Document Type : Original Article

Authors

1 Department of Biology and Control of Disease Vectors (Medical Entomology), School of Health, Shiraz University of Medical Sciences, Shiraz, Iran

2 Research Center for Health Sciences, Institute of Health, Shiraz University of Medical Sciences, Shiraz, Iran

Abstract

Background:Human head lice is one of the most invincible neglected skin diseases. The use of pyrethroid insecticides is a standard method of treating the disease, which leads to lice population resistance in the long run. The main aim of the current survey was to screen the biomarkers of permethrin-associated kdr (knockdown resistance) point mutations through molecular analysis of the human head lice populations in primary school children in the south of Iran.
 
Methods: In an experimental study, Field-collected head lice from infested students were fixed in ethanol, identified using valid taxonomic keys, and processed by PCR for kdr mutant studies. Sequencing partial voltage-sensitive sodium channel gene in different head lice populations was subsequently implemented and compared with the permethrin-resistant diamondback moth, Plutella xylostella (Lepidoptera: Plutellidae) as the gold standard.
 
Results:Human head lice appeared to reflect kdr point mutations in specimens from the city of Shiraz. At least three amino acid mutations at designated sites of D820E, L840F, and N874G, corresponding to replacements of aspartic acid to glutamic acid, leucine to phenylalanine, and asparagine to glycine, are clear in this representative population, respectively. At the same time, only L840F is reported as a new mutant in this survey.
 
Conclusion: The ongoing treatment of head lice infested in school children harboring kdr-mutated or permethrin-resistant mutants in Shiraz is risky, illogical, and contrary to the One Health initiative of the World Health Organization. Health executives should thus immediately take the indispensable steps to prohibit further procurement of permethrin.

Keywords

1.Durden L, Musser G. The mammalian hosts of the sucking lice (Anoplura) of the world: a host-parasite list. Bulletin of the Society for Vector Ecology, 1994;19(2):130-68.
2.Reed DL, Light JE, Allen JM, Kirchman J. Pair of lice lost or parasites regained: the evolutionary history of anthropoid primate lice. BMC Biology. 2007;5(1):7.
3.Drali R, Abi-Rached L, Boutellis A, Djossou F, Barker SC, Raoult D. Host switching of human lice to new world monkeys in South America. Infection, Genetics and Evolution, 2016;39:225-31.
4.Amanzougaghene N, Mediannikov O, Ly TDA, Gautret P, Davoust B, Fenollar F, et al. Molecular investigation and genetic diversity of Pediculus and Pthirus lice in France. Parasites and Vectors, 2020;13:1-11.
5.Reed DL, Smith VS, Hammond SL, Rogers AR, Clayton DH. Genetic analysis of lice supports direct contact between modern and archaic humans. PLoS Biol. 2004;2(11):e340.
6.Amanzougaghene N, Akiana J, Mongo Ndombe G, Davoust B, Nsana NS, Parra H-J, et al. Head lice of pygmies reveal the presence of relapsing fever Borreliae in the Republic of Congo. PLoS neglected tropical diseases. 2016;10(12):e0005142.
7.Leo N, Hughes J, Yang X, Poudel S, Brogdon W, Barker S. The head and body lice of humans are genetically distinct (Insecta: Phthiraptera, Pediculidae): evidence from double infestations. Heredity. 2005;95(1):34-40.
8.Veracx A, Raoult DJTip. Biology and genetics of human head and body lice. 2012;28(12):563-71.
9.Boutellis A, Abi-Rached L, Raoult D. The origin and distribution of human lice in the world. Infection, Genetics, and Evolution. 2014;23:209-17.
10.Lane RP, Crosskey RW. Medical insects and arachnids: Springer Science & Business Media; 2012.
11.Organization WH. Report of the tenth meeting of the WHO Strategic and Technical Advisory Group for neglected tropical diseases. Geneva: World Health Organization. 2017.
12.Azizi K, Askari MB, Kalantari M, Moemenbellah-Fard MD. Molecular detection of Leishmania parasites and host blood meal identification in wild sand flies from a new endemic rural region, south of Iran. Pathogens and global health. 2016;110(7-8):303-9.
13.Oryan A, Shirian S, Tabandeh MR, Hatam GR, Kalantari M, Daneshbod Y. Molecular, cytological, and immunocytochemical study and kDNA sequencing of laryngeal Leishmania infantum infection. Parasitology research. 2013;112(4):1799-804.
14.Azizi K, Davari B, Kalantari M, Fekri S. Gerbillid rodents fauna (Muridae: Gerbillinae) and detection of reservoir hosts (s) of zoonotic cutaneous leishmaniasis using a nested-PCR technique in Jask City in Hormozgan Province in 2008. Scientific Journal of Kurdistan University of Medical Sciences. 2011;16(2).
15.Hunter J, Barker S. Susceptibility of head lice (Pediculus humanus capitis) to pediculicides in Australia. Parasitology research. 2003;90(6):476-8.
16.Fox K, Larkin K, Sanchez A. Global Trends in Genetic Markers of Pediculus humanus capitis Resistance Mechanisms. Current tropical medicine reports. 2020;7:65-73.
17.Manrique-Saide P, Pavía-Ruz N, Rodríguez-Buenfil JC, Herrera Herrera R, Gómez-Ruiz P, Pilger D. Prevalence of pediculosis capitis in children from a rural school in Yucatan, Mexico. Revista do Instituto de Medicina Tropical de São Paulo. 2011;53(6):325-7.
18.Al Bashtawy M, Hasna F. Pediculosis capitis among primary-school children in Mafraq Governorate, Jordan. EMHJ-Eastern Mediterranean Health Journal, 18 (1), 43-48, 2012. 2012.
19.Govere J, Speare R, Durrheim D. The prevalence of pediculosis in rural South African schoolchildren: research in action. South African Journal of Science. 2003;99(1):21-3.
20.Rassami W, Soonwera M. Epidemiology of pediculosis capitis among schoolchildren in the eastern area of Bangkok, Thailand. Asian Pacific journal of tropical biomedicine. 2012;2(11):901-4.
21.Etim S, Ohioma M, Okon O, Akpan P. Pediculosis among primary school children in Calabar, Nigeria and implications for control. Scientific Research and Essays. 2013;7(47):4071-5.
22.Downs A, Stafford K, Stewart G, Coles G. Factors that may be influencing the prevalence of head lice in British school children. Pediatric dermatology. 2000;17(1):72-4.
23.Haghi FM, Golchin M, Yousefi M, Hosseini M, Parsi B. Prevalence of pediculosis and associated risk factors in the girls' primary school in Azadshahr City, Golestan Province, 2012-2013. Iranian Journal of Health Sciences. 2014;2(2):63-8.
24.Saghafipour A, Akbari A, Norouzi M, Khajat P, Jafari T, Tabaraie Y, et al. The epidemiology of pediculus is humanus capitis infestation and effective factors in elementary schools of Qom Province Girls 2010, Qom, Iran. Qom University of Medical sciences journal. 2012;6(3):46-51.
25.Moradiasl E, Habibzadeh S, Rafinejad J, Abazari M, Ahari SS, Saghafipour A, et al. Risk factors associated with head lice (pediculosis) infestation among elementary school students in Meshkinshahr county, North West of Iran. International Journal of Pediatrics. 2018;6(3):7383-92.
26.Heukelbach J, Van Haeff E, Rump B, Wilcke T, Moura RCS, Feldmeier H. Parasitic skin diseases: health care‐seeking in a slum in north‐east Brazil. Tropical Medicine International Health. 2003;8(4):368-73.
27.Downs A, Stafford K, Hunt L, Ravenscroft J, Coles G. Widespread insecticide resistance in head lice to the over‐the‐counter pediculicides in England, and the emergence of carbaryl resistance: Therapeutics. British Journal of Dermatology. 2002;146(1):88-93.
28.Kristensen M, Knorr M, Rasmussen A-M, Jespersen JB. Survey of permethrin and malathion resistance in human head lice populations from Denmark. Journal of Medical Entomology. 2006;43(3):533-8.
29.Moemenbellah-Fard MD, Nasiri Z, Azizi K, Fakoorziba MR. Head lice treatment with two interventions: pediculosis capitis profile in female schoolchildren of a rural setting in the south of Iran. Annals of Tropical Medicine and Public Health. 2016;9(4):245.
30.Kalari H, Soltani A, Azizi K, Faramarzi H, Moemenbellah-Fard MD. Comparative efficacy of three pediculicides to treat head lice infestation in primary school girls: a randomised controlled assessor blind trial in rural Iran. BMC dermatology. 2019;19(1):13.
31.Hemingway J, Miller J, Mumcuoglu K. Pyrethroid resistance mechanisms in the head louse Pediculus capitis from Israel: implications for control. Medical and Veterinary Entomology. 1999;13(1):89-96.
32.Firooziyan S, Sadaghianifar A, Taghilou B, Galavani H, Ghaffari E, Gholizadeh SJJoME. Identification of novel voltage-gated sodium channel mutations in human head and body lice (Phthiraptera: Pediculidae). 2017;54(5):1337-43.
33.Shouroki FK, Neghab M, Mozdarani H, Alipour H, Yousefinejad S, Fardid R. Genotoxicity of inhalational anesthetics and its relationship with the polymorphisms of GSTT1, GSTM1, and GSTP1 genes. Environmental Science and Pollution Research. 2019;26(4):3530-41.
34.Hoosh-Deghati H, Dinparast-Djadid N, Moin-Vaziri V, Atta H, Raz AA, Seyyed-Tabaei SJ, et al. Composition of Anopheles species collected from selected malarious areas of Afghanistan and Iran. Journal of arthropod-borne diseases. 2017;11(3):354.
35.Mohammad Rezaei F, Hashemzadeh S, Ravanbakhsh Gavgani R, Hosseinpour Feizi M, Pouladi N, Samadi Kafil H, et al. Dysregulated KDR and FLT1 Gene Expression in Colorectal Cancer Patients. Reports of Biochemistry and Molecular Biology. 2019;8(3):244-52.
36.Oh J-M, Lee IY, Lee W-J, Seo M, Park S-A, Lee SH, et al. Prevalence of pediculosis capitis among Korean children. Parasitology research. 2010;107(6):1415-9.
37.Ashfaq M, Prosser S, Nasir S, Masood M, Ratnasingham S, Hebert PD. High diversity and rapid diversification in the head louse, Pediculus humanus (Pediculidae: Phthiraptera). Scientific Reports. 2015;5(1):1-13.
38.Control CfD, Prevention. Pictorial keys to arthropods, reptiles, birds, and mammals of public health significance: Department of Health & Human Services, Centers for Disease Control and …; 2003.
39.Alipour H, Raz A, Zakeri S, Djadid ND. Molecular characterization of matrix metalloproteinase-1 (MMP-1) in Lucilia sericata larvae for potential therapeutic applications. Electronic Journal of Biotechnology. 2017;29:47-56.
40.Ebrahimi S, Alipour H, Azizi K, Kalantari M. Construction of PX-LmGP63 Using CRISPR-Cas9 as Primary Goal for GP63 gene Knockout in Leishmania major and Leishmanization. Jundishapur Journal of Microbiology. 2021;14(1).
41.Omidi A, Khodaveisi M, MOGHIM BA, Mohammadi N, Amini R. Pediculosis capitis and relevant factors in secondary school students of Hamadan, West of Iran. 2013.
42.Firooziyan S, Sadaghianifar A, Taghilou B, Galavani H, Ghaffari E, Gholizadeh S. Identification of novel voltage-gated sodium channel mutations in human head and body lice (Phthiraptera: Pediculidae). Journal of Medical Entomology. 2017;54(5):1337-43.
43.Karakuş M, Atıcı T, Karabela ŞN, Baylan O, Limoncu ME, Balcıoğlu İC. Detection of permethrin resistance and phylogenetic clustering of turkish head lice (Pediculus humanus capitis; De Geer, 1767 populations. Acta Tropica. 2020;204:105362.
44.Kokturk A, Baz K, Bugdayci R, Sasmaz T, Tursen U, Kaya TI, et al. The prevalence of pediculosis capitis in schoolchildren in Mersin, Turkey. International journal of dermatology. 2003;42(9):694-8.
45.Hatam-Nahavandi K, Ahmadpour E, Pashazadeh F, Dezhkam A, Zarean M, Rafiei-Sefiddashti R, et al. Pediculosis capitis among school-age students worldwide as an emerging public health concern: a systematic review and meta-analysis of past five decades. Parasitology Research. 2020:1-19.
46.Nezhadali A, Babazadeh T, Nadrian H, Allahverdipour H. Cognitive factors associated with pediculosis preventive behaviors among mothers of school-age children in Chaldoran county, Iran. Journal of Multidisciplinary Healthcare. 2020;13:19.
47.Saghafipour A, Zahraei-Ramazani A, Vatandoost H, Mozaffari E, Rezaei F, KaramiJooshin M. Prevalence and risk factors associated with head louse (Pediculus humanus capitis) among primary school girls in Qom province, Central Iran. International Journal of Pediatrics. 2018;6(4):7553-62.
48.Moradi A, Zahirnia A, Alipour A, Eskandari Z. The prevalence of Pediculosis capitis in primary school students in Bahar, Hamadan Province, Iran. 2009.
49.Azizi K, Shahidi-Hakak F, Asgari Q, Hatam GR, Fakoorziba MR, Miri R, et al. In vitro efficacy of ethanolic extract of Artemisia absinthium (Asteraceae) against Leishmania major L. using cell sensitivity and flow cytometry assays. Journal of Parasitic Diseases. 2016;40(3):735-40.
50.Ebrahimi V, Hamdami E, Moemenbellah-Fard MD, Jahromi SE. Predictive determinants of scorpion stings in a tropical zone of south Iran: use of a mixed seasonal autoregressive moving average model. Journal of venomous animals and toxins including tropical diseases. 2017;23.
51.Fakoorziba M, Neghab M, Alipour H, Moemenbellah-Fard M. Tick-borne Crimean-Congo haemorrhagic fever in Fars province, southern Iran: Epidemiologic characteristics and vector surveillance. Pak J Biol Sci. 2006;9(14):2681-4.
52.Neghab M, Momenbella-Fard M, Naziaghdam R, Salahshour N, Kazemi M, Alipour H. The effects of exposure to pesticides on the fecundity status of farmworkers resident in a rural region of Fars province, southern Iran. Asian Pacific journal of tropical biomedicine. 2014;4(4):324-8.
53.Alipour H, Darabi H, Dabbaghmanesh T, Bonyani M. Entomological study of sand flies (Diptera: Psychodidae: Phlebotominae) in Asalouyeh, the heartland of Iranian petrochemical industry. Asian Pacific journal of tropical biomedicine. 2014;4:S242-S5.