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Plant Extracts, Isolated Phytochemicals, and Plant-Derived Agents Which Are Lethal to Arthropod Vectors of Human Tropical Diseases - A Review

22 Mar 2011-Planta Medica (© Georg Thieme Verlag KG Stuttgart · New York)-Vol. 77, Iss: 6, pp 618-630
TL;DR: Examples of plant extracts, EOs, and isolated chemicals exhibiting noxious or toxic activity comparable or superior to the synthetic control agents of choice (pyrethroids, organophosphorous compounds, etc.) are provided in the text for many arthropod vectors of tropical diseases.
Abstract: The recent scientific literature on plant-derived agents with potential or effective use in the control of the arthropod vectors of human tropical diseases is reviewed. Arthropod-borne tropical diseases include: amebiasis, Chagas disease (American trypanosomiasis), cholera, cryptosporidiosis, dengue (hemorrhagic fever), epidemic typhus (Brill-Zinsser disease), filariasis (elephantiasis), giardia (giardiasis), human African trypanosomiasis (sleeping sickness), isosporiasis, leishmaniasis, Lyme disease (lyme borreliosis), malaria, onchocerciasis, plague, recurrent fever, sarcocystosis, scabies (mites as causal agents), spotted fever, toxoplasmosis, West Nile fever, and yellow fever. Thus, coverage was given to work describing plant-derived extracts, essential oils (EOs), and isolated chemicals with toxic or noxious effects on filth bugs (mechanical vectors), such as common houseflies (Musca domestica Linnaeus), American and German cockroaches (Periplaneta americana Linnaeus, Blatella germanica Linnaeus), and oriental latrine/blowflies (Chrysomya megacephala Fabricius) as well as biting, blood-sucking arthropods such as blackflies (Simulium Latreille spp.), fleas (Xenopsylla cheopis Rothschild), kissing bugs (Rhodnius Stal spp., Triatoma infestans Klug), body and head lice (Pediculus humanus humanus Linnaeus, P. humanus capitis De Geer), mosquitoes (Aedes Meigen, Anopheles Meigen, Culex L., and Ochlerotatus Lynch Arribalzaga spp.), sandflies (Lutzomyia longipalpis Lutz & Neiva, Phlebotomus Loew spp.), scabies mites (Sarcoptes scabiei De Geer, S. scabiei var hominis, S. scabiei var canis, S. scabiei var suis), and ticks (Ixodes Latreille, Amblyomma Koch, Dermacentor Koch, and Rhipicephalus Koch spp.). Examples of plant extracts, EOs, and isolated chemicals exhibiting noxious or toxic activity comparable or superior to the synthetic control agents of choice (pyrethroids, organophosphorous compounds, etc.) are provided in the text for many arthropod vectors of tropical diseases.

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Introduction
!
Arthropod vectors of human
tropical disease
Arthropods are the vectors of a variety of human
diseases which affect tropical countries around
the world (
l
"
Table 1)[122]. Biting, blood-suck-
ing arthropods are the most important vectors in
terms of public health. These include mosquitoes,
tsetse flies [7], kissing bugs, sandflies, ticks, etc.,
which are responsible for the transmission of ma-
laria, dengue hemorrhagic fever, filariasis [7],
American [36] and Human African [7] trypano-
somiasis, leishmaniasis [7,13], spotted [7, 18],
West Nile, and yellow fevers [7], among other se-
vere tropical diseases. Importantly, several doz-
ens of species of anopheline mosquitoes are re-
sponsible for the transmission of the 4 Plasmo-
dium parasite species which cause human ma-
laria. According to data from the World Health Or-
ganization (WHO), half the worldʼs human popu-
lation lives in regions where malaria is endemic
[7]. On the other hand, non-biting or non-blood-
sucking coprophagic (feces-eating), saprophagic
(living on decaying or decomposing materials),
and other arthropods, such as dung beetles, com-
mon houseflies, and cockroaches can be mechan-
ical vectors of amebiasis [1,2], cholera [7, 8], cryp-
tosporidiosis [1,7], giardia [1, 10, 11], isosporiasis
[12], sarcocystosis [1], toxoplasmosis [1, 16], and
Abstract
!
The recent scientific literature on plant-derived
agents with potential or effective use in the con-
trol of the arthropod vectors of human tropical
diseases is reviewed. Arthropod-borne tropical
diseases include: amebiasis, Chagas disease
(American trypanosomiasis), cholera, cryptospor-
idiosis, dengue (hemorrhagic fever), epidemic ty-
phus (Brill-Zinsser disease), filariasis (elephantia-
sis), giardia (giardiasis), human African trypano-
somiasis (sleeping sickness), isosporiasis, leish-
maniasis, Lyme disease (lyme borreliosis), ma-
laria, onchocerciasis, plague, recurrent fever, sar-
cocystosis, scabies (mites as causal agents), spot-
ted fever, toxoplasmosis, West Nile fever, and yel-
low fever. Thus, coverage was given to work de-
scribing plant-derived extracts, essential oils
(EOs), and isolated chemicals with toxic or noxi-
ous effects on filth bugs (mechanical vectors),
such as common houseflies (Musca domestica Lin-
naeus), American and German cockroaches (Peri-
planeta americana Linnaeus, Blatella germanica
Linnaeus), and oriental latrine/blowflies (Chryso-
mya megacephala Fabricius) as well as biting,
blood-sucking arthropods such as blackflies (Si-
mulium Latreille spp.), fleas (Xenopsylla cheopis
Rothschild), kissing bugs (Rhodnius Stål spp., Tria-
toma infestans Klug), body and head lice (Pedicu-
lus humanus humanus Linnaeus, P. humanus capi-
tis De Geer), mosquitoes (Aedes Meigen, Anopheles
Meigen, Culex L., and Ochlerotatus Lynch Arri-
bálzaga spp.), sandflies (Lutzomyia longipalpis
Lutz & Neiva, Phlebotomus Loew spp.), scabies
mites (Sarcoptes scabiei De Geer, S. scabiei var
hominis, S. scabiei var canis, S. scabiei var suis ),
and t icks (Ixodes Latreille, Amblyomma Koch, Der-
macentor Koch, and Rhipicephalus Koch spp.). Ex-
amples of plant extracts, EOs, and isolated chem-
icals exhibiting noxious or toxic activity compara-
ble or superior to the synthetic control agents of
choice (pyrethroids, organophosphorous com-
pounds, etc.) are provided in the text for many ar-
thropod-vectors of tropical diseases.
Supporting information available online at
http://www.thieme-connect.de/ejournals/toc/
plantamedica
Plant Extracts, Isolated Phytochemicals, and
Plant-Derived Agents Which Are Lethal to
Arthropod Vectors of Human Tropical Diseases
A Review
Authors Adrian Martin Pohlit
1,2
, Alex Ribeiro Rezende
2
, Edson Luiz Lopes Baldin
3
, Norberto Peporine Lopes
2
,
Valter Ferreira de Andrade Neto
4
Affiliations
1
Instituto Nacional de Pesquisa da Amazônia, Manaus, Amazonas State, Brazil
2
Universidade de São Paulo, Ribeirão Preto, São Paulo State, Brazil
3
Universidade Estadual de São Paulo, Botucatu, São Paulo State, Brazil
4
Universidade Federal de Rio Grande do Norte, Natal, Rio Grande do Norte State, Brazil
Key words
l
"
botanicals
l
"
acaricide
l
"
insecticidal and larvicidal
plants
l
"
plant extracts
l
"
essential oils
l
"
biotechnology
l
"
natural products
l
"
phytochemicals
received Sept. 23, 2010
revised February 19, 2011
accepted March 4, 2011
Bibliography
DOI http://dx.doi.org/
10.1055/s-0030-1270949
Published online March 22,
2011
Planta Med 2011; 77: 618630
© Georg Thieme Verlag KG
Stuttgart · New York ·
ISSN 00320943
Correspondence
Prof. Valter Ferreira
de Andrade Neto, PhD
Departamento de Microbiologia
e Parasitologia
Laboratório de Biologia
da Malária e Toxoplasmose
Universidade Federal
do Rio Grande do Norte
Campus Universitário
Av. Senador Salgado Filho
Lagoa Nova
CEP 69061-000 Natal RN
Brazil
Phone: + 55 84 3215 34 37
ext. 2 26
Fax: +558432119210
aneto@cb.ufrn.br
618
Pohlit AM et al. Plant Extracts, Isolated Planta Med 2011; 77: 618630
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other infectious diseases and so must also be controlled for rea-
sons of disease prevention and public health (
l
"
Table 1).
Literature on Plants for Arthropod Vector Control
!
In recent years, numerous scientific reports have been published
on plants which are usefl (or potentially useful) for the control of
arthropod vectors of tropical diseases. Major emphasis has been
on the most important arthropod-vector the mosquito. Reviews
of the scientific literature have been published recently on mos-
quito larvicidal plant extracts and fractions [19], plant EOs exhib-
iting arthropod-killing (mosquitocidal, larvicidal) among other
biological activities [20], and mosquito repellent and insecticidal
plant EOs and chemical components [2123]. The patent litera-
ture on plant EO-containing mosquito repellent inventions is also
reviewed in this special issue of Planta Medica [24]. In the present
review, emphasis is on literature published in the period 2007
2010 describing plant extracts and their active chemical compo-
nents which cause the death of or are noxious to one or more of
Table 1 Human tropical diseases, etiological agents, and arthropod vectors.
Tropical disease Arthropod vector
Name Etiologic agent Occurrence Common name Scientific name Source
Amebiasis Entamoeba
histolytica, E. díspar
China, Mexico, S. America,
S.-E. & W. Africa, S.-E. Asia
German cockroach Blatella germanica Linnaeus [1, 2]
American cockroach Periplaneta americana Linnaeus
Common housefly Musca domestica Linnaeus
Chagas disease
(American
trypanosomiasis)
Trypanosoma
cruzi
Americas, Europe Kissing bug Triatoma, Rhodnius Stål spp.,
Panstrongylus megistus Burmeister
[36]
Cholera Vibrio cholerae Worldwide Common housefly Musca domestica Linnaeus [7, 8]
Cryptosporidiosis Cryptosporidium sp. Africa, Asia, Australia, Europe,
Americas
Dung beetle Onthophagus Latreille,
Anoplotrupes Jekel & Aphodius Illiger spp.
[1, 7]
Common housefly Musca domestica Linnaeus
Dengue
(hemorrhagic fe-
ver)
Flavirus sp. Africa, Americas,
E. Mediterranean, S.-E. Asia & W.
Pacific
Mosquito Ae. Aegypti L., Ae. Albopictus Skuse [7]
Epidemic typhus
(Brill-Zinsser disease)
Rickettsia prowazekii Africa, C. & S. America Louse Pediculus humanus corporis [9]
Filariasis or
Elephantiasis
Wuchereria bancrofti Africa, Asia, S. America Mosquito Aedes Meigen, Anopheles Meigen,
Culex L. spp.
[7]
Giardia, giardiasis Giardia lamblia Worldwide German cockroach Blatella germanica Linnaeus [1, 10,11]
Common housefly Musca domestica Linnaeus
Human African
trypanosomiasis
(sleeping sickness)
Trypanosoma
brucei
Africa Tsetse fly Glossina Wiedemann spp. [7]
Isosporiasis Isospora belli Africa, Australia, Caribbean
Islands, Latin America, S.-E.
Asia
Dung beetle Onthophagus Latreille spp. [12]
Common housefly Musca domestica Linnaeus
Leishmaniasis Leishmania sp. Asia, C. & S. America, E. Africa,
Europe, India
Sandfly Lutzomyia França, Phlebotomus Loew &
Sergentomyia França & Parrot spp.
[7, 13]
Lyme disease
(lyme borreliosis)
Borrelia spp. Asia, Europe, Americas Tick Ixodes Latreille, Amblyomma Koch spp. [14, 15]
Malaria Plasmodium spp. Africa, Mexico, C. & S. America,
Asia
Mosquito Anopheles Meigen spp. [7]
Onchocerciasis Onchocerca volvulus Africa, Mexico, C. & S. America Blackfly Simulium Latreille spp. [7]
Plague Yersinia pestis Africa, Asia, Brazil, Bolivia, Peru,
Ecuador, USA
Oriental rat flea Xenopsylla cheopis Rothschild [10]
Recurrent fever Borrelia recurrentis Africa, Asia, Europe, N. America Louse Pediculus humanus spp. [14]
Tick Ornithodoros C. L. Koch spp.
Sarcocystosis Sarcocystis spp. Worldwide German cockroach Blatella germanica Linnaeus [1]
American cockroach Periplaneta Americana Linnaeus
Common housefly Musca domestica Linnaeus
Scabies Worldwide (Itch) Mite Sarcoptes scabiei var hominis [17]
Spotted fever Rickettsia rickettsii Brazil, Colombia, Mexico,
Panama, Canada, USA
Tick Dermacentor Koch, Rhipicephalus Koch,
Amblyomma Koch spp.
[7, 18]
Toxoplasmosis Toxoplasma gondii Worldwide Dung beetle Onthophagus Latreille spp. [1, 16]
German cockroach Blatella germanica Linnaeus
American cockroach Periplaneta americana Linnaeus
Common housefly Musca domestica Linnaeus
Oriental latrine
or blowfly
Chrysomya megacephala Fabricius
West Nile fever Flavivirus sp. Worldwide Mosquito Culex L. spp., Ochlerotatus Lynch Arribálzaga
spp.
[7]
Yellow fever Flavivirus sp. Africa, Latin America Mosquito Ae. aegypti L., Ae. albopictus Skuse [7]
619
Pohlit AM et al. Plant Extracts, Isolated Planta Med 2011; 77: 618630
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the developmental stages (eggs, nymphs/larvae, pupae, adults) of
a broad range of arthropod vectors of human tropical diseases
such as blowflies, common houseflies, cockroaches, fleas, lice,
mosquitoes, ticks, etc.
The plant sources of extracts, EOs, fractions, and isolated com-
pounds which exhibit toxicity to, are noxious to, or are otherwise
useful in the control of arthropods covered herein are terrestrial
plants which generally have medicinal and other useful (eco-
nomic) properties. Edible green and blue-green algae (cyanobac-
terium) having toxic properties towards insect species including
larvae of Aedes Meigen, Anopheles Meigen, and Culex L. spp. were
recently reviewed [25]. Thus, algae and aquatic plants are not
covered herein nor are arthropod/insect control derivatives from
bacteria and fungi (such as Bacillus thuringiensis israelensis, B.
sphaer icus,andSaccharopolyspora spinosa/Spinosad
®
) cultures.
Blackflies
The water extracts of the leaves of Chromolaena odorata (L.) R.M.
King & H. Rob. exhibited lethality to larvae of Simulium damno-
sum Theobald (LC
50
= 1 µg/mL) which was not statistically differ-
ent from that of the synthetic organophosphorous larvicide chlo-
pyrifos [26].
Hydrogenated catnip (Nepeta cataria L. leaf, stem) EO containing
15 weight-percent (wt %) of stereoisomeric dihydronepetalac-
tones (1.67 g/m
2
) as active repellent ingredients was formulated
into a liquid and a lotion both of which provided > 7.5 h mean
complete protection against adult Simulium decorum Walker in
the field [27].
Remarkably, in a field study in Thailand, the blackfly Simulium ni-
grogilvum Summers was effectively repelled by lotions contain-
ing 10% w/w EO in absolute ethanol (60%) and additives vanillin
(10%), propylene glycol (10%), and polyethylene glycol (10%).
Thus finger root (Boesenbergia rotunda [L.] Mansf.) EO, guava
(Psidium guajava L.) leaf EO, and turmeric ( Curcuma longa L.) EO
were separately formulated into lotions which were tested to-
gether with the proprietary product Repel Care
®
(active ingre-
dients: 5% w/w turmeric EO and 4.5% w/w Eucalyptus citriodora
Hook. EO) and DEET (10% w/w lotion formulated as for EOs). All
five formulations provided 100% protection for 9 h and > 82% for
10 and 11 h against S. nigrogilvum [28].
Blowflies
Topical application of eucalyptol (1,8-cineole) caused the death of
Chrysomya megacephala Fabricius adult males and females
(LD
50
= 197 and 221 µg/fly, respectively) [29]. Eucalyptol exhib-
ited low activity against C. megacephala third instars (LD
50
=
642 µg/µL) using the dipping method. Also, Azadirachta indica
A. Juss. seed extracts (containing 0.24% azadirachtin A) caused
swelling of the protocuticle of third instars and first stage pupae
of C. megacephala by the dipping method [30]. Larvae of C. mega-
cephala were effectively killed by betel (Piper betle L.) EO. At con-
centrations of 34% betel EO, 100% larvae mortality was ob-
ser ved [31]. Nine plant EOs were screened for ovicidal activity
against C. megacephala and Eugenia caryophyllata Thunb., Illicium
verum Hook. f. and Cinnamomum cassia (L.) C. Presl EOs exhibited
the most activity (LC
50
= 1.61, 2.49, and 0.43 mg/mL, respectively).
Also, synthetic cinnamaldeyde showed ovicidal activity
(LC
50
= 0.28 mg/mL) [32].
Cockroaches
Pure components from EOs were screened for lethality against
different developmental stages of Blatella germanica Linnaeus
[34]. Topically applied pure components caused the death of
adult males, females, gravid females, and nymphs at different
stages of development of B. germanica. The most active sub-
stances against B. germanica adult males were thymol, E-cinna-
maldehyde, carvacrol, and eugenol (LD
50
= 0.070, 0.078, 0.101,
0.109 mg/cockroach, respectively). Against B. germanica adult fe-
males the most active substances were carvacrol, E-cinnamalde-
hyde, and thymol (LD
50
= 0.186, 0.188, and 0.195 mg/cockroach,
respectively), and these same substances were also the most ac-
tive against gravid B. germanica:thymol>E-cinnamaldehyde >
carvacrol (LD
50
= 0.122, 0.133, and 0.146 mg/cockroach, respec-
tively).
Large B. germanica nymphs were also susceptible to topical treat-
ment with EO components, and for large nymphs the most active
substances were E-cinnamaldehyde, carvacrol, and thymol
(LD
50
= 0.117, 0.129, and 0.220 mg/cockroach, respectively) while
for medium nymphs the most active substances were thymol,
carvacrol, E-cinnamaldehyde, and eugenol (LD
50
= 0.060, 0.061,
0.082, and 0.109 mg/cockroach, respectively) [34]. Small B. ger-
manica nymphs were the most sensitive to natural components
of EOs, and substances exhibited activity in the following order:
E-cinnamaldehyde > thymol ~ geraniol > carvacrol ~ S-()-limo-
nene > ()-menthone (LD
50
= 0.0360.060 mg/cockroach). Dimin-
ished nymph hatching was observed for B. germanica eggs treat-
ed with ()-menthone. Based on these and other data, the group
of substances thymol, E-cinnamaldehyde, carvacrol, geraniol, and
eugenol exhibited interesting lethality to different stages of de-
velopment of B. germanica [34].
Using a T-tube olfactometer, 17 EOs were screened, and 5 EOs ex-
hibited signif icant repellency against B. germanica and other
cockroach species. Thus, adult female Periplaneta americana Lin-
naeus (American cockroach) and B. germanica (German cock-
roach) were repelled by grapefruit (Citrus × paradisi Macfad.),
lemon (Citrus × limonum Risso), lime [Citrus × aurantiifolia
(Christm.) Swingle], orange [Citrus × sinensis (L.) Osbeck] EOs by
90.3, 85.7, 83.3, and 70.0%, respectively, and 96.7, 92.9, 86.7, and
71.4%, respectively [33]. Adult female B. germanica were also re-
pelled by clove leaf (Eugenia caryophyllata Thunb.) EO (repel-
lency = 70.0%). Another cockroach, Periplaneta fuliginosa Serville,
was less repelled by these Citrus L. spp. EOs: 82.4, 72.0, 70.6, and
62.5%, respectively. Yoon et al. [33] identified two different
types of Citrus oils based on the relative quantity of the compo-
nents limonene (> 90% = type I = grapefruit and orange EOs; 48
61% = type II = lemon and lime EOs) and α-pinene, β-pinene, γ-
terpinene, β-myrcene, and benzene. Generally, type I EOs exhib-
ited repellencies which could be reproduced by placing the vol-
ume of pure limonene present in 10 µL of EO in the olfactometer
for both B. germanica and P. americana. To study the effects of
type II EOs, limonene (6.4 µL) combined with β-pinene (1.4 µL)
was found to provide repellency (90.3%) comparable to that of
10 µL of lemon and lime (type II) EOs against B. germanica. Adult
female B. germanica were repelled about equally by limonene (ca.
6.1 µL) + β-pinene (1.6 µL) or 10 µL of type II (lemon and lime)
EOs. In a ternary mixture of limonene + β-myrcene + γ-terpinene
(6.1 + 0.1 + 0.4 µL), a repellency of 83.3% was attained which was
comparable to the type II EO repellency against adult female
B. germanica. When the individual components were tested for
repellency against P. americana adult females in the volumes
present in 10 µL of type II EOs, β
-pinene (1.17 µL) fully repro-
620
Pohlit AM et al. Plant Extracts, Isolated Planta Med 2011; 77: 618630
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duced the repellency of 10 µL of lime EO. For type II EOs, to repro-
duce the repellent effect of 10 µL of lime and lemon EOs to adult
P. americana, only ternary combinations of limonene (6.1 µL) + γ-
terpinene (0.4 µL) + [either β-myrcene (0.1 µL), β-pinene (1.4 µL),
or α-pinene (0.2 µL)] produced repellencies (8083 %) compara-
ble to those of both type II EOs [33]. This work demonstrates the
very complex synergistic and suppressive interactions among the
monoterpenes in these Citrus EOs and the species specific nature
of repellency in these cockroach species.
Common houseflies
Solvent extracts of plants and isolated chemical components
have been tested for important control effects mainly against ma-
ture Musca domestica Linnaeus. Thus, seed and root petroleum
ether extracts of Griffonia simplicifolia (M. Vahl ex DC.) Baill. and
root and stem petroleum ether extracts of Zanthoxylum xan-
thoxyloides (Lam.) Waterman repelled (median repellent doses,
RD
50
=1.01.7 µg/cm
2
) and killed mature M. domestica (topical
LC
50
=0.305 µg/fly) [35]. In other work, EtOH extracts of
A. indica which contain the active ingredient azadirachtin A were
found to be highly lethal to adult flies (94% mortality) at a con-
centration of 0.025%, but were only moderately lethal to earlier
stages (larvae, pupae) even at higher concentrations [30]. Couma-
rin was isolated from the hexane extract of the leaves of Age-
ratum conyzoides L. and shown to be highly toxic (LD
50
=1.2,
LD
90
= 3.7 mg/g) to mature M. domestica [36]. Also, friedelin was
isolated from Cacalia tangutica (Maxim.) Hand.-Mazz. extract
and (as a coating on sugar) was found to be as lethal
(LC
50
= 0.130 mg/g sugar) to mature M. domestica as rotenone
(LC
50
= 0.091 mg/g sugar) which was used as control substance
[37]. These examples demonstrate the potential of plant extracts
and their active principles as sources of control agents for mature
M. domestica.
A number of plant EOs and volatile chemical components exhib-
iting adulticidal activity against M. domestica have been identi-
fied in recent publications. Eucalyptus LʼHér. spp., Citrus × sinensis
(L.) Osbeck, Lavandula angustifolia Mill., Mentha L. spp., and Pe-
largonium graveolens LʼHér. EOs were found to effectively knock
down and kill M. domestica (KT
50
=318 min; LD
50
=0.07
0.16 µg/insect) [38]. Several of the isolated monoterpenes of
these EOs, namely 1,8-cineole (KT
50
= 2.3 min, LD
50
= 0.13 µg/in-
sect), limonene (KT
50
= 7.5 min, LD
50
= 0.10 µg/insect), linalool
(KT
50
= 7.6 min, LD
50
= 0.04 µg/insect), menthone (KT
50
=19.0
min, LD
50
= 0.11 µg/insect), and menthyl acetate (KT
50
= 22.6 min,
LD
50
= 0.09 µg/insect) were found to be toxic to M. domestica [38].
However, an independent study on 1,8-cineole found much low-
er lethal doses against M. domestica mature males (LD
50
= 118 µg/
fly) and females (LD
50
= 177 µg/fly) [29]. In another screening for
fumigant activity, C. sinensis, Citrus × aurantium L., Citrus × limo-
num Risso, Citrus × paradisi Macfad., Citrus × reticulata Blanco, Cor-
iandr um sativum L., Eucalyptus cinerea F. Muell. ex Benth., Laurus
nobilis L., and Myristica fragrans Houtt. EOs werefound to be active
(LC
50
=3.98.8 mg/cm
3
) against mature M. domestica, and several
of the monoterpene components of these EOs were evaluated for
activity against M. domestica. Besides 1,8-cineole (LC
50
= 3.3 mg/
dm
3
), () and (+)-limonene (LC
50
= 5.0 and 6.2 mg/dm
3
, respec-
tively), chemical components such as γ-terpinene (LC
50
= 4.0 mg/
dm
3
), α-terpinene (LC
50
= 6.2 mg/dm
3
), citronellal (LC
50
= 8.1 mg/
dm
3
), ()-β-pinene (LC
50
= 6.4 mg/dm
3
), and ()-α-pinene
(LC
50
= 8.9 mg/dm
3
) were also found to be toxic to mature
M. domestica [39]. Phenylpropanoids are another class of volatile
compounds having important lethality to M. domestica.Ina
recent study on the lethality of the EO and chemical components
from the leaves of Piper betle L. to M. domestica,EO
(LC
50
= 10.3 mg/dm
3
) and individual phenylpropanoid EO com-
ponents safrole (LC
50
= 4.8 mg/dm
3
), dihydrosafrole (LC
50
=4.7
mg/dm
3
), isosafrole (LC
50
= 2.3 mg/dm
3
), and eugenol
(LC
50
= 7.3 mg/dm
3
) all proved to have significant toxicity to ma-
ture M. domestica [40].
In the Supporting Information, data from literature sources on
plant extracts, EOs, monoterpenes, and phenylpropanoids exhib-
iting fumigant and other activities against M. domestica are pre-
sented.
Dung beetles
No recent studies on plant extracts, oils, or chemical components
for the control of Anoplotrupes Jekel & Aphodius Illiger spp. of
dung beetles were found. This could be an interesting group for
future study given that these filth-associated organisms exist in
many countries around the world where basic hygiene and coex-
istence with these species may be a source of contamination and
infections (
l
"
Table 1).
Fleas
Incense cedar (Calocedrus decurrens [Torr.] Florin) heartwood EO
(LC
50
= 0.24, LC
90
= 0.31 mg/mL), Port-Orford [Chamaecyparis
lawsoniana (A. Murray) Parl.] cedarwood EO (LC
50
= 1.21, LC
90
=
1.85 mg/mL), and western juniper (Juniperus occidentalis Hook.)
heartwood EO (LC
50
= 0.31, LC
90
= 0.93 mg/mL) exhibited adultici-
dal effects on Xenopsylla cheopis Rothschild fleas [41].
Isolated components from Alaska yellow cedar (Chamaecyparis
nootkatensis [D. Don] Spach) heartwood EO, derivatives, and
commercially acquired products were tested against X. cheopis.
Carvacrol, valencene, nootkatene, crystalline nootkatone, noot-
katone grapefruit extract, isolated nootkatone, valencene-13-ol,
nootkatol, valencene-13-aldehyde, nootkatone 1,10 epoxide,
nootkatone diepoxide all were act ive against X. cheopis exhibiting
LC
50
= 0.00290.064% w/v and LC
90
= 0.00490.10% w/v 24 h
after exposure. Nootkatone (grapefruit EO) was the most active
sample tested (LC
50
= 0.0029, LC
90
= 0.008% w/v) [42].
Kissing bugs (assassin bugs, bloodsucking conenoses,
barbeiros)
24 plant extracts were screened for insecticidal activity against
fourth stageblood-replete nymphs of Rhodnius milesi Carcallo, Ro-
cha, Galvão & Jurberg by applying 50 µg of each extract to the ab-
domen of the nymphs. Hexane and ethanol extracts of Simarouba
versicolor A.St.Hil., Guarea kunthiana A. Juss., G. guidonia (L.)
Sleumer, and Talauma ovata A.St.Hil. caused 2095% mortality
among nymphs, and the ethanol extract of the root bark of S. versi-
color and hexane extrac t of the roots of G. guidonia were responsi-
ble for 95 and 75% nymph mortalities, respectively [43].
Topically applied Pilocarpus spicatus A. St.Hil. leaf EO was toxic
to and paralyzed Rhodnius prolixus Stål fifth stage male nymphs
(0.5 and 1.0 µL EO/insect, 90.5 and 91.1% mortality, respectively,
after 24 h; 89 and 92% paralysis of surviving nymphs after 15
days) as well as retarded moulting and had partial antifeedant ef-
fects [44]. In other work, EOs and monoterpenes were screened
for fumigant activity (exposure to vapors emitted by 100 µL of
EO or monoterpene in a closed vessel) against R. prolixus first in-
stars. Eucalyptus EO was the most active fumigant
(KT
50
= 216 min) and eucalyptol (1,8-cineole) was the most active
fumigant monoterpene (KT
50
= 117 min) [45].
621
Pohlit AM et al. Plant Extracts, Isolated Planta Med 2011; 77: 618630
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In the above work, EOs and monoterpenes were also screened for
repellency against R. prolixus first instars. Thus, mint and laven-
der EOs produced slight repellent effects at 400 µg/cm
2
; geraniol
and menthyl acetate produced slight repellent effects, respective-
ly, at 40 and 400 µg/cm
2
; and menthone produced a slight repel-
lent effect at 400 µg/cm
2
[45].
Schinus molle L. leaf and root hexane extracts exhibited greater
repellency than DEET against first instars of blood-sucking cone-
noses Triatoma infestans Klug. Also, 3% w/v (maximum concen-
tration tested) hexane extract of the fruit of S. molle caused 80%
inhibtion of hatching of T. infestans eggs [46].
Lice
Hedychium spicatum Buch.-Ham. ex Sm. rhizome EO at 15% con-
centrations exhibited pediculicidal activity against human body
lice (Pediculus humanus humanus) which was greater than a 1%
permethrin based produc t which was tested for comparison
[47]. In other work, head lice (P. humanus capitis) were killed by
the ethyl acetate extracts of the seeds of custard apple (Annona
squamosa L.), and the hexane extract of seeds contains oleic acid
(13.88 wt %) and a triglyceride with one oleate ester (7.70 wt %).
Ethyl acetate extract, oleic acid, and triglyceride with one oleate
ester were diluted (1:1) in inactive coconut oil and found to kill
clinically obtained P. humanus capitis in 31.7, 47.3, and 10.0 min,
respectively [48]. In another study involving clinically-obtained
third instars and adult head lice (P. humanus capitis), 1,8-cineole
was found to inhibit acetylcholine-esterase in a homogenate of
P. humanus capitis and was found also to cause intoxication
(knockdown) after 20 min of exposure to 1,8-cineole vapor. This
result was better than contact with the standard lice control
compound DDVP (dichlorvos) which after 60 min of exposure
had only knocked down 50% of head lice [49]. This same group
of researchers tested 23 monoterpenoid compounds for ovicidal
and fumigant activity (adulticide activity) in permethrin-resist-
ant P. humanus capitis. Of 6 monoterpenes screened, only (+)-α-
pinene (KT
50
= 34.5 min) and ()-α-pinene (KT
50
= 28.5 min) had
fumigant activity against adult P. humanus capitis [50]. These au-
thors compared this result to previous work by the group in
which 1,8-cineole (KT
50
= 11.1 min), anisole (KT
50
= 12.7 min),
limonene (KT
50
= 27.2 min), β-pinene (KT
50
= 33.9 min), linalool
(KT
50
= 37.7 min), menthone (KT
50
= 39.7 min), α-pinene (KT
50
=
42.7 min), and benzyl alcohol (KT
50
= 59.7 min) were shown to
be active fumigants against adult P. humanus capitis.
Louse egg mortalities > 80% relative to negative controls were ob-
tained for anisole (100%), α-pinene (97%), β-pinene (96%), (+)-α-
pinene (96%), 1S-()-α-pinene (94%), anethole (93%), carvone
(92%), limonene (90%), linalool (88%) and 1,8-cineole (84%)
[50]. These results demonstrate the potential use of monoter-
penes and other substances in the control of permethrin-resist-
ant head lice.
Mosquitoes
Several recent reviews have been published on mosquito control
agents from plants and related topics. In 2010, Nerio et al. [23]
published a review on mosquito-repellent EOs and their repel-
lent components. Both Bakkali et al.ʼs 2008 review [20] on the bi-
ological activity and toxicity of EOs and components and Burfield
&Reekieʼs (2005) review [21] on EOs and components for mos-
quito control included data from publications on larvicidal, adul-
ticidal, and other biological activities related to mosquito control.
In the present work, the literature on plant extracts, fractions,
and isolated chemical components having useful biological activ-
ities for mosquito control were reviewed. Given the large number
of publications, emphasis was given to literature describing the
lethal activity of isolated phytochemicals against mosquitoes. As
Supporting Information, adulticidal, larvicidal, and ovicidal activ-
ities and other effects of plant extracts, essential oils, and frac-
tions are summarized for publications which failed to report bio-
logical activity for isolated component chemicals (active princi-
ples) and which were not covered in this review. Also, Supporting
Information includes data on extracts, EOs, and fractions as well
as most nonvolatile active components discussed in this review.
Publications on active extracts and essential oils having at least
one (isolated) active principle which is potentially relevant for
the purpose of mosquito control are discussed below.
Mosquitocides
EOs and their isolated components which exhibit important fu-
migant activity in knockdown and adulticide assays against mos-
quito species have been the subject of recent publications. Kiran
and Devi [88] described fumigant activity of Chloroxylon swiete-
nia DC. EO to adult An. gambiae, Cx. quinquefasciatus, and Ae. ae-
gypti (LD
50
= 1.0, 1.2, and 1.7 µg/cm
3
, respectively; KT
50
= 0.32,
0.50, and 0.72 h, respectively). This f umigant activity was attr i-
buted to sesquiterpene components present in the EO such as
germacrene D (LD
50
= 1.8, 2.1, and 2.8 µg/cm
3
, respectively)
which was purportedly acting synergistically with other compo-
nents in the EO (EO was more active than these individually
tested components) (
l
"
Table 4). In other work, Eucalyptus spp.
EOs exhibited general efficiency in knocking down adult Ae. ae-
gypti (KT
50
=412 min), which was associated with the presence
of 1,8-cineole and other components in the EOs (
l
"
Table 4) [89].
These authors also confirme d the relationship between the vapor
pressure of Eucalyptus spp. EOs and highly active individual com-
ponents such as 1,8-cineole, α-pinene, and p-cymene and me-
dian knockdown time (KT
50
)inAe. aegypti adult mosquitoes.
Mentha × piperita L. was also found to be highly active against
mature Ae. aegypti [90]. Chloroxylon swietenia, Eucalypt us spp.,
and Mentha × piperita EOs contain a number of volatile mos-
quitocidal chemical components whose fumigant activity was
investigated in the above studies and is summarized in
l
"
Table
4. Knockdown times of just 46 min were observed for 1,8-cin-
eole, p-cymene, and α -pinene (Eucalyptus spp.) against mature
Ae. aegypti while mugetanol, α-terpineol, and thymol (found in
Mentha L. spp. EO) were highly effective at knocking down and
killing mature Ae. aegypti, An. tessellates Theobald, and Cx. quin-
quefasciatus. Interestingly, L-menthol was found not to be toxic
to adult Ae. aegypti [90]. This is a reminder that molecular and
taxonomic specificities may be important characteristics of the
toxic effects of certain mosquitocidal substances.
Mosquito larvicides
A. indica or neem oil formulations are important mosquito con-
trol agents, and a formula containing 0.15% of the limonoid aza-
dirachtin was tested and found to be highly effective at killing Ae.
aegypti (LC
50
= 1.7 ppm) and An. stephensi Liston (LC
50
= 1.6 ppm)
in the lab and Aedes spp. (95100% reduction of larvae over 7
days), Anopheles spp. (80100% reduc tion of larvae over 3
weeks), and Culex spp. ( 80% reduction of larvae over 3 weeks)
in the field [51]. For another formulation comprised of wood
and bark chips of neem tree (A. indica) in water, effective larvici-
dal activity was observed against first thru fourth instars of An.
gambiae (IE
90
=0.120.6 g wood chips/L H
2
O) [52]. Interestingly,
no azadirachtin was found in these aqueous solutions; however,
622
Pohlit AM et al. Plant Extracts, Isolated Planta Med 2011; 77: 618630
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