Marys Medicine


Expert Review of the Evidence Base for Arthropod Bite Avoidance
Larry I. Goodyer, PhD,∗ Ashley M. Croft, MD,† Steve P. Frances, PhD,‡ Nigel Hill, PhD,§
Sarah J. Moore, PhD,§ Sangoro P. Onyango, BSc,§ and Mustapha Debboun, PhD¶
∗Leicester School of Pharmacy, De Montfort University, Gateway, Leicester, UK; †Surgeon General's Department, London,
UK; ‡Australian Army Malaria Institute, Brisbane, Qld., Australia; §London School of Hygiene and Tropical Medicine, London,
UK; Ifakara Health Institute, Ifakara, Morogoro, Tanzania; ¶US Army Medical Department Center & School, Center for
Health Education & Training, Fort Sam, Houston, TX, USA
Bite avoidance measures are commonly recom- at; click on ‘‘ISTM Committees'' and mended to international travelers to help reduce the risk of various arthropod-borne diseases. A keystrategy is the use of repellents applied topically to skin Part 1: Repellents for Topical Use
or clothing which are considered in the first part ofthis review. Also advised are a variety of methods that Major Findings employ the use of insecticides and physical barriers such N ,N -diethyl-3-methylbenzamide (deet), (2-(2-hydroxy- as mosquito nets or oil preparations applied to the skin.
ethyl)-piperidinecarboxylic acid 1-methyl ester (icari- In the following document, the authors considered din), p-methane 3, 8-diol (PMD), and ethyl butylacety- some of the most widely used bite avoidance methods laminopropionate (IR3535)-based repellents all provide and identified the strength and quality of evidence that protection against biting arthropods, but volatile oils determined efficacy. The overall purpose of the review and other natural products are less reliable. On the is to provide the available evidence, in a graded format, strength of available evidence, the first-line choice for upon which to base recommendations for the selection those visiting areas where malaria or other arthropod- of appropriate repellents and other methods of bite borne diseases are endemic remains formulations with avoidance in those traveling overseas.
higher concentrations (20–50%) of deet. Higher con-centration icaridin and PMD preparations are the mostuseful alternatives to deet where they are available. See Desired Outcomes and Methods
Table 1 for a summary of the findings.
The authors were asked to consider the effectivenessof the most commonly used active ingredients Diethyltoluamide (Other Name Deet; Chemical (AIs) in repellent formulations and methods of bite Name: N ,N -Diethyl-3-Methylbenzamide, Former avoidance. The evidence base considered protection Nomenclature N ,N -Diethyl-m-Toluamide) against nuisance biting insects, reduction in the Deet has been widely used in insect repellent products incidence of arthropod-borne diseases, and safety for use on human skin to protect against biting profile. Effectiveness of the repellent related to spectrum arthropods.1–5 The majority of laboratory and field of activity against various mosquito species and other tests conducted to compare the efficacy of repellents arthropods was examined as well as longevity of applied use deet as the primary formulation or as a comparison.
dose. Where possible, efficacy was compared to deet Deet is considered the most effective broad spectrum as being the accepted gold standard. All sections repellent AI against biting arthropods.6 employed MEDLINE via PubMed in literature searches The first laboratory tests against mosquitoes were augmented by others depending on the subject area reported by Gilbert and colleagues7 who showed investigated. Details of the review process can be found deet and dimethylphthalate were equally effectiveagainst Anopheles quadrimaculatus. Altman8 reportedfield studies in Panama against Anopheles albimanus Corresponding Author: Larry I. Goodyer, PhD, Leicester
and showed 75% deet provided protection for at least School of Pharmacy, DeMontfort University, The Hawthorn 3 hours. Field studies undertaken in the last 20 years Gateway, Leicester in Africa,9,10 Australia,11,12 Papua New Guinea,13,14 Malaysia,15 and Thailand16 have shown that protection 2010 International Society of Travel Medicine, 1195-1982Journal of Travel Medicine 2010; Volume 17 (Issue 3): 182–192 Expert Review of Bite Avoidance Summary of evidence base for topically applied repellents Aspect of bite avoidance DeetDermal application to avoid mosquitoes Deet provides shorter protection against Anopheles sp.
mosquitoes than Culicine mosquitoes. Reapplicationtimes will vary to maintain optimal effectiveness.
Dermal application to avoid ticks Laboratory and field tests showed deet provides minimal protection, recent test showed adequate protection.
Application of deet to wristbands Wristbands provide no protection for uncovered and untreated human skin.
IcaridinDermal application to avoid mosquitoes Icaridin provided good protection against Anopheles sp.
mosquitoes in Africa and Asia, also effective againstCulicine mosquitoes.
Dermal application of icaridin to humans to avoid ticks Laboratory test showed icaridin provides protection for 1 h. Recent test showed adequate protection.
IR3535Dermal application to avoid mosquitoes Based on limited field studies for mosquitoes. Not recommended in malaria endemic areas.
Dermal application to avoid sand flies Based on one laboratory study.
PMDDermal application to avoid mosquitoes Can be highly recommended as an alternative repellent to deet at concentrations of >20% as a repellent foruse in disease endemic areas. (Some evidence ofefficacy against ticks.) Not recommended for use when engaging in vigorous activities, in disease endemic areas or areas with highdensities of mosquitoes.
More studies should be conducted before it is recommended as a repellent.
Essential oils require careful formulation to be effective, and safety data suggest skin irritation is a factor.
∗A = good evidence to support use; B = moderate evidence to support use; C = poor evidence to support use; D = moderate evidence to support a recommendationagainst use; E = good evidence to support a recommendation against use.
† I = evidence from one or more properly randomized, controlled trial; II = evidence from one or more well-designed clinical trial without randomization, fromcase-controlled analysis of cohort study; III = consensus evidence, evidence from one authority or reports of expert committees, single case studies.
against Anopheles spp. is less than that provided against may cause damage, and thus the use of deet applied to clothing is not widely accepted. The use of wristbands The response of different mosquito species to deet treated with deet and other AIs offered no protection is variable.17 Field tests of repellent formulations against mosquitoes.4 containing deet against biting Culex spp., Aedes spp., There have been a number of reviews concerning the Mansonia spp., and Verrallina spp. have been reported.5 safety of deet,25,26 and they have attested to its generally The protection provided by deet was longer against acceptable safety profile. There are few reports of these genera than provided against Anopheles spp.12 systemic toxicity in adults following dermal application.
Studies have shown that deet provides only minimal The safety profile in the second and third trimester of or poor protection against ticks.18–21 However, recently pregnancy has been established through observation of Carroll and colleagues22 showed that a 33% deet, very low placental cord concentrations after maternal Extended Duration formulation provided high levels application of deet,27 and animal models do not of protection for 12 hours.
indicate any teratogenic effects.28 Recommendations Deet is recommended to be applied to the exposed for use in young children do vary between countries, skin of humans. However, alternative methods of with some recommending lower concentrations29 and using deet have been proposed and investigated. The others suggesting that higher strengths can be used.30 application of deet to wide mesh cotton/nylon jackets However, the causation between the few reported cases provided good protection against mosquitoes and biting of encephalopathy in children and the topical use of flies.23 Deet-treated netting used as groundsheets were deet cannot be supported by a good evidence base.31 shown to provide significant protection against ticks.24 The scientific evidence and continued use of deet for Although application of deet to nylon/cotton fabrics >50 years has shown this AI is the best broad spectrum has been shown to enhance protection against bites, the repellent available for minimizing bites of mosquitoes, application of deet to some synthetic fibers and plastics ticks, and other biting arthropods.
J Travel Med 2010; 17: 182–192 Goodyer et al. Icaridin (Formerly Picaridin; commercially available preparations. Importantly, PMD has been proven to prevent malaria in a clinical trial in 1-Methyl Ester; WHO Designation: Icaridin; Trade the Bolivian Amazon.44 Name: Bayrepel; Development Reference Code: KBR Studies carried out both in the laboratory and the field using rigorous methodology have shown PMD Independent field studies demonstrating the effective- to be a repellent of equal efficacy and longevity as ness of repellents containing icaridin against mosquitoes deet.45 At 30% AI, PMD provided almost complete have been conducted in Malaysia32,33 and Florida.34 protection for 4 hours in South America46 and complete In Australia, a formulation containing 19.2% icaridin protection for 6 hours at 50% AI in Sub-Saharan Africa provided similar protection as 20% deet against Ver- against malaria vectors.47 In both of these studies, the rallina lineata.35 In another study in Australia, the protection time was equivalent to the deet controls. A same formulation provided >95% protection against well-designed laboratory trial of PMD against a further Culex annulirostris for 5 hours, but only 1 hour pro- African malaria vector showed complete protection tection against Anopheles spp.12 KBR 3023 at concen- for 4 to 5 hours using PMD impregnated towlettes,48 trations of 2% to 13% v/v in 90% ethanol provided again comparable with deet. Laboratory trials using better protection against Anophelines in Africa than the main vectors of dengue fever have shown good comparable formulations containing deet.10 protection, which is important for travelers as the Field studies against mosquitoes in two locations in vector bites in the day-time.45,49 Against the tick vectorsof Lyme disease and Rocky Mountain spotted fever, Australia showed that a 9.3% formulation only provided PMD reduces attachment and feeding success by around 2-hour protection against V lineata35 and 5-hour 77%, and PMD is highly effective against the Highland protection against C annulirostris,36 while 7% icaridin Midge.50 PMD has not been tested against the vectors of provided 5.7 hours of protection against Aedes albopictus leishhmaniasis in vivo, although in vitro results suggest in laboratory tests.37 The use of lower concentrations that it may be effective.51 of icaridin in commercial formulations may requirethe user to reapply repellent more often to maintain effectiveness than with the higher concentrations( Citronella is one of the essential oils obtained from >20%) of icaridin used in the field.
Protection from biting by ticks provided by 20% the leaves and stems of different species of Cymbopogon lotions of KBR 3023 was reported to be short.38 Carroll grasses. From the available literature and information, and colleagues22 showed that Bayrepel (10 and 20% we can conclude that the complete protection time forcitronella-based repellents is icaridin) repellent provided high levels of protection <2 hours4,49,52 because the repellent is highly volatile, but this can be prolonged for 12 hours when applied to human volunteers against by careful formulation and the addition of fixatives like Amblyomma americanum under simulated field-contact IR3535 [Also known as 3535 or EBAAP (EthylButylacetylaminopropionate)] Neem is a vegetable oil pressed from the fruits and seedsof neem (Azadirachta indica). Several field studies from Five field studies were identified, all testing IR3535 India have shown very high efficacy of neem-based against mosquitoes.10,34,39–41 These indicated that preparations.54–56 However, these studies have used IR3535 is as effective as deet in repelling mosquitoes of questionable methodologies and their results contrast the Aedes and Culex genera but may be less effective than strongly with several others that have shown medium- deet in repelling anopheline mosquitoes. A number of range protection from neem products being inferior laboratory studies were also identified, testing IR3535 to deet.46,49,57 Neem has a low dermal toxicity but against a variety of other arthropods, including blackflies can cause skin irritation such as dermatitis.58 However, and ticks.42 An uncontrolled field study of a new, caution should be taken as neem is a proven reproductive controlled-release formulation of IR3535 reported that toxicant and long-term subchronic exposure could these formulations may provide complete protection impair fertility.59 against mosquito biting for 7.1 to 10.3 hours.41 IR3535may be more effective than deet in protecting against Essential Oils phlebotomine sandfly biting (10.4 h mean protection vs Many commercial repellents contain a number of plant 8.8 h, respectively).42 essential oils either for fragrance or as repellents. Themost effective of these include thyme oil, geraniol, PMD: Lemon Eucalyptus (Corymbia citriodora) Extract peppermint oil, cedar oil, patchouli, and clove.52,60,61 The principal repellent component of lemon eucalyptus Most of these essential oils are highly volatile and extract is PMD, which is the main by-product of lemon this contributes to their poor longevity as mosquito eucalyptus hydrodistillation.43 The active component is repellents. They can be irritating to the skin49,62 prepared through acid modified extraction of leaves or and their repellent effect is variable, dependent on a synthetic version of PMD is used in the majority of formulation and concentration.
J Travel Med 2010; 17: 182–192 Expert Review of Bite Avoidance important tool or method of personal protection The largest body of evidence for effectiveness in terms against arthropod bites and disease-transmitting vec- of spectrum of activity and longevity relates to deet that tors. Some of the insecticides that are recommended remains as a gold standard to which newer repellents are and used for treatment of fabrics are permethrin, compared in reducing nuisance bites from arthropods.
Icaridin and PMD are reasonable alternatives to deet for cyfluthrin, and etofenprox.66 However, the insecticide those visiting areas where arthropod-borne diseases are most commonly used for fabric impregnation is perme- endemic, whereas IR3535 has shown reduced efficacy thrin [3-(phenoxyphenyl) methyl (±)-cis, trans-3-(2,2- against Anopheles mosquitoes and should not be advised for malaria endemic areas. When advising a formulation, the concentration of AI and the expected application Permethrin is a synthetic pyrethroid insecticide rate of AI should always be considered because these derived from crushed dried flowers of the plant will greatly influence longevity of the applied dose.
Chrysanthemum cinerarifolium. Although permethrin's There are, for instance, some icaridin formulations primary mode of action is contact toxicity against a wide containing suboptimal concentrations. Apart from the variety of biting arthropods, it is also unique in that repellent choice, the following factors will determine it serves both as a contact insecticide and as an insect the duration of any repellent product.
repellent. Permethrin-impregnated clothing providesgood protection against mosquitoes,67–77 ticks,78–84 1. Product concentration: In general, the higher chigger mites,85,86 fleas,87 lice,88,89 sand flies,90,91 kissing percentage of AI, the greater the protection time bugs,92,93 and tsetse flies.94 Thus, the use of permethrin- will be, although this tends to plateau at 50% w/v in treated clothing will decrease the biting frequency and the case of deet.63 transmission of arthropod-borne diseases among civilian 2. The rate of application that is applied to the exposed travelers and deployed military personnel. Today, human skin is also variable.64 And travelers have been military personnel from many countries use permethrin shown to apply relatively low doses of AI on treated to repel and kill arthropods that land on many kinds of treated surfaces, including field uniforms, tents, bed 3. Activity level of the user: The effectiveness of a nets, and helmet covers.95 repellent is reduced by evaporation and absorption Impregnated-treated fabrics such as bed nets, from the skin surface and wash-off by sweat.
curtains, chaddars (veils or wraps worn by Muslim 4. Environmental conditions: Rain or water, washing women), top sheets, and blankets have also been found the repellent off the body, wind, and high ambient to be effective in reducing the burden of malaria temperatures will reduce a product's effectiveness.
and other vector-borne diseases96–100 and have been 5. User's overall attractiveness to blood-feeding used in the Roll Back Malaria Program by the World arthropods, such as mosquitoes.
Health Organization for tropical countries. However, 6. Number and species of blood-feeding arthropods due to the development of pyrethroid resistance in (biting density).
mosquito vectors, the use of impregnating fabrics withinsecticide mixtures, a combination of a repellent and Part 2: Area and Barrier Methods
insecticide-treated bed nets or mixtures of repellentsand non-pyrethroid–treated fabrics have become new Major Findings promising tools for disease vector control.101,102 The strongest level of evidence exists for the use of The development and use of long-lasting insecticide insecticide-treated mosquito nets, and these are to be nets such as Olyset Net and Perma Net has also been advised for all travelers visiting disease endemic areas proven to be effective in reducing or eliminating the at risk from biting arthropods on retiring. Insecticide- need for insecticide retreatment of insecticide-treated treated clothing and other fabrics would also be a useful nets.103–107 In addition, recently, the use of tent barrier adjunct to dermal applied repellents. Electric insecticide treatments with bifenthrin and permethrin is another vaporizers, essential oil candle, and coils to burn do effective method of personal protection against biting reduce bites from arthropods, but there is little evidence on the efficacy of knockdown insecticide sprays. Thereis some concern regarding the potential adverse effects Electric Insecticide Vaporizers of burning coils. There is less evidence that these An insecticide vaporizer, which are mains- or battery- technologies reduce the incidence of malaria. There operated electrical devices releasing a pyrethroid is only weak evidence regarding the efficacy of oils used insecticide, will clear a room of insects in around 30 on the skin. See Table 2 for a summary of the findings.
minutes and will remain effective for over 6 hours.112 Ten field and laboratory studies were identified, Fabric Impregnation With Insecticides testing a variety of insecticides and devices in different The use of fabric impregnated with insecticides, par- settings, against a range of flying insects, including ticularly insecticide-treated bed nets, has become an various mosquito species.113–122 J Travel Med 2010; 17: 182–192 Goodyer et al. Summary of evidence base for area and barrier methods InsecticidesEffectiveness of insecticides on clothing Strong evidence from numerous authorities or reports of expert committees supporting the use of impregnatedinsecticides (permethrin) on clothing as an importantmethod of personal protection against arthropod bites.
Effectiveness of net impregnation Numerous studies have shown good personal protection against arthropod bites with the use of netsimpregnated with insecticides.
Effectiveness of use on tents Consistent evidence from studies showing good personal protection against arthropod bites with the use ofimpregnated tents with insecticides.
Vaporizing insecticide matsInhibition of nuisance biting by mosquitoes Consistent evidence that insecticide vaporizers cause mosquito bite inhibition, mosquito repellence,mosquito knockdown, and mosquito death.
Malaria prevention No evidence from three studies Mosquito coilsInhibition of nuisance biting by mosquitoes Good evidence of protection against mosquito bites Malaria prevention Consensus that mosquito coils could be a useful measure to prevent malaria Prior exposure to mosquito coil smoke was more common in lung cancer patients than in controls.
Lung cancer risk was higher in frequent burners ofmosquito coils than in non-burners.125 Other adverse effects Breathlessness,132 chest irritation,114 eye and nose Essential oil candlesInhibition of nuisance biting by mosquitoes Two studies demonstrating significant repellency compared to control.73,134 Inhibition of nuisance biting by other insect Essential oil, linalool, and geraniol but not citronella candles repelled significantly more sandflies than didthe control candle.135 Mosquitoes knockdown spraysInhibition of nuisance biting by mosquitoes Anecdotal evidence only.
and other insect species Malaria prevention Two studies showed no significant reduction in malaria Prevention of other insect-transmitted Oil-based productsInhibition of nuisance biting by midges Evidence for bath oils only.
Inhibition of nuisance biting by mosquitoes Evidence for chemical base oils only. Inhibition was observed mostly in culicine mosquitoes.148 Soybean oil inhibition of nuisance biting by More studies (field trials) needed to establish the efficacy mosquitoes and black fly of soybean oil as a repellent, although initial studiesare very promising. Toxicity very low.
Garlic and vitamin B Do not confer protection against haematophagous arthropods and this notion should be discouraged.
∗A = good evidence to support use; B = moderate evidence to support use; C = poor evidence to support use; D = moderate evidence to support a recommendationagainst use; E = good evidence to support a recommendation against use.
† I = evidence from one or more properly randomized, controlled trial; II = evidence from one or more well-designed clinical trial without randomization, fromcase-controlled analysis of cohort study; III = consensus evidence, evidence from one authority or reports of expert committees, single case studies.
Electric insecticide vaporizers using pyrethrins or vaporizers containing these classes of insecticide pyrethroids inhibit nuisance biting by mosquitoes, and should be used by travelers with caution. Vaporized vaporized pyrethrins kill house flies. There is no direct neem oil is an effective inhibitor of mosquito evidence that the technology does prevent malaria landing and appears safe to humans.121 It should or any other insect-transmitted infection.119,120,122 be investigated further for its potential usefulness in Exposure to pyrethrins and/or pyrethroids may present preventing malaria and other mosquito-transmitted a low-level health hazard to humans,123 and so J Travel Med 2010; 17: 182–192 Expert Review of Bite Avoidance Mosquito Coils insecticide sprays should be discouraged, in favor of Mosquito coils are made from a paste of powdered vector avoidance strategies of proven effectiveness.138 insecticide, usually a pyrethrin or pyrethroid whichwhen lit will smolder at a steady rate. Burning one Bath Oils and Chemical Base Oils mosquito coil releases the same amount of particulate Bath oils, and chemical base oils also, seem to protect matter as does burning 75–137 cigarettes124 and emits against insect biting not by a repellant action but by formaldehyde equivalent to 51 cigarettes.125 forming a physical barrier between the human target Historically, some authorities have advised interna- and the insect.139 They are reported to be especially tional travelers to burn mosquito coils in their room at effective against small flying insects, creating an oily night, in order to discourage mosquito biting and so layer which traps these insects on the sticky surface help prevent mosquito-transmitted infection, notably of the skin.140 Some studies have suggested that small malaria. These authorities include some national expert flying insects, such as biting midges and sandflies, are not efficiently repelled by conventional repellants (deet Consistent evidence from a systematic review and pyrethroid insecticides).141,142 indicated that coils cause mosquito bite inhibition, One small randomized controlled trial (nine adult mosquito repellence, mosquito deterrence, mosquito volunteers) tested a commercial bath oil preparation knockdown, and mosquito death. Inhibition of nuisance (Avon Skin-so-Soft, SSS)140 and found that deet biting is seen in all mosquito species: Aedes, formulations were significantly more effective in Anopheles, Culex, and Mansonia.131 There has been preventing midge biting than was SSS.
little evidence that this technology prevents malariatransmission120,131,132 or other mosquito-transmittedinfection. However, the expert group considers that they Soybean Oil would be effective in preventing malaria in the light of Two well-designed laboratory evaluations of Bite as yet unpublished data.133 Exposure to mosquito coil Blocker, a commercial preparation containing 2% smoke could be hazardous to humans due to its potential soybean oil in addition to other oils and emulsifiers, association with lung cancer, but this should be taken have shown that it is competitive with deet, against a in context of the amount likely to be inhaled over an dengue vector and nuisance biting mosquitoes in one evening and the very occasional use by travelers. In study49 and equivalent to that of low-concentration many countries, such coils are licensed for outdoor use deet in a second study.4 A field trial showed 3.5-hour only due to these concerns.
protection under intensive biting pressure of nuisancemosquitoes, but this was not conducted by independent Essential Oil Candles researchers.143 In a similar study against black flies, Three field studies were identified, demonstrating soybean oil provided complete protection from black fly the effectiveness of essential oil candles in repelling bites of 9.7 hours as compared to 6.6-hour protection mosquitoes and sand flies.134–136 provided by deet.144 Burning essential oil candles is likely to prevent biting by both mosquitoes and by sandflies. They may Garlic and Vitamin B also prevent biting by other insect species. While there It is still commonly believed and reported in magazines is no evidence that this technology prevents malaria, that ingestion of garlic or B vitamins makes the human leishmaniasis, or any other insect-transmitted disease, skin unpalatable to blood feeding and biting arthropods this is an aspect which should be investigated. Candles which have been refuted.145,146 Garlic and B vitamins containing 5% essential oil of geraniol appear to hold must never be suggested as a natural method of bite the most promise.
Knockdown Insecticide SpraysKnockdown insecticides are aerosol sprays which are designed to be sprayed indoors and into the air, toeliminate flying insects by killing them as they fly The use of insecticide-treated mosquito nets and through the room.128 clothing is well supported by the data and is to be Two individual studies were identified which failed recommended to travelers visiting malaria endemic to demonstrate that knockdown insecticide sprays areas. Electric insecticide vaporizers and essential oil prevented malaria in travelers to Africa.119,132 Only candles inhibit nuisance biting, but there is little anecdotal evidence supports the assumption that evidence that they help prevent malaria. Mosquito knockdown sprays inhibit nuisance biting by flying coils are effective and may help to reduce the risk of insects. There is an obvious, but mostly unquantified malaria, although safety concerns have been raised. The health risk to humans, from inhaling any insecticide use of bath oils and other oils should be discouraged vapor.137 In the absence of persuasive evidence on in travelers until further effective personal protection the benefits of this technology, the use of knockdown evidence is available.127 J Travel Med 2010; 17: 182–192 Goodyer et al. against Anopheles (Diptera: Culicidae) in Lae, Papua NewGuinea. J Am Mosq Control Assoc 1999; 14:339–341.
The authors dedicate this review to the memory of 14. Frances SP, Cooper RD, Popat S, Beebe NW. Field Dr Nigel Hill who died suddenly in January 2010.
evaluation of the repellents containing deet and AI3-37220, against Anopheles koliensis in Papua New Guinea.
J Am Mosq Control Assoc 2001;17:42–44.
Declaration of Interests
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Impaired muscle metaboreflex-induced increases inventricular function in heart failure Donal S. O'Leary, Javier A. Sala-Mercado, Robert A. Augustyniak, Robert L.Hammond, Noreen F. Rossi and Eric J. AnsorgeAm J Physiol Heart Circ Physiol 287:H2612-H2618, 2004. First published 15 July 2004;doi:10.1152/ajpheart.00604.2004

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