New Discoveries in Agrochemicals - American Chemical Society

four locations in Texas (TCC-HL, TMF-HL, TMS-HL and TSA-HL). A permethrin- ... jeopardy (14) (LT5 0 values, Tables 1 and 2). ... 0.5%malathion + 0.1%D...
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Chapter 34

Control and Resistance Management of Human Pediculosis

Downloaded by PENNSYLVANIA STATE UNIV on September 7, 2012 | http://pubs.acs.org Publication Date: November 23, 2004 | doi: 10.1021/bk-2005-0892.ch034

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Si Hyeock Lee , Kyong Sup Yoon , Jian-Rong Gao , Young-Joon Ahn , and J. Marshall Clark 1

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School of Agricultural Biotechnology, Seoul National University, Seoul 151-742, Republic of Korea Department of Veterinary and Animal Science, University of Massachusetts, Amherst, M A 01003 2

Head louse resistance to commonly used pediculicides is wide spread worldwide. Resistance to permethrin and pyrethrum is 40- to 70-fold based on tolerance to knockdown response in US populations of head louse. Resistance to malathion is likewise widespread but at lower levels (2.0- to 3.3-fold). Currently, there appears to be little or no resistance to abamectin or lindane. Permethrin-resistant head lice are significantly more tolerant to knockdown and are cross-resistant to DDT, indicating a kdr-type of resistance mechanism. Sequence analysis of the full-length cDNA fragments of voltage-sensitive sodium channel α-subunit gene from permethrin-resistant head louse populations has identified three mutations (M815I, T917I, and L920F). All these mutations appear to exist en bloc as a haplotype and have functional significances in resistance. We have developed DNA-diagnostic protocols, including serial invasive signal amplification reaction (SISAR), for the detection of the conserved point mutations resulting in knockdown resistance to the pyrethrins, the pyrethroids, and DDT. A sound resistance management strategy based on efficient DNA-based genotyping techniques will greatly expand the lifespan of the valuable and effective pediculicides, such as permethrin, and ensure safe control of pediculosis.

© 2005 American Chemical Society In New Discoveries in Agrochemicals; Clark, J., et al.; ACS Symposium Series; American Chemical Society: Washington, DC, 2004.

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Introduction Pediculosis caused by Pediculus capitis, the human head louse, is the most prevalent parasitic infestation of humans worldwide, especially among school children of 3-12 years old (7). More than 6-12 million people in the United States (US) are estimated to have pediculosis. Symptoms of infestations are relatively mild, but the social, mental and economic consequences are substantial. Pediculosis is not widely tolerated in the US and is repeatedly treated by a variety of over-the-counter pediculicides, which are exclusively limited to those containing pyrethrin or permethrin as active ingredients. Because these pediculicides share a common mechanism of action on the voltage-sensitive sodium channel in the nervous system of insects (2), their repetitive and continued use has imposed a high pressure for the selection of resistant louse populations. To date, head louse resistance to permethrin has been reported from France (5), Czech Republic (4), Israel (J), Britain (d), Argentina (7,5), and the US (912). Head louse populationsfromthe US that were resistant to the lethal effect of permethrin also exhibited knockdown resistance (kdr) to the same material in behavioral knockdown bioassay (10). Through molecular cloning and sequencing analysis, the T929I and L932F mutations (T917I and L920F in louse sequence numbering, respectively) in a voltage-sensitive sodium channel asubunit gene was identified to be associated with permethrin resistance via nerve insensitivity mechanism. One of the mutations, T929I, has already been functionally validated to be responsible for knockdown-type resistance in the diamondback moth, Plutella xylostella (13), indicating strongly that the same mutation in the human head louse plays a critical role in knockdown resistance to permethrin. Nevertheless, it is not known how widely permethrin-resistant head lice are distributed in the field nor is known the relative frequency of the kdr alleles within permethrin-resistant populations. Resistance to permethrin in the US head louse populations is of great concern because there currently are no effective alternative treatments available as replacements, which have the same low level of mammalian toxicity as do the pyrethroids. Therefore, there is an urgent need for developing monitoring and resistance management strategies and discovery of new alternative pediculicides. In this article, the level of susceptibility to various insecticides in different human head louse populations in the US was investigated to assess the distribution of resistance. We also reported on the molecular mechanisms of head louse resistance to pyrethroid mediated by sodium channel mutations. Also discussed were the genotyping techniques for resistance monitoring and the

In New Discoveries in Agrochemicals; Clark, J., et al.; ACS Symposium Series; American Chemical Society: Washington, DC, 2004.

385 attempts for the discovery of new alternative pediculicides from plants, which will be critical elements in constructing a sound pediculosis management system.

Downloaded by PENNSYLVANIA STATE UNIV on September 7, 2012 | http://pubs.acs.org Publication Date: November 23, 2004 | doi: 10.1021/bk-2005-0892.ch034

Extent and Mechanisms of Resistance to Pediculicides Insecticide-susceptible strains of body louse from Israel (IS-BL) and head lice from Panama (PA-HL) and Ecuador (EC-HL) have been previously described (10,14). Another permethrin-susceptible strain of head louse was collected from Seoul, Korea (KR-HL). Permethrin-resistant strains of head louse were obtained from Western Massachusetts (MA-HL), Plantation, Florida (FLHL), Homestead, FL (SF-HL), San Bernardino County, California (SC-HL) and four locations in Texas (TCC-HL, TMF-HL, TMS-HL and TSA-HL). A permethrin- and malathion-resistant strain (BR-HL) of head louse was provided by G. Coles (University of Bristol). Resistance levels to permethrin in the FL-HL and MA-HL strains were 41and 69-times higher, respectively, when compared by knockdown ratios and 3.8and 4.3-times higher, respectively, when compared using mortality ratios, than those of the susceptible PA-HL strain (10). The higher resistance ratios determined by knockdown suggest that nerve insensitivity, most likely mediated by mutations in the sodium channel gene (kdr), is a principal resistance mechanism. Lack of synergism by piperonyl butoxide (PBO) and crossresistance to DDT in the FL-HL strain substantiate this suggestion. The MA-HL (10) and SC-HL (14) strains, however, were PBO-synergized, possibly indicating the involvement of oxidative resistance. Recently, permethrin resistance was determined in southern California (SC-HL) (14) and south central Texas (TCC-HL, TMF-HL, TMS-HL, TSA-HL)(/J) (Table 1), suggesting that resistance is widespread but not yet uniform. Cross-resistance to pyrethrum and PBO-synergized pyrethrum in the SF-HL and SC-HL strains was also apparent, indicating that the effective longevity of pediculicidal shampoos is now in jeopardy (14) (LT values, Tables 1 and 2). Malathion resistance was not detected in the MA-HL and FL-HL populations (10) but levels from 2.0- to 3.3-fold were determined in the SF-HL and SC-HL populations (14) (Table 1). Malathion resistance in the SF-HL strain was completely synergized by DEF, indicating a role of malathion carboxylesterase, but had no effect on the SC-HL population (14) (Table 2 and 1). The SC-HL population, however, responded as a susceptible population when treated with malaoxon (14) (Table 1) and PBO actually protected this strain from malathion (data not shown), indicative of a reduced desulfuration activity (decreased formation of malaoxon) as a resistance mechanism. Similar findings using the 50

In New Discoveries in Agrochemicals; Clark, J., et al.; ACS Symposium Series; American Chemical Society: Washington, DC, 2004.

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malathion-resistant BR-HL population from the UK (14) validate the importance of reduced desulfiiration. The lack of substantial cross-resistance to malathion in the permethrin-resistant US populations suggests that malathion may be an effective alternative treatment. However, presence of dual permethrin- and malathion-resistant populations in the U K (16) and our biochemical data (2.3 to 3.4-fold increase in esteratic activity in the dual resistant BR-HL strain, data not shown) indicate that its effectiveness will be short-lived unless augmented with alternative pediculicides and resistance management. a

Table 1. Resistance Ratio (RR ) of Head Lice from F L , C A , and T X

Treatment l%Permethrin 0.33%Pyrethrum 0.5%Malathion 0.5%Malaoxon 10%Abamectin l%Lindane a

SF-HL 8.5 2.8 2 0.6 1.7 0.8

SC-HL 5.3 2.6 3.3 0.8 1.8 0.8

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Head Louse Strain TCC-HL TSA-HL 4.6 4.5

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-

-

-

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TMF-HL 5.5 -

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RR=LT of resistant population/LT of susceptible population (EC-HL) 50

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Table 2. Synerglistic Effect of PBO and DEF on Pyrethrum-and Malathion-resistant Head Lice (SF-HL and SC-HL) Louse Population and Treatment

0.33%pvrethrum + 4%PBO SF-HL SC-HL*

Ν

LT;o(95%CL)

Slope ± SE

30 30

1505 (1464-1548) 1296(1257-1338)

3.0 ±2.2 6.6 ±1.4

1 1.1

23 27

91(59-126) 399(377-418)

4.2 ±0.6 17.0 ±2.3

2.6 1

0.5%malathion + 0.1%DEF SF-HL" SC-HL a

Logit regression is significantly differentfromunsynergized populations

Low levels of resistance to abamectin (1.7- to 1.8-fold) and lindane (0.8fold) were observed in the tested US head lice (14) (Table 1). Because dexamethasone pretreatment protects lice from abamectin toxicity (data not shown), a 3"-