Parasitology Research

, Volume 110, Issue 5, pp 1601–1606 | Cite as

Comparative efficacy of new commercial pediculicides against adults and eggs of Pediculus humanus capitis (head lice)

  • Anabella Gallardo
  • Gastón Mougabure-Cueto
  • Claudia Vassena
  • María Inés Picollo
  • Ariel Ceferino Toloza
Original Paper

Abstract

The use of pyrethroids to control head louse infestations have suffered considerable loss of efficacy due to the development of resistance. In the last past years, several new alternative products to synthetic pyrethroids have been developed and are sold in the Argentinean market against head lice. The present study investigated the efficacy of two new Argentinean products Nopucid Qubit® and Nopucid Bio Citrus® and its comparison with two reference products Nyda® and Hedrin®. Nopucid Qubit® is a two-phase lotion containing geraniol and citronellol (phase 1) and ciclopentaxiloxane (phase 2); while Nopucid Bio Citrus® contains dimethicone, ciclopentaxiloxane, and bergamot essential oil. These products are physically acting compounds. The sensitivity of two laboratory assays for testing insecticide activity of new formulations was also compared. Mortality (100%) of motile forms occurred after they were exposed to any product for 1 and 2 min, either by in vitro or ex vivo test. Concerning ovicidal activity, the most effective pediculicides were Nopucid Bio Citrus® and Nyda®, followed by Hedrin® and Nopucid Qubit®. The present study revealed, for the first time, the efficacy of over-the-counter commercial pediculicides available in Argentine (Nopucid Bio Citrus® and Nopucid Qubit®) on either motile stages or eggs against head lice.

Introduction

Head lice infestation is caused by the ectoparasite Pediculus humanus capitis De Geer, an insect that live on the head of humans and feed on the scalp. Infestation is more common in schoolchildren between the ages of 4 and 13 and can be found in any sex, race, or social class (Burgess 2004; Mumcuoglu et al. 2009). However, girls are more frequently infested than boys (Downs et al. 1999; Mumcuoglu et al. 2001). Normally, head louse transmission occurs by direct host-to-host contact (Takano-Lee et al. 2005). Even though there are no direct evidence that head lice can act as vectors, experimental tests has shown that they can act as vectors of Rickettsia prowazekii and Bartonella quintana, the causative agents of typhus and trench fever (Robinson et al. 2003; Sasaki et al. 2006). Nowadays, there is an increase in head louse prevalence worldwide due to the lack of efficacy of pediculicides containing synthetic insecticides (Falagas et al. 2008). The low effectiveness is a consequence of the development of resistance against long-used insecticides like pyrethroids (permethrin and deltamethrin) and organophosphorus (malathion) (Burgess 2004, 2009; Heukelbach 2010). Considering an annual rate of 15 million infestations with head lice and a cost of 150 US dollars per treatment in the USA, the associated direct and indirect costs of treatment are estimated to be of around US$ 2,250 million (West 2004; Gur and Schneeweiss 2009). In practice, and historically, most of the registered pediculicides contain insecticides with neurotoxic mode of action. However, recent active substances like silicon derivates or essential oils have been developed (Burgess 2004; Toloza et al. 2006, 2010; Semmler et al. 2009; Abdel-Ghaffar et al. 2010). The efficacy of commercial pediculicide containing dimeticone was demonstrated by different laboratory assays (Asenov et al. 2010; Oliveira et al. 2007). These products showed to be highly effective against head lice as compared to neurotoxic insecticides (Burgess 2009; Heukelbach 2010; González-Audino et al. 2011).

In Argentina, the market of pediculicide products decreased from 1997 to 2000 due to the development of insecticide resistance (Picollo et al. 1998, 2000). In addition, pediculosis is a serious sanitary problem affecting more than 30% of the schoolchildren and has epidemic status (Toloza et al. 2009). In the last past years, several new alternative products to synthetic pyrethroids have been developed and are sold in the Argentinean market. These products contain essential oils as their active ingredients or silicon derivates. However, no efficacy in vitro tests were performed against permethrin-resistant head lice from Argentina. Thus, the aims of the present study were (1) to assess the efficacy of two new Argentinean products (Nopucid Qubit® and Nopucid Bio Citrus®) compared with two reference products (Nyda® and Hedrin®) and (2) to compare the sensitivity of two laboratory assays for testing insecticide activity of new formulations.

Materials and methods

Head lice

Head lice and eggs were collected from the head of 508 children 6–13 years old using a fine-toothed antilouse metal comb. The lice were collected from two elementary schools (Ricardo Guiraldes and Escuela Nº14) and were transported to our laboratory according to Picollo et al. (1998). The protocol for lice collection was approved by the ad hoc committee of the Centro de Investigaciones de Plagas e Insecticidas (Research Center of Pests and Insecticides), Buenos Aires, Argentina, and archived in our laboratory.

Products tested

Details of the over-the-counter (OTC) product tested are shown in Table 1. We assessed the efficacy of two available commercial products in Argentina, Nopucid Qubit® and Nopucid Bio Citrus®, which are based on plant and silicon derivatives. They were purchased in Buenos Aires, Argentina. We also tested the efficacy of two dimeticone-based products, Nyda® and Hedrin®, which were purchased in Sitges, Spain.
Table 1

Products tested for their pediculicidal activity against head lice

Trade name

Producer

Presentation

Active compound

Nopucid Qubit®

Laboratorio ELEA, Argentina

Two-phase lotion

Phase 1, geraniol (0.75%), citronellol (0.75%); phase 2, ciclopentaxiloxane (48.6%)

Nopucid Bio Citrus®

Laboratorio ELEA, Argentina

Lotion

Ciclopentaxiloxane (48.6%), dimethicone (48.6%), bergamot essential oil (2%)

Nyda®

G. Pohl-Boskamp GmbH & Co., Germany

Spray

Dimethicone (92%)

Hedrin®

Thornton & Ross Ltd., UK

Lotion

Dimethicone (4%), cyclomethicone 5

Motile stages testing

The adulticidal and third-stage nymph activity was assessed using two techniques: an in vitro immersion test (Mougabure Cueto et al. 2002) and ex vivo hair tuft test. Briefly, the in vitro test consisted of batches of at least ten adults and/or third-stage nymphs that were immersed for 0.5, 1, or 2 min in 1 ml of each tested product. Once the exposure period finished, the insects were placed onto a wire mesh and washed sequentially with 100 ml of water. Lice were then transferred onto a Whatman no. 1 filter paper (7.0 cm in diameter) moistened with 0.5 ml of water that was placed in the bottom of a plastic Petri dish (9.0 cm in diameter). The exposed lice were observed for evidence of any affected symptoms at 5, 10, 60, 120, 180, 240, and 1,080 min. Criterion of affected insects was if a louse remained on its back with no or only occasional low leg or antennal movements. During the recorded period of symptoms, Petri dish containing head lice were kept in enclosed plastic containers where water was added (to produce a high-humidity environment), located inside an environmental chamber (Ambi-Hi-Low Lab-line, Iowa, USA) set at 18 ± 2°C (Gallardo et al. 2009). Each experiment was replicated at least three times. Once used in a given assay, the insects were discarded and not used in another experiment.

The ex vivo hair tuft test was a modification of the assay previously described by Oliveira et al. (2007). Batches of 10–15 lice were placed on hair strands (6 cm in length). One milliliter of every product was dropped on the hair strand containing lice (experimental unit) and three exposure times were performed: 0.5, 1, or 2 min. After the exposure time, each experimental unit was washed with 100 ml of water. Then, they were placed in the bottom of a plastic Petri dish (9.0 cm in diameter), and evidence of affected symptoms was recorded at 5, 10, 60, 120, 180, 240, and 1,080 min. Any louse dislodged during treatment or washing was placed back onto the hair strand. Treated hair tuft with lice were examined under a dissecting microscope. Criterion of affected insects was if a louse remained on its back with no or only occasional low leg or antennal movements. Three replicates were made for each exposure time per product. After the recorded period of symptoms, treated lice were discarded. During each assay, the assembled experimental units were placed in an enclosed chamber with a high-humidity environment, kept in an environmental chamber.

Ovicidal effect

Groups of 10–20 late development viable eggs were selected as described previously by Mougabure-Cueto et al. (2006). Late eggs showed black eye spots and clearly visible appendages of the embryo. Tested eggs were fixed to a microscope slide by a double-face adhesive tape. Slides containing eggs were immersed in the tested pediculicides for 0.5, 1, or 2 min. After the exposure period, the slide containing the eggs was dried on a filter paper. Then, head louse eggs were incubated at 28 ± 1°C and 75 ± 5% RH (closed containers with saturated aqueous solutions of NaCl). Mortality data of treated eggs were recorded 5 days after the eclosion of controls. Treatments and controls were replicated three times. The criterion for mortality was eggs with closed operculum or eggs with opened operculum with the nymph inside (Mougabure-Cueto et al. 2006).

Inflammability test

To test the inflammability of the Nopucid Qubit® and Nopucid Bio Citrus®, we little modified the methodology followed by Abdel-Ghaffar et al. (2010). Briefly, human hairs of 10 cm long were assorted into plastic Petri dish (11.0 cm in diameter). Then, these hair portions were treated with 2 ml of tested products. Each strand of hair was treated once and then discarded. Control consisted of untreated hairs. In all treatments, the hair was made fully wet by the products and they were transferred on a white glazed tile (15 × 15 cm) placed into a digestorium. Then, the flame from a lighter touched the treated hair and the results were registered by a digital picture camera (Sony DSC-P200, Japan). Before another test, the tile was carefully cleaned.

Statistical analysis

Percentage affected response or mortality was determined and transformed to arcsine square-root values for analysis of variance. Treatment means were compared and separated by the Duncan test (StatSoft Inc. 2004). All statistical tests were performed with α = 0.05 for the significance of statistical tests.

Results

Total mortality occurred when the insects were exposed to any product for 1 and 2 min either by in vitro or ex vivo test. In the dipping technique, for an exposure time of 0.5 min, the Argentinean pediculicides Nopucid Qubit® and Nopucid Bio Citrus® killed 94% and 96% of head lice, respectively. However, they differed significantly from Nyda® and Hedrin® (F = 28.61; df = 4.8; P < 0.0001) (Table 2). Irrespectively of the exposure time (0.5, 1, or 2 min.), the hair tuft test showed a 100% of mortality on motile forms. As the treated lice were immobile almost immediately, it appears that it was due to the physical action of the silicones that coated the louse surface and enters through the respiratory tract, blocking either spiracles or tracheae (Richling and Böckeler 2008; Burgess 2009).
Table 2

Percentage of affected head lice treated with over-the-counter pediculicides following exposure of 0.5 min

Product

Evaluation technique

Affected lice (%) ± SE

Time (min)

5

10

60

120

180

240

1,080

Nopucid Qubit®

Immersion

100

100

100

95.8 ± 7.2

95.8 ± 7.2

95.8 ± 7.2

83.8 ± 5.3

Hair tuft

100

100

100

100

100

100

100

Nopucid Bio Citrus®

Immersion

94.5 ± 7.8

94.5 ± 7.8

94.5 ± 7.8

94.5 ± 7.8

94.5 ± 7.8

94.5 ± 7.8

94.5 ± 7.8

Hair tuft

100

100

100

100

100

100

100

Nyda®

Immersion

100

100

100

100

100

100

100

Hair tuft

100

100

100

100

100

100

100

Hedrin®

Immersion

100

100

100

100

100

100

100

Hair tuft

100

100

100

100

100

100

100

The ovicidal activity of commercial products is summarized in Fig. 1. Significant differences in ovicidal action were observed among the tested products after 0.5, 1, and 2 min (P < 0.0001). For any exposure time, the most effective pediculicides were Nopucid Bio Citrus® and Nyda®, followed by Hedrin® and Nopucid Qubit®. The highest differences were observed in eggs exposed for 0.5 and 1 min, which showed more than 90% efficacy for Nopucid Bio Citrus® and Nyda® and less than 50% for Nopucid Qubit® and Hedrin®. After 2 min, these products showed a significantly improved efficacy.
Fig. 1

Ovicidal effect of over-the-counter pediculicides at different exposition times. Means in same bar followed by different letters are significantly different by Duncan’s test (P < 0.05)

The inflammability test showed that both Nopucid Bio Citrus® and Nopucid Qubit® were inflammable and produced flames up to 3–6 cm high that persisted constantly inflamed and wandered along the entire hair. These features were similar to those showed by Nyda® and Hedrin®.

Discussion

The present study revealed, for the first time, the efficacy of OTC commercial pediculicides available in Argentine (Nopucid Bio Citrus® and Nopucid Qubit®) on either motile stages or eggs of head lice. Comparatively, the effectiveness of these products was similar to Nyda® and Hedrin®, two commercial pediculicides with well-documented lethality (Oliveira et al. 2007; Burgess et al. 2007, 2008; Heukelbach et al. 2008; Burgess 2009; Abdel-Ghaffar et al. 2010). In addition, Oliveira et al. (2007) reported high mortality of head lice treated with Nyda® and Hedrin® by a 3-min immersion test. Also, Burgess et al. (2005) reported a cure ratio of about 70% after treating head lice infestation with Hedrin® in randomized controlled equivalence trial. These results demonstrated the high efficacy of silicone-based products, which mode of action is physical rather than neurotoxic. A possible mode of action is the penetration through the respiratory tract blocking both spiracles and tracheae causing physiological stress that leads to death through rapid immobilization, water excretion inhibition, and gut disruption (Burgess 2009). It has been suggested that this mode of action should delay the development of resistance (Heukelbach 2010).

Our analysis of mortality in head lice using the hair tuft technique could not differentiate between the effectiveness of pediculicides because 100% mortality was obtained on all products and all exposure times. As an alternative, the direct immersion technique was able to detect a slightly lower mortality of head lice exposed for 0.5 min to Nopucid Qubit® and Nopucid Bio Citrus®. Therefore, it can be considered a more sensitive method to detect small differences in mortality.

Even though the Argentinean product Nopucid Bio Citrus® is a silicone-based product as Nyda® and Hedrin®, it had more ovicidal activity than Hedrin®. It could be explained due to the concentration of dimeticone and the presence of other components (i.e., essential oil of bergamot) that would affect the efficacy of the product.

The study of Abdel-Ghaffar et al. (2011) analyzed the effect of a neem seed aqueous extract against both motile lice and nits. The authors found high efficacy in a very short time, suggesting that a single application of this product would eliminate either motile lice or eggs of an infested head. This topic is of main importance in reinfestation events.

An “ideal pediculicide” should have the following characteristics: 100% efficacy in killing motile stages and eggs, easy to apply, toxicological safety, low cost, non-inflammable, high acceptability to users, good environmental profile, prevents reinfestation, has a single treatment application, requires <5 min to act, and possesses a delayed resistance developing (Heukelbach 2010; Abdel-Ghaffar et al. 2010). Although all these characteristics are difficult to find in any of the OTC products worldwide [an exception might be the neem seed extract tested by Abdel-Ghaffar et al. (2011)], both Nopucid Bio Citrus® and Nopucid Qubit® cover some of the mentioned topics. The subjects filled by these products are as follows: almost 100% effective in killing motile lice and around 50% to 90% of ovicidal effect, easy to apply, low cost, high acceptability by consumers, and less than 2 min to produce toxic effect against head lice. On the other hand, the topics not covered by the mentioned products are related to some of the toxicological safety of the silicones and their inflammability. As mentioned by Nair (2003), cyclomethicone and dimethicones are non-irritant, non-genotoxic, non-carcinogenic, had no adverse effect in pregnant or fetuses, and were considered by the cosmetic ingredient review expert panel as unlikely to be absorbed into the skin. However, adverse effects were observed in one inhalation study of a cream formulation with 1% dimethicone. Moreover, Abdel-Ghaffar et al. (2010) mentioned the possibility that some components of dimethicone products could by inhaled, covering the lung epithelia. The monoterpenoids found in Nopucid Bio Citrus® and Nopucid Qubit® (i.e., geraniol, citronellol, and bergamot essential oil) have been placed under Generally Recognized as Safe category by the Food and Drug Administration of the USA and classified as safer and nontoxic compounds (at lower doses such as those use in the studied products) (USEPA 1993). Concerning inflammability, both pediculicides were highly inflammable and a warning note should be included in the manufacturer instructions. The starting of a flame is not only related to direct contact with an open fire, but a simple malfunction of a hairdryer could produce a spark that would catch fire. Future works on the Argentinean pediculicides should focus on the development of an in vivo test to study the efficacy of a single treatment against head lice.

Notes

Acknowledgments

The authors wish to thank all the authorities of the elementary schools where head lice material was collected. This investigation received financial support from Consejo Nacional de Investigaciones Científicas y Técnicas (Argentina). The authors declare no competing financial interests with any of the evaluated products. The experiments in this work comply with the current laws of Argentina.

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Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Anabella Gallardo
    • 1
  • Gastón Mougabure-Cueto
    • 1
  • Claudia Vassena
    • 1
  • María Inés Picollo
    • 1
  • Ariel Ceferino Toloza
    • 1
  1. 1.Centro de Investigaciones de Plagas e Insecticidas (CONICET-CITEDEF)Juan Bautista de La Salle 4397Villa MartelliArgentina

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