Skip to main content
Download PDF

Epidemiological analysis of pediculosis and the distribution of kdr mutation frequency in head lice populations in Torbat Heydarieh city of Khorasan Razavi Province, Northeastern Iran

BMC Research Notes volume 17, Article number: 323 (2024) Cite this article

Abstract

Head lice infestations are the most prominent ectoparasitic infection in the world, including Iran, particularly among school children. Recently, numerous cases of infestation have been reported in various provinces of the country. This study aimed to investigate the prevalence of head louse infestations and analyze kdr gene sequences in terms of resistance mutations in the Torbat-e Heydarieh, Mahvelat, and Zaveh cities of Khorasan Razavi Province, Northeast Iran. The data related to the epidemiological and demographic history of head lice populations were extracted from their medical records and analyzed in Excel software. After extracting the genomic DNA, the kdr fragment was amplified using specific primers. The sequences were also analyzed using bioinformatics software. The prevalence of head louse infestations was 1.59% and 1.7% during 2016 and 2017, respectively. Sequence analysis revealed the frequency distribution of two kdr haplotypes, I and V, in the study areas. The increase in head louse infestations in recent years and the simultaneous presence of kdr mutations indicate the need for new treatments and monitoring/controlling resistance to head louse insecticides.

Peer Review reports

Introduction

Head and body lice are the most common external parasites in humans, causing serious health problems, especially among school students worldwide [1]. These lice are not recognizable by their appearance and can be classified only based on the place where they live, on the human head or body [2]. In many areas, improvements in health, economic, and social status have had a significant impact on reducing lice infestation. Nevertheless, the parasite is still widespread in the globe. In recent years, the prevalence of pediculosis has been increasing in different parts of the world, with varying degrees of infection severity [3,4,5,6]. Epidemiological investigation in the some middle east countries showed that the head lice prevalence among students in Saudi Arabia is 64.2% [7], Jordan 20.4% [8], Syria 14.3% [9], Turkey 51.9% [10], Iraq 9.6% [11]. In Iran, the prevalence of pediculosis was reported as 1.73% in 2011 and 7.4% in 2015 [12, 13]. Mean infestation prevalence between Iranian preschool and primary school students is 10.6 in 2024 [14]. Hatam-Nahavandi et, al. 2020 In the Meta analysis study mentioned that the prevalence of louse infestation varies in different continent, country, cities and villages as overall it is highest in central and south America (33%) and lowest in Europe (5%) [15]. It could be differ by gender, age, occupation and many other social and economic factors as it is 0-58.5% [15, 16] in male students and 0-93.2 in girls [17, 18].

Raising public awareness, improving health behaviors, diagnosing, and treating patients in epidemics using insecticides are the most important interventions to decrease the prevalence of head lice infestation [19, 20]. Regular rinsing the head with normal soap and shampoo and warm water reduces the number of adult lice. According to the Center for Infectious Diseases Management of Iran’s Ministry of Health and Medical Education, permethrin1%, dimethicone4%, and gammabenzene (lindane) shampoo are used to treat head lice infestation (Control Disease Center [CDC], Iran). The extensive use of pediculicides has accelerated the development of resistance [21]. The indiscriminate use of pyrethroids has also led to the ubiquitous development of resistance, which causes the insect control program to fail [22]. Various reports of treatment failure from different countries, such as Denmark, Mexico, Chile, Madagascar, and Thailand, have shown developed resistance of head lice to well-known pediculicides, making it increasingly difficult to eliminate infestations [1, 23,24,25,26,27,28,29].

Knockdown resistance (KDR) is a well-recognized mechanism of resistance to pyrethroid insecticides innumerous insect species. This resistance is instigated by point mutations in the pyrethroid target site, specifically the para-type sodium channel [30, 31].The insect sodium channel shares homology with the α-subunit found in mammalian sodium channels [32]. The pore-forming subunits of sodium channels consist of four homologous repeats, each containing six transmembrane helices (S1–S6). The S5 and S6 segments combine to construct a central ion-conducting pore, while the S1–S4 segments compose the channel’s voltage-sensing region [33].The insect para channel serves as the primary target site for pyrethroids, dichloro diphenyl trichloro ethane(DDT), synthetic analogues of N-alkylamides, and dihydropyrazoles [34, 35].This gene (voltage gated sodium channel) comprises 2014 amino acids, and the second S1-S5 in subunit II, which is the site of insecticide action, located between amino acids 782–940 in Pediculus [36]. The diminished sensitivity of nerve cells (kdr type) plays a significant role as a resistance mechanism in lice, particularly concerning pyrethroids and DDT. Pyrethroid-resistant strains, unlike susceptible strains, exhibit two mutations, T917I and L920F within domain 2 and subdomain 5 (IIS5) and one mutation (M815I) within IIS1-2. These mutations are linked to resistance against the insecticide permethrin [12, 37], and in the sodium channel, they diminish the channel’s susceptibility to pyrethroids, resulting in resistance to pyrethroids, notably permethrin [38].

Resistance diagnosis assays should be sufficiently flexible to track resistance development. They should also enable the detection of resistant lice genotypes when their frequencies are still low enough to permit the adaptation of lice control strategies to restrict further resistance selection. For this reason, molecular methods together with infestation prevalence data can be helpful in concluding bioassay data [21, 39].

In recent times, identification of kdr amino acid substitutions, including M815I, T917I, and L920F, has been supplemented by the discovery of six new mutations within the extracellular loop of IIS1-2 (H813P) and IIS5 (I927F, L928A, R929V, L930M, and L923M), as well as the mutation F815I in head lice and the mutation N818D in body louse populations across the country. These alpha subunits have been demonstrated to robustly linked with kdr resistance, and the existence of the mutations F815I and N818D have also been documented [36, 40]. In the course of the present study, however, a total of four novel amino acid substitutions—namely, K794E, P813H, F815I, and N818D—were identified in head lice for the very first time. These mutations are situated in the vicinity of positions recognized for their correlation with kdr-associated mutations in IIS1 and the IIS1-2 linkers [41].

The prevalence of pediculosis and the frequency of kdr gene mutations in Torbat-e Heydarieh, Mahvelat, and Zaveh counties of Khorasan Razavi Province, Iran, remain uncharted. In light of the rising incidence of infestations throughout the country, the principal objective of this ongoing study was to investigate the pediculosis prevalence and undertake kdr gene sequencing in lice populations situated in region covered by Torbat-e Heydarieh University of Medical Sciences (THUMS).

Materials and methods

Head lice sample collections

The samples of head lice were collected from Torbat-e Heydarieh, Mahvelat, and Zaveh counties of Khorasan Razavi Province, Northeastern Iran, with Mashhad as its capital city (Fig. 1).The epidemiological and demographical data of individuals infested with head lice were gathered via their medical records and analyzed in the Excel software. The extraction and input of data into the software were performed under the supervision of the Center for Infectious Diseases Management (Iran’s Ministry of Health). The head lice were removed from the hair using a fine-tooth comb, following the acquisition of informed consent. Before being transferred to the Entomology Laboratory at Urmia University of Medical Sciences (UUMS), all the samples were preserved in 70% ethanol.

Fig. 1
figure 1

Torbet-e Heydarieh city map showing the location of Mehvalat, Torbet-e Heydarieh, and Zaveh among the cities of the province

Full size image

DNA extraction and PCR amplification

Genomic DNA was extracted using a DNA extraction kit (Yekta Tajhiz Azma [YTA], Tehran, Iran). The head lice specimens were removed from the 70% ethanol by being washed three times with phosphate buffer saline (PBS 1×). Then an individual whole-body louse from each sample was homogenized by a pestle in 200 µl of buffer TG1 and 20 µl of proteinase K. The rest of the DNA extraction process was followed based on the manufacturer’s instructions (YTA).

For the amplification of a 900-bp fragment within the voltage-gated sodium channel (VGSC) gene, species-specific primers were employed; the PCR reaction conditions and thermal program were used according to firooziyan et, al 2017 [36].

The complete reference sequence was determined through a combination of direct sequencing, BLAST analysis, and multiple sequence alignments. This reference sequence was subsequently compared with the GenBank entry DQ062568 [1] and AY191157 [42]. The multiple sequences of lice were assembled and analyzed with Clustal Omega [43] and MEGA6 [44].

Results

Epidemiology of head lice infestation

As per the data sourced from the national health portal (Iran’s Ministry of Health), the overall number of head lice infestations across the country stood at 818,233 and 766,496 cases during the years 2016 and 2017, respectively.

A total of 9,962 adult head lice samples were systematically collected from the districts of Torbat-e Heydarieh, Mahvelat, and Zaveh during the years 2016 and 2017. The number of lice infestations documented within the population covered by the health services of THUMS totaled 4,303 cases in 2016 and 5,659 cases in 2017, indicating a 24% increase in the number of infested cases in 2017 compared to its previous year. These statistics correspondingly accounted for 0.53% and 0.74% of the nationwide total cases in 2016 and 2017, respectively. The majority of cases were found in primary school children, while the fewest cases were observed among non-student individuals. The number of cases in the cities of Torbat-e Heydarieh and Mahvelat increased between 1 and 4% in 2016 compared to 2017, while in the city of Zaveh, it decreased by about 4%. Among head lice infestation cases reported in 2016 and 2017, over 88% and nearly 90% were found in girls and women, showing about 2% growth in the number of cases infected with head lice in 2017 compared to 2016. The highest number of infestation cases in Torbat-e Heydarieh in 2016 and 2017 was reported from two different health service centers, Shahid Beheshti and Taleghani, situated in the southern and outskirts of the city. In Zaveh city, during the same years, the highest incidence of head lice infestation was observed in Muslim-Ibn-Aqeel and Buri-Abad healthcare centers, which are located in rural areas. Zaveh encompasses 10 comprehensive health service centers. Among them, the majority of registered cases in 2016 and 2017 were linked to Dolat Abad, an urban health service center. Notably, the peak incidence of infestation during the aforesaid time periods was attributed to two rural centers within the region (Shahin&Chakhmagh).In Mehvelat County, there are seven comprehensive health service centers; the greatest number of cases recorded in 2016 and 2017 were attributed to an urban health service center named Feyzabad. Interestingly, the highest incidence of infestation during the above-mentioned years was associated with Mehne, a rural center.

Studying the parental literacy of cases of head lice infestation within the population covered by THUMS in 2016 and 2017 unveiled that the most notable instances of infection were observed among individuals whose parents held diplomas. Conversely, the lowest incidence of infestation was found in children whose parents possessed literacy beyond the bachelor’s level. Hence, no significant distinction was discerned between parental literacy levels and the incidence of infestation. However, it is important to note that some groups (illiterate, Bachelor’s degree, and above Bachelor’s degree) experienced more infestation in 2017 than 2016 (Table 1).

Table 1 Cases of head lice infestation in the population covered by Torbat Heydarieh University of Medical Sciences based on parents’ literacy and by city in 2016 and 2017
Full size table

The results, based on parents’ occupation, showed that the highest number of infected cases in 2016 was related to those whose parents were agricultural workers (37%), followed by freelance (21%) and livestock (18%) workers. This pattern persisted with varying percentages in 2017. There was no statistically significant difference between parents’ occupations and the infestation rate. However, a positive correlation was observed between the number of members in each family and the infestation rate. In both years, families with four and three members exhibited higher infestation rates compared to those with more than four members. Comparison of infestation cases living in urban area with those living in rural area revealed higher infection cases in urban than rural areas in both years. Interestingly, there was a 5% increase of infestation in urban areas in 2017 compared to the previous year, while this trend was reverse for rural areas.

Comparison between the number of head louse cases in the study area’s population and the quantity of anti-head louse compounds distributed among this population revealed that in both 2016 and 2017, all individuals affected by the infestation had access to at least one head lice treatment protocol (Table 2).The prevalence status of head lice infestation of the study area’s population by city compared to the whole country during 2016 and 2017 in terms of prevalence and incidence showed that, despite the decreasing incidence in the whole country in 2016 compared to 2017, the pediculosis incidence in this population has increased, especially in Torbat-e Heydariyeh, which is almost twice the national average.

Table 2 The amount of distribution of anti-head lice compounds in the population covered by Torbat-e Heydarieh University of Medical Sciences by city
Full size table

Genetic resistance

A 900-bp fragment of the sodium channel gene was amplified and sequenced in total head lice specimens collected from the study areas. Comparing the resulting sequence with those in the World Gene Bank revealed that this sequence consists of three exons and two introns. The sizes of introns 1 and 2 in the studied samples were 86–87 bp and 88–90 bp, respectively, while the exon sequences measured as 142 bp, 174 bp, and 162 bp, respectively. Comparing the exon region sequences within our samples and contrasting sequences with those of the Gene Bank (representing four reported haplotypes) revealed a striking similarity between our samples and the Gene Bank sequences, ranging from 98.5 to 100% and from 97.98 to 98.53%, respectively. Minor differences were detected in 14 mismatches, six within exon 1, and the remainder within exon 3. Notably, of these 14 instances of nucleotide mismatches, only seven instances led to amino acid substitutions, with four of them originating from the samples collected in Torbat-e Heydarieh. Specifically, the P813H substitution emerged in 50% of the head lice specimens. It is noteworthy that this particular mutation has already been documented in body lice (Fig. 2).Three prior mutations, namely M815I, T917I, and L920F, were present in samples lacking the P813H substitution. Therefore, P813H was introduced as the fifth haplotype to complement the existing four haplotypes. As a result, two distinct haplotypes, labeled as 1 and 5, were identified in the study area.

Fig. 2
figure 2

Alignment of kdr region amino acid sequences in head lice samples collected from Torbat-e Heydarieh city (NKhR1-6) and comparing it with the sequences available in the World Gene Bank (kx301983I, kx301988II, kx301991III, kx301981IV)

Full size image

Discussion

Pediculosis humanus capitis (De Geer) is known as a common problem worldwide, especially in developing countries such as Iran [13, 40, 41, 45, 46].

The outcomes of this study revealed that the prevalence of head lice infection in the study population was 1.59% in 2016 and 1.7% in 2017. These rates are notably lower than the national average rate of 8.8% [13]. The infection rate among girls in comparison to the total population in the southeastern region of Iran, particularly the Bashagard District, was recorded as 67.3% in 2017 [13]. In the study which were condacted in Iraq in primary school, it was 18.7 between girls and 1.82 in boies [11]. In the current study, this rate for the years 2016 and 2017 was approximately 88% and 90%, respectively. These variances in the head lice infection rates can be attributed to factors such as the utilization of communal facilities, the absence of health educators in schools, parents’ limited awareness of pediculosis, prevailing socio-economic conditions, and overall poverty [13]. Based on studies conducted in Iran, Jordan, Egypt, Palestine, and Yemen, the practice of sharing veils and headscarves among girls has an impact on the prevalence of pediculosis [47,48,49,50,51].

The findings of the current study indicated that the occurrence of pediculosis in urban areas is greater than rural areas, especially because of more amenities, which indicates a probable shift in the pattern of pediculosis infection. The reduced number of infestation cases in Zaveh County, compared to the two other cities, in 2016 could possibly be due to incomplete reporting or effective intervention and treatment training. The prevalence of head lice infestation in the Middle East and certain countries within the region has been reported to range between 4.2% and 7.8% [15]. However, across different regions of Iran, these rates ranged from 0.47 to 27.1% among primary school students aged 7 to 11 years [13, 52]. in Iraq inefestion rate among primary school students 9.6 reported mean age of students was 9 years old [11]. As reported in in meta-analysised-based systematic review highest infestation seen in school aged children, adolescents and girls [53]. In this our, 55% of the infestation cases were found among elementary school children, while the remaining cases were associated with secondary school students and non-student individuals. This distribution is due to the fact that primary schools underwent regular screenings every three months. Additionally, in the age range of primary school students, there is a significant amount of physical contact, particularly head-to-head contact, among the students [54]. However, children under the age of six are less likely to be in crowded environments, reducing their susceptibility to infestations. In high school and beyond, individuals tend to adhere to personal and public health practices due to their higher level of education, resulting in fewer instances of infestation.

Numerous studies conducted in Iran, Egypt, Yemen, Palestine, Iraq and Turkey have indicated that the likelihood of head lice infestation among students whose parents have lower levels of literacy is higher [11, 13, 48, 50, 51, 55, 56]. Our findings revealed that students whose parents hold a diploma exhibited a higher infestation rate (26-29%) than those with illiterate parents (approximately 8%). Educated parents are generally anticipated to possess greater knowledge about head lice infestations and methods for prevention [57, 58].

Considering the effectiveness of interventions and education in enhancing public awareness and mitigating vector-borne diseases, it is imperative to design appropriate educational initiatives tailored for parents, teachers, students, and the general population. These programs should focus on enhancing awareness about risk factors of and prevention strategies against head lice infestation. Similar research to present study conducted in countries such as Korea, Jordan, Egypt, Yemen, Malaysia, Turkey, Thailand and Iraq has also highlighted a positive correlation between head lice infections and household size. Crowded living conditions and close contact among family members in such homes tend to facilitate the transmission of head lice [11, 48,49,50, 56, 59,60,61]. Nevertheless, in the context of this study, despite the presence of families ranging from one to six individuals, the greatest number of infection cases was identified within families consisting of 4 and 3 members, respectively. Interestingly, no discernible correlation was observed between the number of family members and the infestation rate. These outcomes align with those of the research conducted by Firoozfar et al. in 2019, focusing on the Kurmanj tribes in North Khorasan [51]. The decrease in the level of lice infestation in families with more than 4 people may be due to the increase in the level of awareness of older children, through the education given in schools by health educators or health centers, or the knowledge that the individual himself/herself during time is gained at the community level.

Despite the application of dimethicone and permethrin 1% for the treatment of head lice in the study area during both the years 2016 and 2017, the incidence of infestations demonstrated a notable 24% rise. Conversely, in various studies, the use of permethrin 1% exhibited effectiveness, ranging from 29 to 90%, after treatment periods of one, two, and three weeks [40, 51, 62]. Direct, face-to-face training on the proper application of anti-lice compounds has demonstrated to be effective in enhancing their effectiveness. Nonetheless, it is crucial to acknowledge the escalating selective pressure on insecticides due to the widespread and unregulated utilization of diverse anti-lice compounds. This intensification of selective pressure could lead to the emergence and dissemination of resistance. To address this concern, consistent monitoring of the resistance status becomes imperative to identify suitable insecticides for effective control measures. The global prevalence of insecticide usage has resulted in reported instances of insecticide resistance from various parts of the world [23, 40, 61, 63,64,65,66,67].The annual escalation in the number of infestation cases within the population encompassed by THUMS, despite concerted efforts, could potentially stem from the emergence of resistance within the region.

Examination of the kdr gene sequence in head lice within the purview of THUMS has revealed the presence of haplotype I (M815I + T917I + L920F), which have previously been documented in Iran [36, 40, 41]. A novel haplotype was also identified in the region, constituting the fifth kdr haplotype in head lice. This newly discovered haplotype is defined by the substitution of the amino acid proline with histidine at position 813 (H813P) within the head lice genome. It was remarkable that the replacement of M815I within the kdr gene has been documented as a contributing factor to insecticide resistance in head lice and various other insect species [31, 42, 68,69,70,71]. The prevalence of these mutations in West Azerbaijan and Zanjan regions has been recorded as 58.33% among head lice population and 76.9% among body lice population [36]. The occurrence of T929I-L932F mutations within the head lice population in Denmark has also been associated with resistance to DDT and pyrethroids [1, 72, 73].

In the current study, a combination of three established mutations (M815I, T917I, and L920F), along with the novel mutation H813P, was detected in 50% of the sequences. This result parallels the findings of a prior study conducted in North Khorasan Province [51]. The exact impact of aforementioned mutations on lice resistance to anti-lice compounds remains uncharted in this region and necessitates in-depth molecular and epidemiological inquiry. In this study, no notable correlation was observed between the literacy and occupation of parents and the size of the family. This absence of correlation could potentially stem from the presence of these mutations within the head lice population in Torbat-e Heydarieh. Nonetheless, further analogous investigations in diverse regions across the country are requisite to validate this conclusion.

In conclusion, factors such as the level of parental literacy, the number of family members, age, gender, and the level of awareness of the ways of spreading lice play a role in the prevalence of lice infestation. Increasing awareness and training on personal hygiene and ways to prevent the spread of head lice among students at school and in family relationships can prevent further spread of contamination. In order to reduce the existing cases of contamination due to the existence of various mutations in the place of effect of, insecticide, alternative compounds should be used while teaching non-chemical combat methods. Limitation: Due to the budget limitation, in this project, insecticide resistance genes were examined in a small number of samples. It is suggested to study in other regions with large sample size and a large number of genes, especially resistance genes to insecticides such as Ivermectin.

Data availability

No datasets were generated or analysed during the current study.

References

  1. Kristensen M. Identification of sodium channel mutations in human head louse (Anoplura: Pediculidae) from Denmark. J Med Entomol. 2005;42(5):826–9.

    Article  CAS  PubMed  Google Scholar 

  2. Boutellis A, Abi-Rached L, Raoult D. The origin and distribution of human lice in the world. Infect Genet Evol. 2014;23:209–17.

    Article  PubMed  Google Scholar 

  3. Burgess IF. Human lice and their control. Annual Reviews Entomol. 2004;49(1):457–81.

    Article  CAS  Google Scholar 

  4. 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. Rev Inst Med Trop Sao Paulo. 2011;53:325–7.

    Article  PubMed  Google Scholar 

  5. Speare R, Harrington H, Canyon D, Massey PD. A systematic literature review of pediculosis due to head lice in the Pacific Island Countries and territories: what country specific research on head lice is needed? BMC Dermatol. 2014;14:1–6.

    Article  Google Scholar 

  6. Bartosik K, Zając Z, Kulisz J. Head pediculosis in schoolchildren in the eastern region of the European Union. Ann Agric Environ Med. 2015;22(4).

  7. Moussa S, El-Edailli S, Alshammari R, AlObaidi S, Al-Reshidi HF, Alshammari HN. Knowledge and behavioral practice of pediculosis in Hail Region, Saudi Arabia. Int J Med. 2018;4(5):11–21.

    Google Scholar 

  8. Khamaiseh AM. Head lice among governmental primary school students in southern Jordan: prevalence and risk factors. J Glob Infect Dis. 2018;10(1):11–5.

    Article  PubMed  PubMed Central  Google Scholar 

  9. Ismail MT, Kabakibi MM, Al-Kafri A. Epidemiology of pediculosis capitis among schoolchildren in Damascus, Syria. Indian J Pediatr Dermatology. 2018;19(4):331–4.

    Article  Google Scholar 

  10. Özdemir A, Ünal E, Çeki L. The prevalence of Pediculus Capitis and Personal Hygiene Status in TwoVocational High Schools. Int J Caring Sci. 2019;12(2).

  11. Hama-Karim YH, Azize PM, Ali SI, Ezzaddin SA. Epidemiological Study of Pediculosis among primary School children in Sulaimani Governorate, Kurdistan Region of Iraq. J Arthropod-Borne Dis. 2022;16(1):72.

    PubMed  PubMed Central  Google Scholar 

  12. Amirkhani M, Alavian S, Maesoumi H, Aminaie T, Dashti M, Ardalan G, et al. A nationwide survey of prevalence of pediculosis in children and adolescents in Iran. Iran Red Crescent Med J. 2011;13(3):167.

  13. Moosazadeh M, Afshari M, Keianian, Nezammahalleh H, Enayati A. Prevalence of head lice infestation and its associated factors among primary school students in Iran: a systematic review and meta-analysis. Osong Public Health Res Perspect. 2015;6(6):346–56.

  14. Nasirian H, Ahmadi SAY. Pediculus capitis (Anoplura: Pedicullidae) infestation in preschool and primary school students and the community: a global-scale evidence review. Int J Trop Insect Sci. 2024;44(2):441–536.

  15. Hodjati MH, Mousavi N, Mousavi M. Head lice infestation in school children of a low socioeconomy area of Tabriz city, Iran. Afr J Biotechnol. 2008;7:13.

    Google Scholar 

  16. Lashari MH, Sial N, Akhtar MS, Siddique F, Nawaz M, Yousaf M et al. Prevalence of head lice among school children. Gomal J Med Sci. 2015;13(4).

  17. Rassami W, Soonwera M. Epidemiology of pediculosis capitis among schoolchildren in the eastern area of Bangkok, Thailand. Asian Pac J Trop Biomed. 2012;2(11):901–4.

    Article  PubMed  PubMed Central  Google Scholar 

  18. Saddozai S, Kakarsulemankhel JK. Infestation of head lice, Pediculus humanus capitis, in school children at Quetta city and its suburban areas, Pakistan. Pakistan J Zool. 2008;40(1):45.

    Google Scholar 

  19. Gunning K, Pippitt K, Kiraly B, Sayler M. Pediculosis and scabies: a treatment update. Am Fam Physician. 2012;86(6):535–41.

    PubMed  Google Scholar 

  20. Bohl B, Evetts J, McClain K, Rosenauer A, Stellitano E. Clinical practice update: pediculosis capitis. Pediatr Nurs. 2015;41(5):227.

    PubMed  Google Scholar 

  21. Clark JM. Permethrin resistance due to knockdown gene mutations is prevalent in human head louse populations. Open Dermatology J. 2010;4(1).

  22. Limoee M, Davari B, Moosa-Kazemi SH. Toxicity of pyrethroid and organophosphorous insecticides against two field collected strains of the German cockroach Blattella germanica (Blattaria: Blattellidae). J Arthropod-Borne Dis. 2012;6(2):112.

    PubMed  PubMed Central  Google Scholar 

  23. Picollo M, Vassena C, Casadio A, Massimo J, Zerba E. Laboratory studies of susceptibility and resistance to insecticides in Pediculus capitis (Anoplura; Pediculidae). J Med Entomol. 1998;35(5):814–7.

    Article  CAS  PubMed  Google Scholar 

  24. Downs A, Stafford K, Hunt L, Ravenscroft J, Coles G. Widespread insecticide resistance in head lice to the over-the‐counter pediculocides in England, and the emergence of carbaryl resistance. Br J Dermatol. 2002;146(1):88–93.

    Article  CAS  PubMed  Google Scholar 

  25. Eremeeva ME, Warang SS, Anderson ML, Capps D, Zohdy S, Durden LA. Molecular survey for pathogens and markers of permethrin resistance in human head lice (Phthiraptera: Pediculidae) from Madagascar. J Parasitol. 2019;105(3):459–68.

    Article  CAS  PubMed  Google Scholar 

  26. Roca-Acevedo G, del Solar Kupfer CP, Dressel Roa P, Toloza AC. First determination of pyrethroid knockdown resistance alleles in human head lice (Phthiraptera: Pediculidae) from Chile. J Med Entomol. 2019;56(6):1698–703.

    Article  CAS  PubMed  Google Scholar 

  27. Larkin K, Rodriguez CA, Jamani S, Fronza G, Roca-Acevedo G, Sanchez A, et al. First evidence of the mutations associated with pyrethroid resistance in head lice (Phthiraptera: Pediculidae) from Honduras. Parasites Vectors. 2020;13(1):1–7.

    Article  Google Scholar 

  28. Ponce-Garcia G, Villanueva-Segura K, Trujillo-Rodriguez G, Rodriguez-Sanchez IP, Lopez-Monroy B, Flores AE. First detection of the kdr mutation T929I in head lice (Phthiraptera: Pediculidae) in schoolchildren of the metropolitan area of Nuevo Leon and Yucatan, Mexico. J Med Entomol. 2017;54(4):1025–30.

    Article  CAS  PubMed  Google Scholar 

  29. Yingklang M, Gordon CN, Jaidee PH, Thongpon P, Pinlaor S. Comparative efficacy of chemical and botanical pediculicides in Thailand and 4% dimeticone against head louse, Pediculus humanus capitis. PLoS ONE. 2023;18(6):e0287616.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Farnham AW. Genetics of resistance of houseflies (Musca domestica L.) to pyrethroids. I. knock-down resistance. Pest Sci. 1977;8(6):631–6.

    Article  Google Scholar 

  31. Dong K, Du Y, Rinkevich F, Nomura Y, Xu P, Wang L, et al. Molecular biology of insect sodium channels and pyrethroid resistance. Insect Biochem Mol Biol. 2014;50:1–17.

    Article  PubMed  PubMed Central  Google Scholar 

  32. Catterall WA. From ionic currents to molecular mechanisms: the structure and function of voltage-gated sodium channels. Neuron. 2000;26(1):13–25.

    Article  CAS  PubMed  Google Scholar 

  33. Du Y, Garden D, Khambay B, Zhorov BS, Dong K. Batrachotoxin, pyrethroids, and BTG 502 share overlapping binding sites on insect sodium channels. Mol Pharmacol. 2011;80(3):426–33.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Davies T, Field L, Usherwood P, Williamson M. DDT, pyrethrins, pyrethroids and insect sodium channels. IUBMB Life. 2007;59(3):151–62.

    Article  CAS  PubMed  Google Scholar 

  35. Dong K. Insect sodium channels and insecticide resistance. Invert Neurosci. 2007;7:17–30.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. 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). J Med Entomol. 2017;54(5):1337–43.

    Article  CAS  PubMed  Google Scholar 

  37. Li T, Zhang L, Reid WR, Xu Q, Dong K, Liu N. Multiple mutations and mutation combinations in the sodium channel of permethrin resistant mosquitoes, Culex quinquefasciatus. Sci Rep. 2012;2(1):781.

    Article  PubMed  PubMed Central  Google Scholar 

  38. Yoon KS, Gao J-R, Lee SH, Clark JM, Brown L, Taplin D. Permethrin-resistant human head lice, Pediculus capitis, and their treatment. Arch Dermatol. 2003;139(8):994–1000.

    Article  CAS  PubMed  Google Scholar 

  39. Kim HJ, Symington SB, Lee SH, Clark JM. Serial invasive signal amplification reaction for genotyping permethrin-resistant (kdr-like) human head lice, Pediculus capitis. Pestic Biochem Physiol. 2004;80(3):173–82.

    Article  CAS  Google Scholar 

  40. Ghavami MB, Panahi S, Nabati SM, Ghanbari M, Taghiloo B. A comprehensive survey of permethrin resistance in human head louse populations from northwest Iran: ex vivo and molecular monitoring of knockdown resistance alleles. Parasites Vectors. 2023;16(1):57.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Ghahvechi Khaligh F, Djadid ND, Farmani M, Asadi Saatlou Z, Frooziyan S, Abedi Astaneh F, et al. Molecular monitoring of knockdown resistance in head louse (Phthiraptera: Pediculidae) populations in Iran. J Med Entomol. 2021;58(6):2321–9.

    Article  PubMed  Google Scholar 

  42. Lee SH, Gao J-R, Yoon KS, Mumcuoglu KY, Taplin D, Edman JD, et al. Sodium channel mutations associated with knockdown resistance in the human head louse, Pediculus capitis (De Geer). Pestic Biochem Physiol. 2003;75(3):79–91.

    Article  CAS  Google Scholar 

  43. Thompson J, Gibson T, Higgins D. Multiple sequence alignment using ClustalW and ClustalX. Curr. Protoc. Bioinformatics Chap. 2: Unit 2.3. 2002.

  44. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol. 2013;30(12):2725–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Leung AK, Fong JH, Pinto-Rojas A. Pediculosis capitis. J Pediatr Health Care. 2005;19(6):369–73.

    Article  PubMed  Google Scholar 

  46. Soleimani-Ahmadi M, Jaberhashemi SA, Zare M, Sanei-Dehkordi A. Prevalence of head lice infestation and pediculicidal effect of permethrine shampoo in primary school girls in a low-income area in southeast of Iran. BMC Dermatol. 2017;17(1):1–6.

    Article  Google Scholar 

  47. Morsy TA, El-Ela R, Mawla M, Khalaf S. The prevalence of lice infesting students of primary, preparatory and secondary schools in Cairo, Egypt. J Egypt Soc Parasitol. 2001;31(1):43–50.

    CAS  PubMed  Google Scholar 

  48. Al-Maktari MT. Head louse infestations in Yemen: prevalence and risk factors determination among primary schoolchildren, Al-Mahweet Governorate, Yemen. J Egypt Soc Parasitol. 2008;38(3):741–8.

    PubMed  Google Scholar 

  49. Al Bashtawy M, Hasna F. Pediculosis capitis among primary-school children in Mafraq Governorate, Jordan. East Mediterr Health J. 2012;18(1):43–8.

    Article  CAS  PubMed  Google Scholar 

  50. Alzain B. Pediculosis capitis infestation in school children of a low socioeconomic area of the North Gaza Governorate. Turk J Med Sci. 2012;42(7):1286–91.

    Google Scholar 

  51. Firoozfar F, Moosa-Kazemi SH, Bahrami A, Yusuf MA, Saghafipour A, Armoon Z et al. Head lice infestation (Pediculus humanus capitis) prevalence and its associated factors, among the Kormanj tribes in North Khorasan Province. Shiraz E Med J. 2019;20(4).

  52. Kamiabi F, Nakhaei FH. Prevalence of pediculosis capitis and determination of risk factors in primary-school children in Kerman. EMHJ-Eastern Mediterranean Health Journal, 11 (5–6), 988–992, 2005. 2005.

  53. Mohammadi J, Azizi K, Alipour H, Kalantari M, Bagheri M, Shahriari-Namadi M et al. Frequency of pyrethroid resistance in human head louse treatment: systematic review and meta-analysis. Parasite. 2021;28.

  54. Toloza A, Vassena C, Gallardo A, González-Audino P, Picollo MI. Epidemiology of pediculosis capitis in elementary schools of Buenos Aires, Argentina. Parasitol Res. 2009;104(6):1295–8.

    Article  PubMed  Google Scholar 

  55. Gulgun M, Balci E, Karaoglu A, Babacan O, Turker T. Pediculosis capitis: prevalence and its associated factors in primary school children living in rural and urban areas in Kayseri, Turkey. Cent Eur J Public Health. 2013;21(2).

  56. Raheem AE, El Sherbiny TA, Elgameel NA, El-Sayed A, Moustafa GA, Shahen N. Epidemiological comparative study of pediculosis capitis among primary school children in Fayoum and Minofiya governorates, Egypt. J Community Health. 2015;40:222–6.

    Article  PubMed  Google Scholar 

  57. Vahabi A, Shemshad K, Sayyadi M, Biglarian A, Vahabi B, Sayyad S, et al. Prevalence and risk factors of Pediculus (humanus) capitis (Anoplura: Pediculidae), in primary schools in Sanandaj City, Kurdistan Province, Iran. Trop Biomed. 2012;29(2):207–11.

    CAS  PubMed  Google Scholar 

  58. Davarpanah MA, Kazerouni AR, Rahmati H, Neirami RN, Bakhtiary H, Sadeghi M. The prevalence of pediculus capitis among the middle schoolchildren in Fars Province, southern Iran. Caspian J Intern Med. 2013;4(1):607.

    PubMed  PubMed Central  Google Scholar 

  59. Sim S, Lee W-J, Yu J-R, Lee IY, Lee SH, Oh S-Y, et al. Risk factors associated with head louse infestation in Korea. Korean J Parasitol. 2011;49(1):95–8.

    Article  PubMed  PubMed Central  Google Scholar 

  60. Norsa’adah Bachok RBN, Ibrahim CWANA, Naing L. Prevalence and associated factors of head lice infestation among primary schoolchildren in Kelantan, Malaysia. Southeast Asian J Trop Med Public Health. 2006;37(3):536–43.

    Google Scholar 

  61. Kitvatanachai S, Kritsiriwutthinan K, Taylor A, Rhongbutsri P. Head Lice Infestation in Pre-High School Girls, Lak Hok Suburban Area, Pathum Thani Province, in Central Thailand. Journal of Parasitology Research. 2023;2023.

  62. Moemenbellah-Fard M, Nasiri Z, Azizi K, Fakoorziba M. Head lice treatment with two interventions: pediculosis capitis profile in female schoolchildren of a rural setting in the south of Iran. Annals Trop Med Public Health. 2016;9(4).

  63. Chosidow O, Brue C, Chastang C, Bouvet E, Izri M, Rousset J, et al. Controlled study of malathion and d-phenothrin lotions for Pediculus humanus var capitis-infested schoolchildren. Lancet. 1994;344(8939–8940):1724–7.

    Article  CAS  PubMed  Google Scholar 

  64. Rupes V, Moravec J, Chmela J, Ledvinka J, Zelenkova J. A resistance of head lice (Pediculus capitis) to permethrin in Czech Republic. Cent Eur J Public Health. 1995;3(1):30–2.

    CAS  PubMed  Google Scholar 

  65. Downs A, Stafford K, Coles G. Head lice: prevalence in schoolchildren and insecticide resistance. Parasitol Today. 1999;15(1):1–4.

    Article  CAS  PubMed  Google Scholar 

  66. Hemingway J, Miller J, Mumcuoglu K. Pyrethroid resistance mechanisms in the head louse Pediculus capitis from Israel: implications for control. Med Vet Entomol. 1999;13(1):89–96.

    Article  CAS  PubMed  Google Scholar 

  67. Pollack RJ, Kiszewski A, Armstrong P, Hahn C, Wolfe N, Rahman HA, et al. Differential permethrin susceptibility of head lice sampled in the United States and Borneo. Arch Pediatr Adolesc Med. 1999;153(9):969–73.

    Article  CAS  PubMed  Google Scholar 

  68. Williamson MS, Martinez-Torres D, Hick CA, Devonshire AL. Identification of mutations in the housefly para-type sodium channel gene associated with knockdown resistance (kdr) to pyrethroid insecticides. Mol Gen Genet MGG. 1996;252:51–60.

    Article  CAS  PubMed  Google Scholar 

  69. Martinez-Torres D, Chandre F, Williamson M, Darriet F, Berge JB, Devonshire AL, et al. Molecular characterization of pyrethroid knockdown resistance (kdr) in the major malaria vector Anopheles gambiae Ss. Insect Mol Biol. 1998;7(2):179–84.

    Article  CAS  PubMed  Google Scholar 

  70. Clark JM, Yoon K, Lee S, Pittendrigh B. Human lice: past, present and future control. Pestic Biochem Physiol. 2013;106(3):162–71.

    Article  CAS  Google Scholar 

  71. Gholizadeh S, Nouroozi B, Ladonni H. Molecular detection of knockdown resistance (kdr) in Blattella germanica (Blattodea: Blattellidae) from northwestern Iran. J Med Entomol. 2014;51(5):976–9.

    Article  CAS  PubMed  Google Scholar 

  72. Rosdahl N. DDT-resistent head lice. Ugeskr Laeger. 1975;137(34):1931–3.

    CAS  PubMed  Google Scholar 

  73. Lane RP, Crosskey RW. Medical insects and arachnids. Springer Science & Business Media; 2012.

Download references

Acknowledgements

Our gratitude extends to the Torbat-e Heydarieh University of Medical Sciences, as well as the dedicated administrators, authorities, and staff members of the Torbat-e Heydarieh, Mahvelat, and Zaveh Health Care Network.

Funding

The present research has received a financial support from the “School of Public Health, Urmia University of Medical Sciences, Urmia, Iran” (Research code: 2175).

Author information

Authors and Affiliations

  1. Cellular & Molecular Research Center, Cellular and Molecular Medicine Research Institute, Urmia University of Medical Sciences (UMSU), P. O. Box: 5756115198, Urmia, Iran

    Mohammad Taheri & Saber Gholizadeh

  2. Department of Vector Biology and Control of Diseases, School of Public Health, Urmia University of Medical Sciences, Urmia, Iran

    Mohammad Taheri, Fereshteh Ghahvechi Khaligh, Mehdi Badakhshan & Saber Gholizadeh

  3. Department of Vector Biology and Control of Diseases, School of Public Health, Tehran University of Medical Sciences, Tehran, Iran

    Ahmad Ali Hanafi-Bojd & Kamal Dashti

  4. Zoonoses Research Center, Tehran University of Medical Sciences, Tehran, Iran

    Ahmad Ali Hanafi-Bojd

  5. Department of Biostatistics and Epidemiology, School of Medicine, Urmia University of Medical Sciences, Urmia, Iran

    Hamid Reza Khalkhali

  6. Social Determinants of Health Research Center, Clinical Research Institute, Urmia University of Medical Sciences, Urmia, Iran

    Fereshteh Ghahvechi Khaligh & Mehdi Badakhshan

Authors
  1. Mohammad Taheri
    View author publications

    You can also search for this author inPubMed Google Scholar

  2. Fereshteh Ghahvechi Khaligh
    View author publications

    You can also search for this author inPubMed Google Scholar

  3. Ahmad Ali Hanafi-Bojd
    View author publications

    You can also search for this author inPubMed Google Scholar

  4. Hamid Reza Khalkhali
    View author publications

    You can also search for this author inPubMed Google Scholar

  5. Kamal Dashti
    View author publications

    You can also search for this author inPubMed Google Scholar

  6. Mehdi Badakhshan
    View author publications

    You can also search for this author inPubMed Google Scholar

  7. Saber Gholizadeh
    View author publications

    You can also search for this author inPubMed Google Scholar

Contributions

Mohammad Taheri, Hamidreza Khalkhali, Ahmad Ali Hanafi-Bojd and Saber Gholizadeh designed and supervised the project. MT and KD collected the samples. MT, FGK and MB prepared and identified the samples. MT and FGK performed the bioinformatics and statistical analyses and interpreted the data. HK, AAHB and SG drafted the study. SG and MB revised the study for important content.

Corresponding author

Correspondence to Saber Gholizadeh.

Ethics declarations

Ethics approval and consent to participate

The study was granted approval by the Ethics Committee of the Research Department of the School of Public Health, Urmia University of Medical Sciences, with permit number: IR.UMSU.REC.1396.94. Participants signed a written informed consent form before participating in the study, in accordance with the guidelines of the Declaration of Helsinki.

Consent for publication

This paper is not contains any individual personal data in any form.

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License, which permits any non-commercial use, sharing, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if you modified the licensed material. You do not have permission under this licence to share adapted material derived from this article or parts of it. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by-nc-nd/4.0/.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Taheri, M., Ghahvechi Khaligh, F., Hanafi-Bojd, A.A. et al. Epidemiological analysis of pediculosis and the distribution of kdr mutation frequency in head lice populations in Torbat Heydarieh city of Khorasan Razavi Province, Northeastern Iran. BMC Res Notes 17, 323 (2024). https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s13104-024-06940-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s13104-024-06940-3

Keywords

BMC Research Notes

ISSN: 1756-0500

Contact us