Medical and Veterinary Entomology (2013) 27, 1–9 doi: 10.1111/j.1365-2915.2012.01020.

REVIEW ARTICLE

Insect repellents and associated personal protection

for a reduction in human disease
1 2
M. D E B B O U N and D. S T R I C K M A N
1 Department of Preventive Health Services, Academy of Health Sciences, U.S. Army Medical Department Center and School,
Fort Sam Houston, TX, U.S.A. and 2 Office of National Programs, U.S. Department of Agriculture, Agricultural Research Service,
Beltsville, MD, U.S.A.

Abstract. Personal protection measures against biting arthropods include topical

insect repellents, area repellents, insecticide-treated bednets and treated clothing. The
literature on the effectiveness of personal protection products against arthropods is
mainly limited to studies of prevention of bites, rather than prevention of disease.
Tungiasis was successfully controlled by application of topical repellents and scrub
typhus was reduced through the use of treated clothing. Successful reduction of
leishmaniasis was achieved through the use of topical repellents, treated bednets
and treated clothing in individual studies. Malaria has been reduced by the use of
insecticide-treated bednets (ITN), certain campaigns involving topical repellents, and
the combination of treated bednets and topical repellents. Although area repellents such
as mosquito coils are used extensively, their ability to protect humans from vector-
transmitted pathogens has not been proven. Taken together, the literature indicates
that personal protection measures must be used correctly to be effective. A study
that showed successful control of malaria by combining treated bednets and topical
repellents suggests that combinations of personal protection measures are likely to be
more effective than single methods. Implementation of successful programmes based
on personal protection will require a level of cooperation commonly associated with
other basic societal functions, such as education and food safety.

Key words. Individual prevention, insecticide-treated bednet, integrated pest manage-

ment, malaria, mosquito, mosquito coil, public health, repellent, vector-borne disease.

Introduction Common sense and experience with the public suggest that the
perceived essential advantage of repellents is that they can be
Repellents continue to be widely available in a variety of easily used by the individual, imparting a sense of control over
forms. One previous study estimated that total sales of topical exposure to biting arthropods. In the present study, we attempt
repellents in the U.S. is $200 million per year and growing to review the relevant literature that provides evidence, either
(Black, 2003), motivated by West Nile virus and Lyme disease. direct or circumstantial, that repellents can contribute towards
The U.S. Environmental Protection Agency (EPA) lists 684 disease prevention. The evidence is not quantified in a meta-
registered topical repellent products on their repellent data set, analysis, but considered in a simple logic of the most relevant
which is part of a laudable attempt to inform the consumer studies.
about protection times from mosquitoes and ticks (U.S. EPA, For the purposes of this study, we would like to consider
2011). The reasons for the popularity of insect repellents repellents defined broadly to include some of the products
are difficult to quantify, although there have been open- designed for use by an individual or small group to reduce
source studies of opinions (Frances & Debboun, 2007) and the number of bites from hematophagous arthropods (White,
many proprietary marketing studies by major manufacturers. 2007). Such products include topical repellents applied directly

Correspondence: Dr Daniel Strickman, USDA ARS National Program Staff, Room 4-2112, 5601 Sunnyside Ave., Beltsville, MD 20705-5148,
U.S.A. Tel.: 301-504-5771; Fax: 301-504-4873; E-mail: [email protected]

Published 2012. This article is a U.S. Government work and is in the public domain in the USA. 1
 13652915, 2013, 1, Downloaded from https://resjournals.onlinelibrary.wiley.com/doi/10.1111/j.1365-2915.2012.01020.x by Cochrane Philippines, Wiley Online Library on [01/05/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
2 M. Debboun and D. Strickman

to the skin, but they also include compounds on clothing, a short period of time. This study reviews the literature on
insecticide-treated bednets (ITN) and various devices that emit the prevention of disease in individuals by repellents, includ-
vapour or droplets into a small space (e.g. mosquito coils) ing repellents on the skin, in clothing and dispersed in the
(Strickman et al., 2009). Area repellents, ITNs and treated air. We did not consider possible population level effects, such
clothing often have insecticidal as well as repellent properties, as selection of vector populations that do not tend to feed
but our review of the literature discussed below showed that on humans or direction of vector populations to lethal treat-
combinations of these methods are more likely to protect ments (‘push-pull’ strategy). We conclude that on a practical
individuals; therefore, a review of personal protective measures level, repellents can reduce the incidence of disease caused by
that are not strictly speaking repellents was necessary. The use vector-borne pathogens but they can only rarely eliminate the
of these products have a long history (Moore & Debboun, risk because of the imperfections of use by individuals.
2007), but it is only since 1942 that there has been a concerted
effort to use repellents to prevent transmission of arthropod-
borne pathogens. During that year, the Orlando Laboratory Integrated disease control and the range of repellent products
of the U.S. Department of Agriculture was funded by the
National Emergency Council (as requested by the U.S. Army Integration of disease control is seen by some as an essen-
Surgeon General) to develop methods for protection of military tial move towards effective management of tropical diseases
personnel from epidemic typhus, scrub typhus, plague and (Grépin & Reich, 2008). The basic idea of integration applied
malaria. The result was the development of many of the to disease control is that linkages between those programmes
modern strategies for vector control that we take for granted that exist can make actual health delivery as good as possi-
now, including highly effective, synthetic repellents (Knipling, ble within the local context. Entomological interventions and
1949; Joy, 1999). other activities usually grouped as environmental health are
Major government agencies have endorsed the use of often organized by entities outside of the more usual veteri-
repellents as an important part of an individual’s protection nary and public health communities; therefore, the integration
from infection. The EPA currently has a web page (U.S. EPA, of entomological interventions into health delivery is likely to
2010) that helps people find an appropriate topical repellent. require a special effort. A fair question asked by human health
The introductory material includes the following statement: practitioners is whether entomological interventions actually
reduce disease incidence, rather than just relieve the annoyance
Effective insect repellents can protect you of arthropod bites. Presumably, good evidence for the effec-
from serious mosquito- and tick-borne diseases. tiveness of repellents in reducing the incidence of infections
In the United States, mosquitoes can transmit by vector-borne pathogens resulting in disease would allow
diseases like St. Louis encephalitis and West Nile public health strategists to integrate repellent use into their pro-
virus. Ticks can transmit serious diseases like grammes. The concept of integrated pest management is more
Lyme disease, Rocky Mountain spotted fever, familiar to entomologists and its commonly designated compo-
and Ehrlichiosis. nents of risk assessment, surveillance, control and sustainabil-
ity (Strickman, 2008) could certainly be applied to integrated
The U.S. Centers for Disease Control and Prevention (CDC) disease control. In the context of integrated disease control,
made the positive statement that, ‘Repellents are an important this would mean defining the disease to be controlled, deter-
tool to assist people in protecting themselves from mosquito- mining where its aetiological agent is transmitted, assembling
borne diseases’ (CDC, 2008). They specifically recommended the right tools for both medical and entomological intervention,
topical repellents containing DEET (Frances, 2007a), Picaridin and designing a programme that can achieve its goals perma-
(Frances, 2007b), p-menthane-3,8-diol (PMD) (Strickman, nently by constant response to the real and current situation.
2007a), or IR3535 (Puccetti, 2007) and repellents for clothing There is a wide range of repellent products available for con-
that contain permethrin. The U.S. military promotes personal sideration in an integrated disease control programme. Topical
protection using treated clothing and topical repellents (as well repellents are applied as a spray, lotion or cream directly on
as other personal protective measures) in a detailed manual exposed skin. The inherent efficacy of each product depends on
(Armed Forced Pest Management Board, 2009), which states its active ingredients and its formulation. The usual standard is
that chemical repellents can be the only means available to for complete protection from the target arthropod, so that rela-
avoid bites and associated diseases under certain conditions. tive effectiveness is judged by duration of protection (Barnard
The logic of disease prevention is that repellents reduce the et al., 2007). In fact, this standard is unrealistic and thorough
number of arthropod bites and that arthropod bites are a neces- tests in the field often indicate that protection is high (greater
sary step in the transmission of vector-borne pathogens; there- than 95%) but not perfect even shortly after application. On the
fore repellents reduce the occurrence of infection and disease. other hand, the protective effect does not cease suddenly and
This simple syllogism is not nearly as obvious as it sounds, there is partial protection for some period after biting becomes
principally because only one inoculative bite is required for noticeable (Barnard & Xue, 2007). Area repellents (Strick-
infection and in some situations multiple inoculative bites man, 2007b) are products that disperse a chemical into the air,
would be received over a short period of time. Under those repelling or killing flying, biting arthropods from the immedi-
circumstances, stopping a proportion of bites might have no ate vicinity. The most common area repellents are coils that
effect on the incidence of disease as enough vectors overcome burn a flammable matrix to release gaseous and finely particu-
the repellent to increase the chances of getting infected over late active ingredient into the air. The repellent action of coils is
Published 2012. This article is a U.S. Government work and is in the public domain in the USA. Medical and Veterinary Entomology, 27, 1–9
 13652915, 2013, 1, Downloaded from https://resjournals.onlinelibrary.wiley.com/doi/10.1111/j.1365-2915.2012.01020.x by Cochrane Philippines, Wiley Online Library on [01/05/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Insect repellents for disease control 3

presumed to last as long as the coil is burning but as protection Anopheles culicifacies (Diptera: Culicidae) Giles, annularis
is seldom near 100%, the percentage of bites is the usual mea- Van der Wulp and subpictus Grassi. They found that DEET-
sure of effectiveness. Other area repellent products are not based repellents prevented 93–100% of bites during 11 h at
nearly as common as coils, but they either actively dissemi- night, by contrast with indoor use of mosquito coils that
nate a chemical through heating (e.g. electrically heated mats provided only about 76% protection.
or liquids for indoor use) or air currents. The active ingredients A more critical attempt to relate bite protection to disease
of most area repellent products are pyrethroids that kill some protection has been made by Kiszewski & Darling (2010).
insects and repel others. Repellents can also be applied to cloth- They proposed that the following equation could be used to
ing (McCain & Leach, 2007). There is a long history of the make a quantitative estimate of Plasmodium (Haemospororida:
use of various chemicals, the current standard being permethrin Plasmodiidae) Marchiafava & Celli transmission from mea-
applied as a spray, dip, soak or integrated into the textile during surements of repellent efficacy:
manufacture. Treated clothing stops bites through the cloth or
deters chiggers and ticks from attaching; the clothing does not Fe = (1 − sh)b(1−rc)
affect bites on adjacent exposed skin and not every insect that
contacts the clothing is killed. Finally, ITNs are a popular tool where
for malaria control, especially in sub-Saharan Africa (Lengeler, Fe = the probability that a person avoids malaria during
2009). Current systems either depend on soaking the nets in the given time period
insecticidal solution or integrating insecticide into the nets at s = sporozoite rate in mosquitoes
the time of manufacture. In anti-malaria programmes, ITNs are
h = the proportion of infective bites that cause disease
advocated as a relatively inexpensive and long-lasting method
b = bites per person per time period
to protect people from night-biting vectors of the Plasmodium
r = proportion of bites avoided by wearing repellent
pathogens. There is also evidence that ITNs can be helpful in
c = proportion of people who use the repellent (product
preventing transmission of leishmaniasis (Elnaiem, 2011) and
acceptance).
Chagas disease (Kroeger et al., 2003).
The expectation that repellents will reduce the incidence of A hypothetical application of this model showed that a
disease caused by vector-borne pathogens is repeated often in repellent that prevents 98% of bites and is used by 98% of the
the literature. Gupta & Rutledge (1994) summarized repellent population will reduce the cases of malaria by 88.9% during
systems and their history, stating that repellents are a cheap a 7-month transmission season in which 1.5% of mosquitoes
and practical way to prevent bites and disease. They gave are infected and a person receives an average of 40 bites per
examples that represented well-documented disease reduction night. The calculated reduction in disease becomes much less
achieved with repellent clothing (scrub typhus; McCulloch, as efficiency of protection (r × c in the equation) decreases
1946) and topical repellents (sand fly fever; Philip et al., 1944). or as the number of bites per day increases. For example, the
They also described studies that were less well controlled decrease in malaria incidence during 7 months is only 48.2% if
in which the use of local preparations for cosmetics or the repellent prevents 95% of bites and 80% of people use the
emollients were associated with reductions in malaria. More product. An unpublished report by Del Cielo (Appawu et al.,
recently, Goodyer et al. (2010) performed an extensive review 2011), a private enterprise promoting the use of repellent for
of comparative efficacy, concluding that the topical active malaria prevention in the poorest communities, used data from
ingredients DEET, Picaridin and PMD, as well as treated Kassena Nankana District, Ghana to calculate the reduction in
clothing and ITNs, offered the best potential protection from disease from actual use experience. In that community they
malaria. They concluded that IR3535 was a less effective observed a biting rate of 86 Anopheles gambiae (Diptera:
topical repellent and that citronella, neem, essential oils and Culicidae) Giles and funestus Giles bites per person per
area repellent systems are inadequate to significantly reduce night and 1% of those mosquitoes infected (entomological
the risk of disease. inoculation rate of 418 infective bites per person per year).
Another expression of the expectation of disease protection Distribution of ‘NO MAS,’ Del Cielo’s repellent containing
is in reviews of operational or experimental repellent use. Cope PMD and lemongrass oil in a water-based formulation, resulted
et al. (1996) suggested that the low incidence of leishmaniasis in its use by 97% of the people and investigators measured 90%
(31 cases) and sand fly fever (no cases) among 697 000 protection from bites. Using Kiszewski and Darling’s equation,
American military personnel participating in Operation Desert an untreated population in the same area would have had 1.87%
Storm in Saudi Arabia, Iraq, and Kuwait from December 1990 of its inhabitants infected with malaria per night compared with
to May 1991, was as a result of the use of insecticides, only 0.25% infected if they used NO MAS. This would reduce
repellents and other protective measures. The authors stated the number of cases by 75.8% during 3 months at a cost of
that the incidence of the two diseases might have been US$0.033 per person per day.
higher during warmer parts of the year and Killick-Kendrick
& Peters (1992) thought that weather rather than repellents
were responsible. There are many other examples of testing Repellent field trials and disease reduction
protection from bites with the implication that reduction in
the number of bites will lead to less disease. Two studies There have been relatively few studies that measured dis-
in Ghaziabad, Uttar Pradesh, India (Ansari et al., 1990; ease as an outcome after the use of repellents. The lack
Mittal et al., 2011) measured the efficacy of repellents against of studies probably has many causes. First, the common
Published 2012. This article is a U.S. Government work and is in the public domain in the USA. Medical and Veterinary Entomology, 27, 1–9
 13652915, 2013, 1, Downloaded from https://resjournals.onlinelibrary.wiley.com/doi/10.1111/j.1365-2915.2012.01020.x by Cochrane Philippines, Wiley Online Library on [01/05/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
4 M. Debboun and D. Strickman

sense assumptions of efficacy outlined above may reduce the repellents that continues today (Brown et al., 2005). Field tests
motivation to invest in those studies, leading to the practice with dibutyl phthalate applied every 2 weeks to uniforms of
of distributing repellents for disease control based on hope Australian soliders resulted in a 90% decrease in scrub typhus
rather than evidence. Second, repellents are not considered to (McCulloch, 1946). Welt (1947) performed a controlled trial
be medical items and have been regulated based mainly on with American soldiers from August to November 1944. One
safety rather than efficacy. Finally, the standards for clinical battalion (approximately 600 people) did not receive treatment,
studies based on the principles of informed human consent, the uniforms of another battalion were sprayed with dimethyl
good laboratory practice, double-blind design (in which neither phthalate and the uniforms of 2.5 battalions (approximately
the investigators nor subjects can detect whether a placebo or 1500 people) were treated with an emulsion formulation of
treatment is administered) and sufficient sample size to achieve dimethyl phthalate. All of the soldiers then performed combat
significant statistical power, are considered extremely costly operations for 7–10 days in areas with scrub typhus transmis-
compared with the potential financial market for the products. sion. The dimethyl phthalate spray reduced the number of cases
Nonetheless, there appears to be more interest in performing by 64% (from 45 cases in the control group to 16 cases in the
repellent trials that measure disease as the principal outcome. sprayed group) and the emulsion reduced the number of cases
This interest is in response to the admirable increase in effort by 94% (to 7 cases).
to establish better programmes for control of diseases caused Most repellent trials that measured a reduction in disease
by vector-borne pathogens. were directed at malaria. Some studies have failed to show any
Non-infectious diseases for which the arthropod is the significant effect on transmission, in spite of thorough sampling
direct cause of pathology are often not considered to be of and analysis. Schoepke et al. (1998) collected survey data
major public health significance, but these conditions can be from European tourists returning from East Africa, analysing
extremely important in communities where they are common. the responses of 89 617 people. They found that 1.8% of
Although not technically considered vectors, these insects can them (1594 people) reported using all possible preventive
impair the health of a community as surely as an infectious measures, including sleeping in air conditioned rooms and
disease. One example is pediculosis, the infestation of people taking chemoprophylactic drugs. Surprisingly, these thorough
with lice (Burgess, 1993). An effective repellent applied after measures only reduced malaria incidence by 50% compared
treatment would be useful to prevent the reinfestation as with people who took no precautionary measures at all (4.8%,
individuals were sequentially treated. Another example is the 4319 people). Corrected for chemoprophylaxis, the analysis
chigoe flea, Tunga penetrans (Siphonaptera: Hectopsyllidae) showed that only sleeping in an air conditioned room and
(Linnaeus), infestations of which can incapacitate people. wearing long sleeves and trousers were significantly related to
Schwalfenberg et al. (2004) and Feldmeier et al. (2006) a lower malaria risk; bednets, aerosol insecticide spray, topical
reported careful trials in Fortaleza, Brazil using a cosmetic repellents, vitamin B, mosquito coils and electric fumigators
product with repellent properties to nearly eliminate (92% made no difference. Local residents (n = 547) in the Chennai
reduction) infestations that had affected half the community. (Madras) region of India who sought diagnosis in a malaria
Two of the early successes using repellents to reduce infectious clinic were questioned about their use of repellent measures,
disease involved sand fly fever and scrub typhus. In a previous dividing the respondents into those with malaria and those
paper that is one of the classics of medical entomology, without malaria (Srinivas et al., 2005). The only significant
Cornelius Philip teamed up with two scientists who went on risks were failure to close windows and doors at night [odds
to great fame in the battle against polio, John R. Paul and ratio (OR) 1.61 after adjustment for other factors] and having
Albert B. Sabin (Philip et al., 1944). They identified sand fly at least one member of the family with a history of malaria
fever transmitted by sandflies as a key problem for the U.S. (OR 1.64). Of all the patients, 7% with malaria used topical
military stationed in Cairo during World War II because each repellents, 13% used insecticidal mats and 43% used mosquito
case involved 6–10 days off duty. In 1943, they reported that coils, compared with 2%, 14% and 44% without malaria,
25% of the troops were infected. In a controlled trial from respectively.
24 September to 30 October 1943 they showed that 2 out Treated clothing provided significant protection from malaria
of 57 (3.5%) non-immune volunteers treated with repellent and leishmaniasis during a study conducted in Colombia (Soto
were infected compared with 12 out of 83 (14.5%) untreated et al., 1995). Soldiers who wore permethrin-treated uniforms
volunteers, resulting in a 76% reduction in disease. They used 24 h per day for 4.2 weeks had 75% less malaria (3 cases
military issue dimethyl phthalate on exposed skin, applied just out of 86 soldiers) than a group with untreated uniforms (12
before going to bed. cases out of 86 soldiers). The soldiers with treated uniforms
Scrub typhus, caused by Orientia tsutsugamushi (Rick- exposed in an area with infected sand flies for 6.6 weeks had
ettsiales: Rickettsiaceae) (Hayashi) and transmitted by chiggers 83% less leishmaniasis (4 cases out of 143 soldiers) compared
in the genus Leptotrombidium (Trombidiformes: Trombiculi- with soldiers with untreated uniforms (18 cases out of 143
dae) Nagayo, remains an important rickettsial disease in Asia soldiers). By contrast, Thai soldiers in a highly endemic area
and Australasia, although the advent of modern antibiotics has of Sisaket Province were not protected from malaria by wear-
greatly reduced mortality (Smadel et al., 1948; Kelly et al., ing permethrin-treated uniforms (Eamsila et al., 1994). During
2002). Effective clothing repellents were developed by the U.S. October through to April 1992, 44.5% of 137 soldiers with
Department of Agriculture (Madden et al., 1944), largely solv- treated uniforms got malaria compared with 39.5% (n = 266)
ing the problem for the U.S. military during World War II and in the placebo group. These soldiers were not given any
establishing a precedent for the treatment of uniforms with instruction to wear their uniforms at night and they were not
Published 2012. This article is a U.S. Government work and is in the public domain in the USA. Medical and Veterinary Entomology, 27, 1–9
 13652915, 2013, 1, Downloaded from https://resjournals.onlinelibrary.wiley.com/doi/10.1111/j.1365-2915.2012.01020.x by Cochrane Philippines, Wiley Online Library on [01/05/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Insect repellents for disease control 5

given topical repellents. In a modification of treated clothing, among 530 people) in the placebo group, indicating a statis-
Rowland et al. (1999) issued permethrin-treated headscarves tically significant 56% reduction. By contrast, P. vivax cases
to Afghan women (n = 395) in a Pakistani refugee camp. The were not reduced in the treated group, possibly because of
headscarves were typically used by men, women and children relapses from infections acquired before the study. A study was
as a top sheet while sleeping. When malaria incidence was performed in a similar community (Rowland et al., 2004b) in
14.8% per year, they observed a 64% reduction among chil- which the soap was offered for sale and residents surveyed on
dren up to 10 years old and a 38% reduction among people whether or not they used the soap and ITNs. Use of the soap
less than 20 years old, but no reduction among people more was associated with a 45% decrease in malaria, ITN use was
than 20 years old. associated with a 46% decrease and use of both the soap and
There is a great deal of literature on the effectiveness of ITNs was associated with a 69% decrease (n = 709). Only
ITNs, summarized in a meta-analysis by Lengeler (2009). Five 43% of the households purchased the soap and only 7.8%
trials with childhood mortality as an endpoint showed 17% pro- recalled using it within the previous 10 days, suggesting that
tection compared with no net and 23% protection compared user acceptance of the soap was not high but that those with
with an untreated net. Overall, the use of ITNs would save greater risk of transmission used the soap more frequently.
5.5 children’s lives per year per thousand children. Another More conventional topical repellents were used successfully
21 studies indicated that ITNs reduce the incidence of malaria against malaria in South Africa. Durrheim & Govere (2002)
in areas of stable Plasmodium falciparum (Haemospororida: provided a product with 15% DEET to the community of
Plasmodiidae) Welch transmission by 50% and in areas of Albertsnek, South Africa (population 850) during 21 weeks
unstable transmission by 62%. Plasmodium vivax (Haemo- in 2000. The interiors of residences had been sprayed with
spororoida: Plasmodiidae) Grassi & Feletti transmission was deltamethrin the previous December, but flooding had wetted
reduced by 52%. In Africa, the challenge for ITNs is con- walls and compromised the effectiveness of the insecticide.
sidered to be effectiveness rather than efficacy, in that the Residents were instructed to apply the repellent to their ankles
impact of ITNs is influenced by the use patterns of individ- and feet at sunset and again just before going to sleep. The
uals (Lengeler & Snow, 1996). ITNs were also useful in Latin application was limited to the part of the body most commonly
America. A trial in Chinandega, Nicaragua showed that in bitten by Anopheles arabiensis (Diptera: Culicidae) Patton, the
households where 31–70% of people used ITNs, the homes had principal vector of the area. This procedure reduced malaria
68% less malaria (Kroeger et al., 1999). A 35-week Thai study cases from 42 per week at the beginning of treatment to an
(Kamol-Ratanakul & Prasittisuk, 1992) showed less effective- average of 16 cases per week during the final 8 weeks.
ness in Chonburi, where those who slept under ITNs (n = 126) The most thorough trial of the efficacy of repellents for
were only 6% less likely to get malaria than those who slept a reduction in malaria was funded recently by the Bill and
under untreated nets (n = 135). Melinda Gates Foundation in Beni, Bolivia (Hill et al., 2007).
Topical repellents’ effect on malaria transmission has been This careful study followed standard procedures for clinical
studied in various ways and with a number of unusual products. trials, being double-blind and placebo-controlled. It involved
Pregnant Karen tribeswomen (n = 897) near the Thai-Burmese 4008 volunteers in 860 homes for a total of 15 174 person-
border participated in a 17-month trial (McGready et al., 2001) months of risk examined. All used ITNs and half (2041 people,
of traditional thanaka cosmetic [extract of Limonia acidissima 436 homes) used 10 mL of 30% PMD applied to the legs, arms
(Sapindales: Rutaceae) L.] compared with thanaka mixed with and neck between dusk and bed time. The repellent group had
20% dimethylbenzamide (an analogue of DEET). Although an 80% reduction in P. vivax malaria and an 82% reduction
the incidence among women with the repellent cosmetic was in P. falciparum malaria (although not statistically significant
lower (10.6% incidence of P. falciparum; 21.1% incidence of because of the small number of cases). The use of the repellent
P. vivax ) than among the women with normal cosmetic (14.8% from after dusk combined with ITNs resulted in an overall
P. falciparum, 26.4% P. vivax ), the difference was not statis- reduction of fever by 58%. The authors concluded that use of
tically significant. A repellent soap from Australia containing repellents combined with ITNs could protect local populations,
20% DEET and 0.5% permethrin has been used in Ecuador as well as travellers, from malaria.
and Peru (Kroeger et al., 1997) and Pakistan (Rowland et al.,
2004a). Properly applied, the soap is put on as a normal wet
solution, but it is not rinsed off. In Ecuador, a village with the Practical considerations and future developments
soap started with a malaria prevalence of 12.8% and completed
the study with a prevalence of 8.5%, which was no difference A review of the literature on the use of topical repellents,
from a village without the soap (starting at 14% prevalence and ITNs, and area repellent devices has implications for research
ending at 6.7%). The Peruvian village with soap had 25% less needs and, more importantly, for effective use of these impor-
malaria (prevalence starting at 13.9% and ending at 17.9%) tant tools. In many ways, evaluation of ITNs is at a mature
than the village without soap (starting at 12.6% and ending at stage where further studies can be focused on local conditions,
24.1%), but the difference was not significant. The trial in Pak- new combinations of methods or new kinds of ITNs, rather
istan involved 25% of an Afghan refugee village (population than on proof of the concept. This sort of research may be nec-
3945) in Northwest Frontier Province. During 6 months, the essary in spite of the extensive testing done to date, exactly as
people using the soap had an incidence of 3.7% P. falciparum considerable effort is expended to test marketed products for
(23 cases among 618 people) compared with 8.9% (47 cases refinement of their application, integration with other methods
Published 2012. This article is a U.S. Government work and is in the public domain in the USA. Medical and Veterinary Entomology, 27, 1–9
 13652915, 2013, 1, Downloaded from https://resjournals.onlinelibrary.wiley.com/doi/10.1111/j.1365-2915.2012.01020.x by Cochrane Philippines, Wiley Online Library on [01/05/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
6 M. Debboun and D. Strickman

and to monitor effectiveness. ITNs clearly reduce the incidence Topical repellents offer much promise as important tools for
of malaria in many situations, but they have never been shown prevention of infections from vector-borne pathogens. Under
to eliminate all transmission. The implication is also clear that the best application conditions, current products often provide
they would provide a level of protection from other pathogens nearly 100% protection from flying insects and significant pro-
transmitted by flying insects that bite at times when a person is tection from ticks. Although there is a vigorous search for addi-
under the bed net. Future studies and product development will tional active ingredients, real advances for disease control are
probably further improve efficacy by selection of alternative dependent on improvements in use. The widespread application
chemicals for resistance management (Pennetier et al., 2005, of those improvements is highly dependent on acceptance of
2007) and adjustment of the many economic and cultural fac- their efficacy by the public health community, which remains
tors that influence actual use by the individual (Kroeger et al., justifiably skeptical about topical repellents’ place in vector
2002). The indication that an additional reduction in malaria control. The recent high-quality studies of topical repellents’
can be achieved by combining ITNs with topical repellents use against malaria have shown that they can reduce transmis-
points to the continuing need for studies on the integration sion under at least some circumstances, especially in conjunc-
of methods. In spite of the strong evidence provided by indi- tion with what has become standard use of ITNs. Calculated
vidual studies, the quantitative relationship between protection effectiveness based on much more economical studies of bite
provided by ITNs and topical repellents can only be calculated protection and user acceptability might be a practical method
based on assumptions of biting rate and transmission. Many for wider evaluation of topical repellents, with the caution that
more studies with disease as an endpoint would be necessary diversion to untreated members of a population is a real possi-
to understand the use of these two tools to the point that there bility (Moore et al., 2007). Other potential negative aspects of
would be reliable predictions of effectiveness. widespread repellent use might be selection of species that are
Although treated clothing is widely used by the military, its tolerant to the repellents (Klun et al., 2004), development of
actual effectiveness in preventing malaria and other diseases resistance to repellents (Stanczyk et al., 2010), or unexpected
caused by pathogens transmitted by flying insects appears health impacts of long-term, consistent application. It is diffi-
to be highly dependent on its use. The inherent problem cult to evaluate the practical danger from development of resis-
is that people do not generally sleep in their clothes and tance or selection for species that are naturally more tolerant to
important vectors bite at night. Another problem is that topical repellents, as coverage is seldom high enough to consti-
treated clothing does not protect the individual from bites on tute a strong selective mechanism. Safety of products evaluated
exposed skin. In the authors’ opinion, additional development by the U.S. Environmental Protection Agency, at least, is eval-
of clothing products that improve textiles as mechanical uated based on assumptions of continuous use, so that concerns
barriers, alternatives to pyrethroid active ingredients and the over long-term use might not be as serious as assumed.
use of volatile components that protect adjacent exposed skin The authors think that the technical challenges for public
would be welcome improvements. By contrast, treated military health use continue to be ease of application, user accept-
uniforms appear to be highly effective at preventing scrub ability and price, exactly as is the case for ITNs. Indications
typhus because vectors of the pathogens tend to bite under that active ingredients could be many-fold more effective than
clothing and they must pass over or under treated cloth before DEET and other current active ingredients based on interrup-
attachment. Further studies on use of treated clothing by tion of mosquito receptor physiology (Jones et al., 2011) raises
civilians are needed, especially with respect to Lyme disease in the possibility of completely new kinds of products that might
the United States and Europe, where the use of treated clothing make topical repellents a much more important tool for disease
for this purpose is based more on hope than evidence. It seems control.
unlikely that treated clothing will ever be an important tool for The authors offer the following opinion of the current
large populations exposed to malaria and dengue because of relationship between disease prevention and insect repellents,
the difficulty of assuring that a large proportion of all clothing based on the literature reviewed in this study and recent
is treated; however, improvements would certainly be justified comprehensive summaries of bite protection. Broadly defined,
for a reduction in risk based on occupational or recreational repellents are products used by individuals to reduce the num-
exposure. ber of bites from haematophagous arthropods. If these products
Area repellent systems, especially mosquito coils, are pop- stopped all biting all of the time, there would be no question
ular for relief from flying, biting insects, but the level of that they would be the complete solution for prevention of
protection is much less than 100% and their effectiveness is disease from vector-borne pathogens. Of course, repellents are
dependent on air movement when outdoors. Another potential not such universally effective tools because their effectiveness
drawback is that all current systems depend on dispersal of a is not perfect and their use is dependent on many factors. Iron-
volatile or finely dispersed chemical, raising concerns about ically, individual application is both the biggest appeal and the
various inhalation hazards. The most widely used area repel- biggest limitation to repellent use. By contrast, an effective
lent device, the burning mosquito coil, has never been properly repellent places control of disease in the hands of the per-
tested for its effectiveness at preventing malaria (Lawrance & son who needs protection. However, individual application by
Croft, 2004). Further development and evaluation of area repel- millions of people inevitably results in variation in the qual-
lent systems is justified in spite of their limitations because the ity of application and consequent impact on transmission of
public continues to want such technology, suggesting that a pathogens. Although it is true that a reduction in the num-
truly effective system would make a big difference in public ber of bites cannot hurt, it is also true that limited prevention
health. of bites may not have any impact at all on disease when the
Published 2012. This article is a U.S. Government work and is in the public domain in the USA. Medical and Veterinary Entomology, 27, 1–9
 13652915, 2013, 1, Downloaded from https://resjournals.onlinelibrary.wiley.com/doi/10.1111/j.1365-2915.2012.01020.x by Cochrane Philippines, Wiley Online Library on [01/05/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Insect repellents for disease control 7

entomological inoculation rate is even moderately high. To the Durrheim, D.N. & Govere, J.M. (2002) Malaria outbreak control in
extent that medical entomologists are responsible members of an African village by community application of ‘deet’ mosquito
the public health community, and to the extent that entomolog- repellent to ankles and feet. Medical and Veterinary Entomology,
ical interventions are accepted by the medical community, we 16, 112–115.
need to work towards evidence-based, intelligent application of Eamsila, C., Frances, S.P. & Strickman, D. (1994) Evaluation of
current repellent tools and development of new ones that fill permethrin-treated military uniforms for personal protection against
gaps in our armamentarium. Integrated disease control, rather malaria in northeastern Thailand. Journal of the American Mosquito
than simply reducing the number of bites, requires careful test- Control Association, 10, 515–521.
ing of combinations of methods in order to assemble a series Feldmeier, H., Kehr, J.D. & Heukelbach, J. (2006) A plant-based
of partially effective measures into a single programme that repellent protects against Tunga penetrans infestation and sand flea
reduces the health burden to an acceptable level. Implementa- disease. Acta Tropica, 99, 126–136.
tion of a programme that depends on action by all individuals in Frances, S.P. (2007a) Efficacy and safety of repellents containing
deet. Insect Repellents: Principles, Methods, and Uses (ed. by
a community is always going to be a challenge, but not a hope-
M. Debboun, S.P. Frances & D. Strickman), pp. 311–326. CRC
less one. Societies have had success influencing populations
Press, Boca Raton, FL.
to participate effectively to accomplish complicated objectives
Frances, S.P. (2007b) Picaridin. Insect Repellents: Principles, Methods,
such as education and food safety. The same community par-
and Uses (ed. by M. Debboun, S.P. Frances & D. Strickman),
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pp. 337–340. CRC Press, Boca Raton, FL.
to prevent disease from vector-borne pathogens should also be
Frances, S.P. & Debboun, M. (2007) User acceptability: public per-
possible.
ceptions of insect repellents. Insect Repellents: Principles, Meth-
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