Original Article

Assessing the Susceptibility Status of Mosquitoes (Diptera: Culicidae) in a Dirofilariasis Focus, Northwestern Iran


Background: Mosquitoes are considered as the vectors of dirofilariasis and some vector borne disease in Iran. The objective of this study was to determine the susceptibility level of the vectors to various insecticides recommended by WHO for any control measures in an endemic area in northwestern Iran.Methods: Mosquito larval and adult collections were carried out using different methods provided by WHO including dipping and hand catch techniques. The susceptibility level was assessed to DDT 4%, malathion 5%, propoxur 0.1%, deltamethrin 0.05% and lambda-cyhalothrin 0.05%.Results: Totally, 749 adults and 5060 larvae of Culicidae mosquitoes were collected comprising seven species of adult and larvae, including: Anopheles claviger, An. maculipennis, An. sacharovi, Culex hortensis, Cx. pipiens, Cx. theileri and Culiseta longiaerolata. Frequency of larvae and adults of An. maculipennis was very low, so susceptibility tests on this species did not performed. Results showed that Cx. theileri, Cs. longiaerolata and Cx. pipiens were resistant to DDT 4%, lambda-cyhalothrin 0.05%, and propoxur 0.1% whereas found tolerant to deltamethrin 0.05% and malathion 5%. The LT50 and LT90 values for five insecticides were calculated.Conclusion: We suggest the same study in different parts of the world to obtain the data due to bionomic and susceptibility status of dirofilariasis vectors. This information will help the health authorities for monitoring and evaluation of control measures.

Abai MR (1990) Fauna and seasonal activity of the sand flies and their animal res- ervoirs of visceral leishmaniasis in Meshgin Shahr County. [MSPH dis- sertation], School of Public Health, Teh- ran University of Medical Sciences, Iran.

Abai MR, Azari-Hamidian S, Ladonni H, Hakimi M, Mashhadi-Esmail K, Sheikh- zadeh K, Kousha A, Vatandoost H (2007) Fauna and checklist of mosqui- toes (Diptera: Culicidae) of East Azerbai- jan, northwestern Iran. Iran J Artropod- Borne Dis. 1: 27–33.

Abbott WS (1925) A method for computing the effect of an insecticide. J Econ Entomol. 18: 265–267.

Almeida APG, Galao RP, Sousa CA, Novo MT, Parreira R, Pinto J, Piedade J, Esteves A (2008) Potential mosquito vectors of arboviruses in Portugal: spe- cies, distribution, abundance and West Nile infection. Trans R Soc Trop Med Hyg. 102: 823–832.

Amin AM, Hemingway J (1998) Preliminary investigation of the mechanisms of DDT and pyrethroid resistance in Culex quinquefasciatus Say (Diptera: Culicidae) from Saudi Arabia. Bull Entomol Res.79: 361–366.

Anderson RC (2000) Nematod Parasites of Vertebrates. Their Development and Transmission. Vol. 2. Wallingford, CABI Press, Oxon , UK.

Aranda C, Panyello O, Eritja R, Costella J (1998) Canine filariasis importance and transmission in the BaixLlobregat area, Barcelona (Spain). Vet Parasitol. 77:267–275.

Ariamanesh MR (2000) Infection rate of Dirofilaria immitis on stray dogs in Urmia County. Proceedings of the Forth National Congress of Zoonotic diseases, Mashhad, pp. 189–190.

Ashrafi J, Eslami A, Shirani, D, Meshgi B, Mostofi S (2001) A study on the prev- alence, clinical findings and treatment of feline heartworm disease in Iran. University of Tehran, Iran. J Vet Fac Univ Tehran. 56(4): 21–23.

Atas AD, Ozcelik S, Saygi G (1997) The occurrence of helminth species in stray dogs, their prevalence and significance to public health in Sivas. Acta Parasitol Turcica. 21(3): 305–309.

Athari A (2003) Zoonotic subcutaneous dirofilariasis in Iran. Arch. Iran Med.6: 63–65.

Azari-Hamidian S, Yaghoobi-Ershadi MR, Javadian E (2000) The mosquito fauna (Diptera: Culicidae) in Rasht City. Modares J Med Sci. 3(2): 65–70 (in Persian with English abstract).

Azari-Hamidian S, Yaghoobi-Ershadi MR, Javadian E (2001) The distribiution and larval habitat characteristics of mosquitoes (Diptera: Culicidae) in Rasht City. Modares J Med Sci. 4(2): 96–87 (in Persian with English abstract).

Azari-Hamidian S, Yaghoobi-Ershadi MR, Javadian E, Mobedi I, Abai MR (2007) Review of dirofilariasis in Iran. J Med Fac Guilan Univ Med Sci. 15(60):102–113 (In Persian).

Azari-Hamidian S (2007) Checklist of Ira- nian mosquitoes (Diptera: Culicidae). J Vect Ecol. 32(2): 235–242.

Azari-Hamidian S, Harbach RE (2009) Keys to the adult females and fourth-instar larvae of the mosquitoes of Iran (Diptera: Culicidae) Zootaxa. 2078: 1–33.

Azari-Hamidian S, Yaghoobi-Ershadi MR, Javadian E, Abai MR, Mobedi I, Lin- ton YM, Harbach RE (2009) Distribu- tion and ecology of mosquitoes in a focus of dirofilariasis in northwestern Iran, with the first finding of filarial larvae in naturally infected local mos- quitoes. Med Vet Entomol. 23(2): 111–121.

Barr AR, Kabtman L (1951) Biometrical notes on the hybridization of Culex pipiens L. and C. quinquejasciatus Say. J Para- sit. 37: 419–420.

Ben Cheikh H, Ben Ali-Haouas Z, Marquine Mand Pasteur N (1998) Resistance to organophosphates and pyrethroid insec- ticides Culex pipiens (Diptera: Culicidae) from Tunisia. J Med Entomol. 35: 251–260.

Bisset JA, Rodriguez MM, Hemingway J, Diaz C, Small GJ, Ortiz E (1991) Malathion and pyrethroid resistance in Culex quinquefasciatus from Cuba: ef- ficacy of Pirimiphos-methyl in the pres- ence of at least three resistance mecha- nisms. Med Vet Entomol. 5: 223–228.

Bokai S, Moobedi A, Mohebali M, Hoseini H, Nadim A (1998) Study on prevalence of dirofilariosis in Meshkinshahr- North- west of Iran. J Fac Vet Med Tehran Univ. 53(1,2): 23 (in Persian with Eng- lish abstract).

Bouaziz A, Boudjelida H, Soltani N (2011) Toxicity and perturbation of the me- tabolite contents by a chitin synthesis inhibitor in the mosquito larvae of Culiseta longiareolata. Ann Biol Res.2(3): 134–143.

Chandre F, Darriet F, Darder M, Cuany A, Doannio JMC, Pasteur N, Guillet P (1998) Pyrethroid resistance in Culex quinquefasciatus from west Africa. Med Vet Entomol. 12: 359–366.

Chen KY, Liang S (1993) Blood chemistry of dogs with heart Worm in the Taipei area. J Chinese Soc Vet Sci. 19(2):130–136.

Bazzocchi C, Ceciliani F, Mc Call JW, Ricci I, Genchi C, Bandi C (2000) Antigenic role of the endosymbionts of filarial nematodes: IgG response against the Wolbachia surface protein in cats in- fected with Dirofilaria immitis. Proc R Soc Lond B.267: 2511–2516.

Dehghan H, Sadraei J, Moosa-Kazemi SH (2010) The morphological variations of Culex pipiens larvae (Diptera: Culicidae) in Yazd Province, central Iran. Iran J Arthropod-Borne Dis. 4(2): 42–49.

Enayati AA, Vatandoost H, Ladonni H, Townson H, Hemingway J (2003) Mo- lecular evidence for a Kdr-like py- rethroid resistance mechanism in the malaria vector mosquito Anopheles stephensi. Med Vet Entomol. 17: 138–144.

Farahnak A, Mobedi I, Mohamadi F (1998) Study of zoonotic helminthes of carni- vores in Khuzestan, Iran. Iran J Publ Health. 27(3–4): 15–20.

Fallah A, Onishi A, Mehdipour Zare N (2005) the prevalence of Dirofilaria immitis in Meshgin Shahr County. Pro- ceedings of the Fifth National Congress of parasitic disease in Iran, pp. 14–15.

Finney DJ (1971) Probit Analysis, 3rd Ed.Cambridge University Press, Cambridge, UK.

Genchi C, Rinaldi L, Cascone C, Mortarino M, Cringoli G (2005) Is heartworm dis- ease really spreading in Europe? Vet Parasitol. 133: 137–148.

Gjullin CM, Peters RF (1952) Abstract of recent studies of mosquito resistance to insecticides in California. Calif. Mos- quito Control Assoc. Ann Confr Proc and Papers -20:44-45.

Ghavami MB, Ladoni H (2005) Fauna and density of (Diptera: Culicidae) in Zanjan. J Zanjan Univ Med Sci Health Serv.13(53): 46–54.

Grieve RB, Lok JB, Glickman LT (1983) Epidemiology of canine heartworm in- fection. Epidemiol Rev. 5: 220–246.

Harbach RE (1985) Pictorial keys to the genera of mosquitoes, subgenera of Culex and the species of Culex (Culex) occurring in southwestern. Asia and Egypt, with a note on the subgeneric placement of Culex deserticola (Diptera: Culicidae): Mosq Syst. 17(2): 83–107.

Hatsushika R, Okino T, Shimizu M, Ohyama F (1997) The prevalence of dog heart worm (Dirofilariaimmitis) infection in stray dogs in Okayama, Kawasaki. Ja- pan Med J. 3(4): 75–83.

Isaak LW (1961) Review of insecticide re- sistance in Kern Mosquito Abatement District. In: Proceedings and Papers of the Twenty-nine Annual Conference of the California Mosquito Control Asso- ciation, Vol. 1. Visalia press, Cleveland, Ohio, USA, pp.105–106.

Jafari S, Gaur NS, Khaksar Z (1996) Preva- lence of Dirofilari aimmitis on dog of Fars province of Iran. J Appl Anim Res.9(1): 27–31.

Jamali R, HashemzadeFarhang H (1996) In- fection study to Dirofilaria immitis on stray dogs in the city of Tabriz. Pro- ceedings of the Third National Con- gress of zoonotic diseases, Mashhad, p. 179.

Jinfu W (1999) Resistance to deltamethrin in Culex pipiens pallens (Diptera: Culi- cidae) from Zhejiang, China. J Med Entomol. 36: 389–393.

Choi JS, Choi SY, Kim MK, Kim CH, Yeom BW, Park SH (2002) The first human case of hepatic dirofilariasis. J Korean Med Sci. 17: 686–690.

Katbeh Bader A, Khyami Horani H, Mohsen ZH (1999) Effect of temperature on the susceptibility of Culiseta longiareolata (Macquart) (Diptera: Culicidae) to two standard strains of biocontrol bacteria. J Appl Entomol. 123: 629–631

Khanmohammadi M, Fallah E, Reyhani rad S (2011) Epidemiological studies on fauna and prevalence of parasite hel- minthes on Red Fox (Vulpes vulpes) in Sarab district, East Azerbaijan Prov- ince, Iran. Ann Biol Res. 2(5): 246–251.

Lotfi MD (1970) Iranian species of genus Culex (Culicinae: Diptera). Bull Sot. Pathol Exotique. 63: 400–403.

Maraghi S, Rahdar M, Akbari H, Radmanesh M, Saberi AA (2006) Human diro- filariasis due to Dirofilaria repens in Ahvaz-Iran: a report of three cases. Pak J Med Sci. 22: 211–213.

Mattingly PF, Rozeboom LE, Knight KL, Laven H, Drummond FH, Christophers R, Shute PG (1951) The Culex pipiens complex, Trans. Roy Ent Sot Lond.102: 331–382.

McAbee RD, Kang KD, Stanich MA, Chris- tiansen JA, Wheelock CE, Inman AD, Hammock BD, Cornel AJ (2003) Pyrethroid tolerance in Culex pipiens pipiens var molestus from Marin County, California. Pest Manag Sci. 60: 359–368.

Meshgi B, Eslami A (2001) Study on filariosis of sheepdogs around of Tehran. J Fac Vet Med Tehran Univ. 55(4): 53–57 (In Persian).

Meshgi B, Eslami A, Ashrafi Helan J (2002) Epidemiological survey of blood filariae in rural and urban dogs of Tabriz. J Fac Vet Med Tehran Univ. 57(4): 59–63 (In Persian).

Montoya JA, Morales M, Ferrer O, Molina JM, Corbera JA (1998) the prevalence of Dirofilaria immitisin Gran Canaria, Canary Islands, Spain (1994–1996). Vet Parasitol. 75: 221–226.

Moosa Kazemi SH, Karimiana F, Davari B (2010) Culicinae mosquitoes in Sanandaj County, Kurdistan Province, western Iran. J Vector Borne Dis, 47: 103–107.

Moosa-Kazemi SH, Vatandoost H, Nikookar H, Fathian M (2009) Culicinae (Diptera: Culicidae) mosquitoes in Chabahar County, Sistan and Baluchistan Prov- ince, southeastern Iran. Iran J Arthro- pod-Borne Dis. 3(1): 29–35.

Moosa-Kazemi SH, Vatandoost H, Raeisi A, Akbarzadeh K (2007) Deltamethrin im- pregnated bed nets in a malaria control program in Chabahar, south-east Balu- chistan, Iran. Iran J Arthropod-Borne Dis. 1(1): 43–51.

Moosa-Kazemi SH, Zaim M, Zahra'i Ramezani A (2000) Funa and ecological study of culicidae mosquito in Lenjan area, Is- fahan Province. J Yasuj Uni Med Sci.5(17–18): 46–53.

Mousakazemi SH (1995) Fauna and ecology of culicidae mosquitoes (Diptera) in the region of Mobarake and ZarinShahr, Isfahan Province. [MSPH dissertation]. School of Public Health. Tehran Uni- versity of Medical Sciences, Iran.

Muller R (2002) Worms and Human disease.2nd Ed. CABI publication, Wallingford. Oxon, UK.

Mullen GR, Durden L (2009) Medical and Veterinary Entomology, Mosquitoes (Culicidae) Woodbridge A. Foster and Edward D Walter. Vol. 2. Elsevier, Burlington, pp. 207–260.

Nazari M, Janbakhsh B (2000) a survey of the susceptibility level of Culex theileri and Cx. pipiens to DDT, Dieldrin, Propoxur and Malathion in the south- ern area of Tehran. J Uromia Univ Med Sci. 11(1): 13–19.

Nikookar SH, Moosa-Kazemi SH, Oshaghi MA, Yaghoobi-Ershadi MR, Vatandoost H, Kianinasab A (2010) Species com- position and diversity of mosquitoes in Neka County, Mazandaran Province, northern Iran. Iran J Arthropod-Borne Dis. 4(2): 26–34.

Peribanez MA, Lucientes J, Arce S, Morales M, Castillo JA, Gracia MJ (2001) Histo- chemical differentiation of Dirofilaria immitis, Dirofilaria repens and Acantho- cheilonema dracunculoides microfilar- iae by staining with a commercial kit, Leucognost-SP. Vet Parasitol. 102: 173–175.

Radmanesh M, Saberi A, Maraghi S, Emad- Mostowfi N (2006) Dirofilaria repens: a dog parasite presenting as a paranasal subcutaneous nodule. Int J Dermatol.45: 477–478.

Ranjbar-Bahadori S, Eslami A (2005) Cam- parison of modified Knott and ELISA methods for diagnosis of dirofilariosis in dogs in Golestan Province and de- termining of its periodicity. The 20th International Conference of the World Association for the advancement of Veterinary Parasitology, Christchurch,

New Zealand, p. 249.

Ranjbar-Bahadori Sh, Eslami A, Meshgi B, Mohammad Mohtasham R (2005) Study on blood filaria of dogs in Tonekabon. J Fac Vet Med Tehran Univ. 60(4):Razm Arayi N, Ebrahimi M, Ameghi A (2000) Report of Dirofilaria immitis on wild carnivores in Northern of East Azerbaijan Province. Proceedings of the Fourth National Congress of Zoon- otic diseases, Mashhad, pp. 220–221.

Razmi Gh (1999) Study on situation of in- fection to dogs of Mashhad to types of filaria. J Fac Vet Med Tehran Univ.54(1): 5–7 (In Persian).

Rosa A, Ribicich M, Betti A, Kistermann N, Cardillo N, Basso N, Hallu R (2002) Prevalence of canine dirofilariosis in the city of Buenos Aires and its outskirts

(Argentina). Vet Parasitol. 109: 261–264. Reifur L, Thomaz-Soccol V, Montiani- Fer- reira F (2004) Epidemiological aspects

of filariosis in dogs on the coast of Pa- rana state, Brazil: with emphasis on Dirofilaria immitis. Vet Parasitol. 122:273–86.

Rodriguez M, Ortiz E, Bisset JA, Heming- way J, Saledo E (1993) Changes in malathion and pyrethroid resistance af- ter cypermethrin selection of Culex quinquefasciatus field populations of Cuba. Med Vet Entomol. 7: 117–121.

Siavashi MR, Masoud J (1995) Human cuta- neous dirofilariasis in Iran: a report of two cases. Iran J Med Sci. 20: 85–86.

Sadjjadi S, Mehrabani D, Oryan A (2004) Dirofilariosis of stray dogs in Shiraz Iran. J Vet Parasitol. 18(2): 181–182.

Sadighian A (1969) Helminth parasites of stray dogs and jackals in Shahsavar ar- ea, Caspian region, Iran. J Helminth. 2:372–374.

Shahgudian ER (1960) A key to the anophelines of Iran. Acta Med Iran. 3: 38–48.

Service MW (2003) Medical Entomology for Students. Vol. 3. United Kingdom: Cambridge. University Press, Cambridge.

Silver BJ (2008) Mosquito Ecology: Field Sampling Methods. Vol. 3. Springer- Verlag Press, New York.

Simsek FM (2004) Seasonal larval and adult population dynamics and breeding hab- itat diversity of Culex theileri Theo- bald, 1903 (Diptera: Culicidae) in the Golbasi District, Ankara, Turkey. Turk J Zool. 28: 337–44.

Slocombe JOD, Villeneure A (1993) Heart worm in dogs in Canada in 1991. Ca- nadian Vet J. 4 (10): 630–633.

Sundaramans Y (1949) Biometrical studies on intergradations in the genitalia of certain populations of Culex pipiens and Culex quinquefasciatus in the United States, Amer. J Hyg. 60: 307–314.

Tiawsirisup S, Thanapaisarnkit T, Varatorn E, Apichonpongsa T, Bumpen KN, Rattanapuchpong S,Chungpiwat S, Sanprasert V, Nuchprayoon S (2010) Canine Heartworm (Dirofilaria immitis (Leidy)) Infection and Immunoglobu- lin G Antibodies against Wolbachia (Rickettsiales: Rickettsiaceae) in Stray Dogsin Bangkok, Thailand. Thai J Vet Med. 40(2): 165–170.

Toma L, Menegon M, Romi R, De Matthaeis E, Montanari M, Severini C (2011) Status of insecticide resistance in Culex pipiens field populations from north- eastern areas of Italy before the with- drawal of OP compounds. Pest Manag Sci. 67(1): 6–100.

Venco L, McCall JW, Guerrero J, Genchi C (2004) Efficacy of long term monthly administration of Ivermectin on the progress of naturally acquired heart- worm infections in dogs. Vet Parasitol.124: 259–268.

Vinogradova EB (2000) Mosquitoes Culex pipiens pipiens: taxonomy, distribu- tion, ecology, physiology, genetics and control. PenSoft, Sofia.

WHO/FAO/OIE (1984) Animal health Year- book 1983. Animal health Service, An- imal production and Health Division, World Health Organization, Food and Agriculture Organization, International des Epizooties Rome.

WHO (2002) Entomology and vector control.Training module on malaria control. Guide for participants. World Health Organization, Global Malaria Programme WHO Press, World Health Organization, Avenue Appia, Geneva Switzerland.

WHO (1998) Test procedures for insecticide resistance monitoring in malaria Vec- tors, bio-efficacy and persistence of in- secticides on treated surfaces. Report of WHO Informal Consultation, WHO/ CDS/CPC/MAL/98.12. Geneva, Swit- zerland.

Yildirim A, Ica A, Atalay O, Duzlu O, Inci A (2006) Prevalence and epidemiological aspects of Dirofilariaimmitis (Leidy) (Leidy) in dogs from Kayseri Province, Turkey. Res Vet Sci. 82: 358–363.

Zaim M (1987) Malaria Control in Iran. J Am Mosq Cont Assoc. 3: 392–396.

Zaim M, Cranston PS (1986) Checklist and keys to the Culicinae of Iran (Diptera: Culicidae). Mosq Syst. 18: 233–45.

Zarriffard MR (1993) A study on helminthic parasites of wild carnivorous of east Azer- baijan with emphasis on Echinococcus multilocularis. [PhD dissertation]. School of Public Health, Tehran University of Medical Sciences, Iran.

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Culicidae Vector Dirofilaria immitis Susceptibility test Iran

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Ataie A, Moosa-Kazemi SH, Vatandoost H, Yaghoobi- Ershadi MR, Bakhshi H, Anjomruz M. Assessing the Susceptibility Status of Mosquitoes (Diptera: Culicidae) in a Dirofilariasis Focus, Northwestern Iran. J Arthropod Borne Dis. 9(1):7-21.