Head lice treatment with two interventions: Pediculosis capitis profile in female schoolchildren of a rural setting in the south of Iran

Background: Previous research suggests that certain communities, including rural residents, exhibit endemic infestations which can be prevented by banned interventions such as the use of certain chlorinated lice-killing chemicals. The aim of this study was to evaluate two different treatments on head lice among primary school girls of Lar, Fars Province, south of Iran. Patients and Methods: Lindane (1%) or permethrin (1%) shampoos were used on two groups who were treated for live head lice after screening with plastic lice detection combs at schools. A questionnaire form on the epidemiologic factors was included. The outcomes were followed up for 2 weeks from the initial treatment on days 2, 6, 9, and 14. Data analyses were performed using analysis of variance (ANOVA) and Kruskal–Wallis tests. A P value <0.05 was considered to be statistically significant. Results: From 2,084 students examined, 82 girls (3.93%) were infested with pediculosis. No significant correlation was found between head lice infestation level and hair length, hair style, itching, family size, education grade, and age. The data on days 2, 6, 9, and 14 from permethrin and lindane treatments were 71.8%, 64.1%, 89.7%, and 89.7% versus 92.5%, 92.5%, 97.5%, and 95%, respectively. On days 2 (P = 0.017) and 6 (P = 0.002) after treatment, significant differences were noted on reexamination of the cases. Only one reinfestation case was identified during the treatment period. The level of insensitivity to permethrin was twice that of lindane at the end of this period. Conclusion: The level of cure in treated students was similar for both shampoos. Lindane swiftly acted to reduce the level of infested cases by the second day.

Keywords: Head lice, Iran, lindane, pediculicide, pediculus humanus capitis, permethrin

It is a common practice to conduct new clinical trials in an area where the product will be used by natives. Moreover, health authorities often need data from these regions to assess the situation at a given time. In the case of treatments for head lice, which is an obligate blood-sucking ectoparasite on man,^[1] in most high-income countries the prior application of insecticides has naturally selected populations of head lice that have developed resistance to one or more active ingredients; so tests performed in a remote region where these have not been used extensively, or at all, may deliver an outcome different from that in a country where insecticides are widely applied.

Human head lice infestation, known as pediculosis capitis, caused by Pediculus humanus capitis De Geer, 1778 (Anoplura: Pediculidae) is a common public health problem that occurs in people of all ages and socioeconomic groups.^[2] It is, however, more commonly found among female primary schoolchildren aged 3-11 years.^[3] It is endemic in many parts of the world.^[4] Infestations have been reported from many regions including Iran ^[5],[6],[7] where many other infectious and noninfectious diseases also prevail.^{[8],[9],[10],[11],[12],[13],[14]} This problem has a strong impact on the health of school students and students’ attendance since it is contagious. It can lead to secondary bacterial and fungal infections if left untreated.^[2] There is unequivocal evidence on the emergence of strains of head lice resistant to many pediculicides.^[15],[16] Resistance to permethrin in head lice was first reported in France in 1994 and all over the world thereafter.^[17] A knockdown resistance (kdr) gene mutation is only associated with pyrethroid resistance in head lice.^[18],[19]

Lindane is a low-cost treatment for head lice. It affects the neurons of the insects. Permethrin is also used in Iran as an over-the-counter product for head lice infestation treatment. Both lindane and permethrin insecticides are safe to use intermittently in specific settings.^[20] The main aims of the present study were to show head lice infestation treatment with lindane (1%) and permethrin (1%) shampoos and to explore the role of epidemiologic factors of pediculosis among female primary school students of Lar, Fars Province, southern Iran.

Study area

The present research was performed in the county of Lar (27°40’N, 54°20’E, at an altitude of 900 m above sea level) about 340 km to the southeast of Shiraz, the capital city of Fars Province, southern Iran, from mid-December 2013 to mid-January 2014 [Figure 1]. Lar has a least dense population (<15 persons/km ²) of Iranian tribes. Its population was 226,879 in 2006. The annual mean relative humidity is 63% and its annual mean temperature is 23°C.

Participants

This study was a randomized, single (assessor)-blind study to determine the effectiveness of lindane (1%) versus permethrin (1%) shampoos for treatment against head lice. Since the coverage of all school students was hard to achieve, a representative sample of 13 female primary schools was randomly selected and all these schools’ enrolled students (2,084 persons) were screened and subsequently treated for the presence of live head lice by using standard plastic detection combs (PDC) (Thornton & Ross Ltd., Huddersfield, UK) [Figure 2]. All students were given an information leaflet to take home so that every eligible family member likely to be positive with head lice could visit the school for free treatment. All infested students and family members could take part in the trial; the latter were excluded from the analyses. A signed informed consent and assent method was also included in line with the revised Declaration of Helsinki. Epidemiological characteristics were recorded in a form including the infestation level, hair length, hair style, itching level, family size, and age.

The inclusion criteria for this study were female primary school students aged 7-12 years with one or more live head lice present by using PDC following a standardized procedure set out below. The exclusion criteria were sensitivity to any product, dermal disorder, secondary bacterial infection, favism (glucose 6 phosphate dehydrogenase, or G6PD, deficiency), use of any drug or pediculicide within the previous 4 weeks, and the use of hair colors, bleach, or gels.

Sample size and randomization

A sample size of about 70 infested individuals was calculated to be enough. The randomization scheme was generated using a table of random numbers with 10 blocks of nine random numbers. Unmarked 60 mL bottles of clinical trial material were labeled with patient numbers including the initials of index patients. Each session included complete blocks of nine bottles of clinical trial material to ascertain that each treatment was thoroughly randomized in the participants. All patients had equal probability of allocation to the groups. The participants were completely unaware of which treatment groups they belonged to. The field assessor was also blinded.

Interventions

Participants with head lice were randomized to get either one of the two shampoos (lindane 1% or permethrin 1%) each with two applications with 7 days in between. Both these are used as over-the-counter (OTC) products present in the main Iranian markets. They were used according to the manufacturers’ recommendations. Sufficient amounts of these products were applied, a few drops each time to the base of dry hair to moisten the whole scalp and length of the hair by using a normal comb to spread the solutions evenly. In the treatment, lindane and permethrin were allowed to remain for 4 min and 10 min respectively; the hair was then washed off and allowed to dry naturally.

Outcomes

At first, an evaluation of the intensity of infestation was based on the frequency with which head lice were found during initial combing. This was used on screening and on posttreatment days in line with previous studies. Heavy infestation was when >1 louse was found in the first stroke of the PDC comb, medium infestation was when only 1 louse was found in the first stroke of the comb, and light infestation was when 1 louse was found only after five to six strokes of the comb.^[21]

Each patient was assessed for the presence of head lice on days 2, 6, 9, and 14 following the first treatment using the PDC comb on dry hair in the same manner in which the initial screening was performed in the schools. The main aims of restricted combing on these days were to follow up and record data on the status of head lice infestation under each treatment regime. Each interim combing evaluation involved drawing the PDC comb two to three times through each tuft of hair. This limited dry combing had minimal intervention effect; more frequent combing could have interfered with the results.^[22] In contrast, more combing repetition on day 14 was essential to ensure absence of head lice. The primary outcome criterion was elimination of live head lice with two applications of each treatment. “Cure” was defined as no viable head lice following the second application in the treatment on days 9 and 14. Reinfestation was defined when on days 9 or 14, no more than two adult lice or a third nymph head lice were or was removed from patients who had no infestation following the initial treatment.

The secondary outcome measures involved the reduction of pruritus severity, clinical pathology, and reported adverse events. The degree of itching was evaluated using a visual analog scale as outlined before.^[23] Clinical pathology was the presence of erythema, eczema, and dermal weal. Adverse events such as intolerable irritation included all safety-related factors, which could result from or hinder treatments.

Statistical analysis

This descriptive analytical study included estimating the mean, standard deviation, frequency, and percentage to describe demographic variables in infested participants. One-way analysis of variance (ANOVA) was applied to compare the age with the level (heavy, medium, and light) of infestation in students. For graded or semi-continuous variables, the Kruskal–Wallis ANOVA test was also conducted to determine any statistical difference between the two treatment protocols over the entire period. The Statistical Package for the Social Sciences (SPSS) version 17 was used to analyze the data. A P value of <0.05 was considered to be significant in all tests.

From a total population of 2,084 female primary school students screened for head lice infestation at Lar, only 82 patients (3.93%) were found to be positive for live head lice. On or immediately after the first treatment, three of them were omitted (two persons due to favism and one dropout on day 2). Overall, 79 participants completed the study as required by the protocol. No significant statistical relationship was seen between the different epidemiological variables and the infestation level [Table 1]. The participants had an age range of 7-12 years [Figure 3], the majority (47.6%) of whom had long hair that extended below their shoulders. The medium level of infestation (only one louse/ first stroke) was the most frequent (58.5%) type among all participants. A high proportion of infested participants (40.2%) were initially suffering from grade IV (high) itching level [Table 2]. About a quarter (24.4%) of all infested participants was found to be in the high itching and medium infestation group. Most infested students (78%) also had straight hair. The majority (74.4%) of the patients had a family size of four to six persons. In an 8-year old student suffering from very high itching with straight hair up to her shoulders with a family size of five members, 13 live head lice were located.

Baseline data

Demographic characteristics of the sample population at the baseline are presented in [Table 1]. The groups were generally similar with no significant difference. There was, however, a nonsignificant trend for a larger proportion of children with long straight hair compared to the other groups. There was also a significant (P < 0.01) difference between the groups with respect to “high” level of itching.

Outcomes

Seventy-nine participants were followed up in this study. Two groups comprising 40 patients and 39 patients were allocated to lindane 1% and permethrin 1% treatments, respectively. Of these 39/40 (97.5%) and 38/40 (95%) of the lindane 1% group were free from head lice on assessment days 9 and 14 after the second treatment on the day 7 [Figure 4]. In contrast, 35/39 (89.7%) of the permethrin 1% group were free from head lice on days 9 and 14 following the second treatment on day 7 [Table 3]. There was no significant statistical difference between the two protocols on these posttreatment days (P > 0.05). Initial assessment revealed that after the first treatments on days 2 and 6, significant statistical differences were found between the two protocols with probabilities of 0.017 and 0.002, respectively. So while 28/39 (71.8%) and 25/39 (64.1%) of the permethrin 1% group were lice-free on assessment days 2 and 6 after the first treatment on day 1, 37/40 (92.5%) of the lindane 1% group were lice-free on the same days. The differences of 20.7% on day 2 and 28.4% on day 6 represent a meaningful shift in activity between the two protocols. Therefore, lindane effectiveness outweighed that of the permethrin on days 2 and 6 following the first treatment. Moreover, the level of insensitivity to permethrin (10.26%) was twice that of lindane (5%) at the end of this treatment period [Figure 5]. From the two patients who were not cured in the lindane group, only one was identified as a reinfestation case because she has been free from live head lice from assessment days 2-9. Given that treatments were terminated on day 9 after the second application of the product, family contact could be implicated as a source of reinfestation.

After the treatments were terminated, the degree of itching was restricted to only five patients (6.3%) who had severe dandruff complications. The medium level of infestation (one louse/ first stroke) was still the main type among all remaining participants at the end of the treatment period.

The relatively high effectiveness of lindane 1% found in the resource-poor setting of this study area was a contrast to the results from a systematic review of other clinical trials.^[24] The primary conclusion from this review was that permethrin was the only insecticide sufficiently effective to justify its use. All of the studies cited there were performed in resource-rich settings of the developed world. A single clinical trial on pediculosis capitis with 1% permethrin cream rinse was found to be therapeutically more effective than the single application of 1% lindane shampoo.^[25] The present investigation shows that the action of lindane immediately after the first treatment on days 2 and 6 was significantly more effective in curbing head lice infestations than permethrin 1% shampoo. The logic of using PDC combs instead of the often flawed visual inspection is now well-grounded and of paramount importance among many head lice researchers.^[26] Many earlier reports unacceptable by Cochrane reviewers indicate, however, that permethrin treatment is both more effective and better tolerated than lindane therapy.^{[27],[28],[29]} Lindane is an organochlorine insecticide, which induces excess central nervous system stimulation in head lice and finally cause their death. This insecticide, which was once the prime source of head lice elimination in high-income countries of the world, has virtually been replaced by more favorable and highly efficacious new physical, rather than chemical, agents such as dimeticone.^[30] Lindane use has been banned by the European Union since 2007.^[3]

The patterns of resistance differ geographically.^[31] In countries where resistance to lindane or permethrin has been well-known since long, such as the UK, a new physical product may perform better. In contrast, in rural problematic areas of the developing countries where lack of application of these chemical insecticides persists, head lice population is expected to be susceptible to these products. So the level of resistance to lindane is minimal. It is believed that the difference in effectiveness seen between lindane and permethrin in the present study reflects the failure of permethrin to kill all head lice on the scalp. It is possible that permethrin has been used moderately extensively in this community or in the recent past, which could have induced resistance. Information on this aspect of pediculicide use is, however, lacking. This resulted in persistence of infestation in the children treated with this insecticide, in particular when the intensity of infestation was high. Permethrin resistance cannot, however, be rejected although it appears to be unlikely since the resistance of head lice to insecticides has never been studied systematically in southern Iran.

The quality of some studies conducted earlier on comparative lindane and permethrin therapy could have been seriously flawed both methodologically and conceptually, as indicated before. [24,29]The use of PDC comb was instrumental without which it would have been impossible to achieve the present data. In the present randomized single-blind clinical trial, the comparative effectiveness of the two tested compounds in curbing head lice infestation is emphasized. To the best of the authors’ knowledge no previous study has been conducted so far on this subject in Iran. The application of physical rather than chemical products to control head lice is highly recommended in the future.

It is concluded that the level of cure in treated students was similar for both the shampoos at the end of the therapeutic period. Lindane swiftly acted to reduce the level of infested cases by the second day after the first treatment. Although head lice cure is hard to achieve, more studies are required in this arena.

Acknowledgements

This paper was extracted from the data of an approved M. Sc. student thesis (No: 92-6876, Date: 5-2-2012) conducted by the second author, Ms. Zahra Nasiri. It was documented in the Iranian Registry of Clinical Trials (IRCT) under the registration number: IRCT2015010816372N2. It was financially supported by Shiraz University of Medical Sciences (SUMS). We owe thanks to the Vice-Chancellor for research and technology at SUMS and for permitting the use of the facilities at the university, Ms. T Dabaghmanesh for help with office work, Dr. S. Keshavarzi for statistical assistance, Dr. A Soltani for criticism, and Ms. Z Soltani and Mr. K. Safari who helped with the launch of this research.

Financial support and sponsorship

Nil.

Conflicts of interest

No conflict or competing financial interest exists.

Source of Support: None, Conflict of Interest: None

DOI: 10.4103/1755-6783.184790

[Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5]

[Table 1], [Table 2], [Table 3]