockroach species (Order: Blattodea) in the USA. Insects, 12(6): 550.
12. Zha C, Wang C, Buckley B, et al(2018). Pest prevalence and evaluation of community-wide integrated pest management for re-ducing cockroach infestations and indoor insecticide residues. J Econ Entomol, 111(2):795-802.
13. Hemingway J, Dunbar SJ, Monro AG, et al (1993). Pyrethroid resistance in German
cockroaches (Dictyoptera, Blattelidae) - Resistance levels and underlying mecha-nisms. J
Econ Entomol, 86(6):1631-8.
14. Wang C, Scharf M, Bennett G (2004). Be-havioral and physiological resistance of the
German cockroach to Gel Baits (Blat-todea: Blattellidae). J Econ Entomol, 97:2067–72.
15. Zhu F, Lavine L, O’Neal S, et al (2016). In-secticide resistance and management strategies
in urban ecosystems. Insects, 7(1):2.
16. Whalon M, Mota-Sanchez D, Hollingworth R (2008). Global Pesticide Resistance in Arthropods. CABI Publishing, Cromwell Press, Trowbridge, UK, pp 169.
17. Lee SH, Choe DH, Rust MK, et al (2022). Reduced susceptibility towards commer-cial bait insecticides in field German cockroach (Blattodea: Ectobiidae) popula-tions from california. J Econ Entomol, 115(1):259-65.
18. Umeda K, Yano T, Hirano M (1988). Pyre-throid-resistance mechanism in German cockroach, Blattella germanica (Orthop-tera: Blattellidae). Appl Entomol Zool, 23(4):373-80.
19. Wu X, Appel AG (2017). Insecticide re-sistance of several field-collected German
cockroach (Dictyoptera: Blattellidae) strains. J Econ Entomol, 110(3):1203–9.
20. Scharf ME, Neal JJ, Bennett GW (1998). Changes of insecticide resistance levels and
detoxication enzymes following insecti-cide selection in the German cockroach, Blattella
germanica (L.). Pestic Biochem Physiol, 59(2):67–79.
21. De Vries ZC, Santangelo RG, Crissman J, et al (2019). Exposure risks and ineffective-ness of total release foggers (TRFs) used for cockroach control in residential set-tings. BMC Public Health, 19(1):96.
22. Georghiou GP (1972). The evolution of re-sistance to pesticides. Annu Rev Ecol Syst,
3(1):133–68.
23. Zalucki MP, Furlong MJ (2017). Behavior as a mechanism of insecticide resistance:
evaluation of the evidence. Curr Opin Insect Sci, 21:19–25.
24. Sparks TC, Lockwood JA, Byford RL, et al (1989). The role of behavior in insecticide
resistance. Pestic Sci, 26(4):383–99.
25. Hostetler ME, Brenner RJ (1994). Behavioral and physiological resistance to insecti-cides
in the German cockroach (Dictyoptera: Blattellidae): an experimental reevaluation. J
Econ Entomol, 87(4):885–93.
26. Dong K (1997). A single amino acid change in the para sodium channel protein is
associated with knockdown-resistance (kdr) to pyrethroid insecticides in Ger-man
cockroach. Insect Biochem Mol Biol, 27(2):93–100.
27. Zahraei-Ramazani AR, Saghafipour A, Vatandoost H (2018). Control of Ameri-can cockroach (Periplaneta americana) in municipal sewage disposal system, central Iran. J Arthropod Borne Dis, 12(2):172-9.
28. Hou W, Xin J, Lu H (2021). Resistance de-velopment characteristics of reared Ger-man
cockroach (Blattodea: Blattellidae) to chlorpyrifos. Sci Rep, 11(1):3505.
29. Bloomquist JR (1996). Ion channels as tar-gets for insecticides. Annu Rev Entomol,
41(1):163–90.
30. Busvine JR (1951). Mechanism of resistance to insecticide in houseflies. Nature,
168(4266):193–5.
31. Omotayo AI, Ande AT, Oduola AO, et al (2022). Multiple insecticide resistance mechanisms in urban population of Anopheles coluzzii (Diptera: culicidae) from Lagos, South-West Nigeria. Acta Trop, 227:e106291.
32. Scharf ME, Gondhalekar AD (2021). Insec-ticide resistance: perspectives on evolu-tion, monitoring, mechanisms and man-agement. In: Biology and Management of the German Cockroach, ed, C Wang, CY Lee, M Rust , CSIRO Publishing, Ordibehesht 13, pp 231-56.
33. Liu Z, Valles SM, Dong K (2000). Novel point mutations in the German cock-roach para
sodium channel gene are associated with knockdown resistance (kdr) to pyrethroid
insecticides. Insect Biochem Mol Biol, 30(10):991–7.
34. Ladonni H (2001). Evaluation of three methods for detecting permethrin re-sistance in adult and nymphal Blattella germanica (Dictyoptera: Blattellidae). J Econ Entomol, 94(3):694-7.
35. Nasirian H, Ladonni H, Shayeghi M, et al (2006). Duration of fipronil WHO glass jar method toxicity against susceptible and feral German cockroach strains. Pa-kistan J Biol Sci, 9(10):1955-1959.
36. Fardisi M, Gondhalekar AD, Scharf ME (2017). Development of diagnostic insec-ticide concentrations and assessment of insecticide susceptibility in German Cock-roach (Dictyoptera: Blattellidae) field strains collected from public housing. J Econ Entomol, 110(3):1210-1217.
37. Wadley FM (1962). Probit Analysis: a Statis-tical Treatment of the Sigmoid Response Curve. 2nd Ed. Cambridge Univ. Press, London, UK, pp 318.
38. Gholizadeh S, Nouroozi B, Ladonni H (2014). Molecular detection of knock-down
resistance (kdr) in Blattella germanica (Blat-todea: Blattellidae) from northwestern Iran.
J Med Entomol, 51(5):976–9.
39. Sievers F, Higgins DG (2018). Clustal omega for making accurate alignments of many
protein sequences. Protein Sci, 27(1):135–45.
40. Kumar S, Stecher G, Tamura K (2016). MEGA7: Molecular evolutionary genetics
analysis version 7.0 for bigger datasets. Mol Biol Evol, 33 (7):1870–4.
41. Farmani M, Basseri HR, Norouzi B, et al (2019). Ribosomal DNA internal tran-scribed
spacer 2 sequence analysis and phyloge-netic comparison of seven cockroach species in
northwestern Iran. BMC Res Notes, 12(1):53.
42. Ghaderi A, Baniardalani M, Basseri HR (2021). Level of pyrethroid-resistance as-sociated
with cytochrome P450 expression in German cockroach Blattella germanica (Blattodea:
Ectobiidae) in the field collected strains. J Arthropod Borne Dis, 15(2):152–61.
43. Nardini L, Christian RN, Coetzer N, et al (2012). Detoxification enzymes associated with
insecticide resistance in laboratory strains of Anopheles arabiensis of different geo-graphic
origin. Parasit Vectors, 5(1):113.
44. Valles SM, Dong K, Brenner RJ (2000). Mechanisms responsible for cyperme-thrin
resistance in a strain of German cock-roach, Blattella germanica. Pestic Biochem Phys-iol,
66(3):195–205.
45. Zhai J, Robinson WH (1992). Measuring cy-permethrin resistance in the German
cockroach (Orthoptera: Blattellidae). J Econ Entomol, 85(2):348–51.
46. Valles SM (2004). Effects of cypermethrin Sselection on expression of insecticide
Resistance Mechanisms in the German Cockroach (Blattaria: Blattellidae). J Ento-mol Sci,
39(1):84–93.
47. Brengues C, Hawkes NJ, Chandre F, et al (2003). Pyrethroid and DDT cross-resistance in
Aedes aegypti is correlated with novel muta-tions in the voltage-gated sodium channel
gene. Med Vet Entomol, 17(1):87–94.
48. Chang X, Zhong D, Lo E, et al (2016). Landscape genetic structure and evolu-tionary
genetics of insecticide resistance gene mutations in Anopheles sinensis. Parasit Vec-tors,
9:228.
| Files | ||
| Issue | Vol 53 No 4 (2024) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijph.v53i4.15573 | |
| Keywords | ||
| German cockroach Field strains Insecticide resistance Heterogeneity | ||
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How to Cite
1.
Dashti K, Gholizadeh S, Zaim M, Baniardalani M, Basseri H. Susceptibility Status of Several Field-Collected German Cock-roaches (Blattella germanica) to a Pyrethroid Insecticide and Molecular Detection of Knockdown Resistance (kdr). Iran J Public Health. 2024;53(4):957-966.
