Malaria Journal

Asadollahi et al. Malar J (2019) 18:436

https://doi.org/10.1186/s12936-019-3064-8

REVIEW Open Access

Effectiveness of plant‑based repellents

against different Anopheles species: a systematic
review
Amin Asadollahi1 , Mehdi Khoobdel2* , Alireza Zahraei‑Ramazani1* , Sahar Azarmi1
and Sayed Hussain Mosawi3

Abstract
Plant-based repellents have been applied for generations in traditional practice as a personal protection approach
against different species of Anopheles. Knowledge of traditional repellent plants is a significant resource for the devel‑
opment of new natural products as an alternative to chemical repellents. Many studies have reported evidence of
repellant activities of plant extracts or essential oils against malaria vectors worldwide. This systematic review aimed
to assess the effectiveness of plant-based repellents against Anopheles mosquitoes. All eligible studies on the repel‑
lency effects of plants against Anopheles mosquitoes published up to July 2018 were systematically searched through
PubMed/Medline, Scopus and Google scholar databases. Outcomes measures were percentage repellency and pro‑
tection time. A total of 62 trials met the inclusion criteria. The highest repellency effect was identified from Ligusticum
sinense extract, followed by citronella, pine, Dalbergia sissoo, peppermint and Rhizophora mucronata oils with com‑
plete protection time ranging from 9.1 to 11.5 h. Furthermore, essential oils from plants such as lavender, camphor,
catnip, geranium, jasmine, broad-leaved eucalyptus, lemongrass, lemon-scented eucalyptus, amyris, narrow-leaved
eucalyptus, carotin, cedarwood, chamomile, cinnamon oil, juniper, cajeput, soya bean, rosemary, niaouli, olive, tagetes,
violet, sandalwood, litsea, galbanum, and Curcuma longa also showed good repellency with 8 h complete repellency
against different species of Anopheles. Essential oils and extracts of some plants could be formulated for the develop‑
ment of eco-friendly repellents against Anopheles species. Plant oils may serve as suitable alternatives to synthetic
repellents in the future as they are relatively safe, inexpensive, and are readily available in many parts of the world.
Keywords: Plant, Herb, Repellent, Repellency, Systematic review, Anopheles

Background is one of the significant reasons for maternal and child-

Mosquito-transmitted diseases remain a main source of hood morbidity and mortality, including low birth weight,
illness and death [1]. Despite decades of malaria control stillbirths, and early infant death in sub-Saharan Africa [3].
efforts, malaria continues to be a major worldwide public Among 500 species of Anopheles mosquitoes known glob-
health issue with 3.3 billion persons at risk in 106 countries ally, more than 50 species can transmit malaria from the
and territories in the tropical and subtropical areas [2]. It bite of the infected female Anopheles spp. [4]. Presently,
there is no effective prophylactic anti-malarial vaccine and
no suitable preventive measure other than vector control is
*Correspondence: [email protected]; [email protected] available [5]. Thus, protection from mosquito bites is one
1
Department of Medical Entomology and Vector Control, School of the best approaches to reduce the disease incidence.
of Public Health, Tehran University of Medical Sciences, Tehran, Iran
2
Health Research Centre, Lifestyle Institute, Baqiyatallah University The use of repellents to protect people from bites of
of Medical Sciences, Tehran, Iran mosquitoes previously has been acknowledged as part
Full list of author information is available at the end of the article

© The Author(s) 2019. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing,
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Asadollahi et al. Malar J (2019) 18:436 Page 2 of 20

of an overall integrated insect-borne disease control pro- Eligibility criteria

gramme [6]. Most commercial repellents are produced by Studies were included in the present systematic review
using chemical components such as N, N-diethyl-meta- if they met these criteria: (i) full-text publication was
toluamide (DEET), Allethrin, N, N-diethyl mendelic acid written in English, (ii) inspected the repellency effects
amide, and Dimethyl phthalate [1]. It has been identified of plant extracts and essential oils against malaria vec-
that chemical repellents are not safe for public health and tors, Anopheles spp. mosquitoes, and, (iii) reported the
should be used with caution because of their detrimen- percentage of repellency or complete protection time.
tal impacts on synthetic fabric and plastic as well as toxic Following studies were excluded: studies exploring the
reactions, such as allergy, dermatitis, and cardiovascular repellency effect of chemical-based products, studies
and neurological side effects, which have been reported examining the repellency effect of animal extracts, ani-
generally after misapplication [4]. The frequent use of mal studies (studies not on human subjects), articles
synthetic repellents with chemical origin for mosquito without full texts, reviews, duplicate articles, abstracts,
control has disturbed natural ecosystems and resulted in republished data, comments, conference papers, editori-
the development of resistance to insecticides, resurgence als, and studies with insufficient data. In addition, studies
in mosquito populations, and adverse impact on non- were excluded if the information could not be extracted.
target organisms [4, 7]. Accordingly, the idea of using A screening of titles and abstracts followed by a full-text
natural mosquito repellent products as an alternative to review was performed by two investigators. All titles and
develop new eco-friendly repellents could be an amicable abstracts were screened by two independent investiga-
solution to scale back the undesirable effects on environ- tors for eligibility. If a consensus was reached, a study was
ment and human health. excluded or selected to full-text screening. If a consen-
In recent years, interest in plant-based repellents has sus was not reached, another reviewer was consulted to
been revived, as they contain a rich source of bioactive resolve any feasible discrepancies.
phytochemicals that are safe and biodegradable into non-
toxic by-products, which could be screened for insecti- Data extraction
cidal activities and mosquito repellent. Many studies After identifying the eligible studies, the following data
have reported evidence of repellant activities of plant were collected from each study by application of standard-
extracts or essential oils against malaria vectors around ized data collection form to improve accuracy and critical
the world. The present systematic review was performed appraisal: the first author name, country of origin, journal
to reveal which plant-based repellent can be relied on details, publication year, condition of study (field or labo-
to provide a prolonged and predictable protection from ratory), plant name, Anopheles species, concentration or
species of Anopheles mosquitoes without causing side dose of repellents, repellency percentage and complete
effects on human health. protection time. All data were independently extracted by
For this systematic review, all eligible studies on the two reviewers and disagreements were solved by discus-
repellency effects of plant-based repellants against sion, and if necessary, a third author was involved.
Anopheles spp. published up to July 2018 were system- A total of 383 studies were found by the initial lit-
atically searched through electronic databases PubMed, erature search of the databases. The flow diagram
MEDLINE, Web of Science, Literature retrieval System of the study selection process and excluded studies
of the Armed Forces Pest Management Board, Scopus with specific reasons is reported in Fig. 1. Of the 324
and Google Scholar using the following Medical Subject excluded citations, 102 were duplicated studies; 149
Headings (Mesh) and keywords: (((Plant [Title/Abstract]) were not relevant to the repellency effect of plants
OR Plants [Title/Abstract]) OR herbal [Title/Abstract]) on Anopheles spp. after screening titles/abstracts; 11
AND (botanical [Title/Abstract]) AND ((extract [Title/ were review publications; 8 investigated the repel-
Abstract]) OR extracts [Title/Abstract]) AND ((“essential lency impact of chemical-based repellents or animal
oil” [Title/Abstract]) OR “essential oils” [Title/Abstract]) extracts; 7 studies were conducted on laboratory ani-
AND (((((“Insect repellent” [Mesh]) OR repellents) OR mals; 12 were abstracts, conference papers, comments,
repellent) OR repellence) OR repellency) AND ((“Anoph- and editorials; 10 studies had not reported sufficient
eles” [Mesh]) OR “Anopheles” [Title/Abstract]). The data regarding the percentage of repellency or com-
search was limited to English publications. In addition, plete protection time; and, 15 studies were other irrel-
a manual search was conducted to identify further perti- evant studies. The primary eligibility process yielded
nent articles using references from retrieved studies. 59 documents and crosscheck of the references of
reviews and other databases search provided 3 further
articles [8–10]. A total of 62 studies conducted in dif-
ferent countries, including India [7–40], Thailand [4,
Asadollahi et al. Malar J (2019) 18:436 Page 3 of 20

Records identified after databases search (n=383)

Study excluded after duplicates

removal (n=102)

Studies screened (n=281)

149 articles were excluded after

evaluating the title and abstract

Full text article for eligibility (n=122)

Records excluded (n=63)

Reviews (n=11)

Explored repellency effect of chemical

products or animal extracts (n=8)

Studies that were not on human

subjects (n=7)

Abstracts, comments, conference

papers, and editorials (n=12)

Insufficient data (n=10)

Other irrelevant studies (n=15)

Crosscheck of the reviews references,

Google scholar and web of knowledge
search (n=3)

Studies included in systematic review (n=62)

Fig. 1 Study selection process, up to July 2018

5, 41–48], Ethiopia [49–52], Kenya [53–57], Germany Effectiveness of plant‑based products against Anopheles
[6], Nigeria [1], USA [58], Tanzania [59], Brazil [60], spp.
Sudan [61], Iran [62], Cameron [63] and Ivory Coast Potential plant-based repellents stratified by protec-
[64] were eventually included in the systematic review tion time with at least 4 h protection time are reported
based on the inclusion criteria for the effect of plant- in Table 2. The highest repellency effect was identified
based repellents on species of Anopheles mosquitoes. from Ligusticum sinense extract, followed by citron-
The included studies were published between 1999 ella, pine, Dalbergia sissoo, peppermint and Rhizophora
and 2018. Expect for 6 studies which were field trial, mucronata oils with complete protection time ranging
other studies were conducted on laboratory condition. from 9.1 to 11.5 h. Ethanolic 25% extract of L. sinense was
None of the studies reported the inclusion and exclu- able to completely repel Anopheles minimus for 11.5 h.
sion criteria explicitly other than specifying a healthy Furthermore, essential oils from plants such as laven-
volunteer. Table 1 summarizes the characteristics and der, camphor, catnip, geranium, jasmine, broad-leaved
main results of the eligible studies.
Asadollahi et al. Malar J (2019) 18:436 Page 4 of 20

Table 1 Characteristics of studies. Characteristics of studies included in the systematic review, up to July 2018
Study Year Country Study type Plant extract/ Concentration Anopheles species Repellency % Protection
(essential oil) dose time
(hours)

Ansari et al. 2005 India Field Pine oil (Pinus) 1 ml without dilu‑ An. culicifacies 100 11
tion
Citronella (lemon‑ 1 ml without dilu‑ An. culicifacies 100 11
grass oil) tion
Ansari et al. 2000 India Field D. sissoo oil 1 ml without dilu‑ An. culicifacies 96.1 10.3
tion
D. sissoo oil 1 ml without dilu‑ An. annularis 100 11
tion
D. sissoo oil 1 ml without dilu‑ An. subpictus 89.7 8
tion
Ansari et al. 2000 India Field Peppermint oil 1 ml without dilu‑ An. culicifacies 92.3 9.6
tion
Peppermint oil 1 ml without dilu‑ An. annularis 100 11
tion
Peppermint oil 1 ml without dilu‑ An. subpictus 83.1 7.3
tion
Amer et al. 2006 Germany Laboratory Citronella (Cym- 20% oil solutions An. stephensi 52.4 8
bopogon winteri-
anus) essential oils
Rosewood (Aniba 20% oil solutions An. stephensi 4.8 6.5
rosaeodora) essen‑
tial oils
Lavender (Lavan- 20% oil solutions An. stephensi 80.9 8
dula angustifolia)
essential oils
Camphor (C. cam- 20% oil solutions An. stephensi 42.8 8
phora) essential
oils
Catnip (N. cataria) 20% oil solutions An. stephensi 100 8
essential oils
Geranium (Pelargo- 20% oil solutions An. stephensi 61.9 8
nium graveolens)
essential oils
Thyme (T. serpyllum) 20% oil solutions An. stephensi 33.3 7.5
essential oils
Eucalyptus (E. globu- 20% oil solutions An. stephensi 28.6 5.5
lus) essential oils
Jasmine (Jasminum 20% oil solutions An. stephensi 100 8
grandiflorum)
essential oils
Broad-leaved euca‑ 20% oil solutions An. stephensi 38.1 8
lyptus (Eucalyptus
dives) essential oils
Lemongrass (Cym- 20% oil solutions An. stephensi 100 8
bopogon citratus)
essential oil
Lemon-scented 20% oil solutions An. stephensi 52.4 8
eucalyptus (E.
citriodora) essen‑
tial oil
Fichtennadel (Picea 20% oil solutions An. stephensi 19 3
excelsa) essential
oil
Amyris (Amyris 20% oil solutions An. stephensi 100 8
balsamifera)
essential oil
Asadollahi et al. Malar J (2019) 18:436 Page 5 of 20

Table 1 (continued)
Study Year Country Study type Plant extract/ Concentration Anopheles species Repellency % Protection
(essential oil) dose time
(hours)

Lemon (Citrus limon) 20% oil solutions An. stephensi 9.5 7

essential oil
Narrow-leaved 20% oil solutions An. stephensi 42.8 8
eucalyptus (Euca-
lyptus radiata)
essential oil
Carotin oil (Glycina 20% oil solutions An. stephensi 9.5 8
soja) essential oil
Cedarwood (Juni- 20% oil solutions An. stephensi 38.1 8
perus virginiana)
essential oil
frankincense 20% oil solutions An. stephensi 19 5
(Boswellia carteri)
essential oil
Dill (Anethum gra- 20% oil solutions An. stephensi 71.4 3.5
veolens) essential
oil
Myrtle (M. commu- 20% oil solutions An. stephensi 42.8 6.5
nis) essential oil
Chamomile 20% oil solutions An. stephensi 76.2 8
(Anthemis nobilis)
essential oil
Cinnamon (C. zey- 20% oil solutions An. stephensi 100 8
lanicum) essential
oil
Juniper (Juniperus 20% oil solutions An. stephensi 76.2 8
communis) essen‑
tial oil
Sage (Salvia sclarea) 20% oil solutions An. stephensi 19 5
essential oil
Peppermint 20% oil solutions An. stephensi 57.1 6.5
(Mentha piperita)
essential oil
Basil (Ocimum basili- 20% oil solutions An. stephensi 66.7 3.5
cum) essential oil
Cajeput (Melaleuca 20% oil solutions An. stephensi 100 8
leucadendron)
essential oil
Soya bean (Glycina 20% oil solutions An. stephensi 76.2 8
max) essential oil
Rosemary (R. offici- 20% oil solutions An. stephensi 100 8
nalis) essential oil
Niaouli (Melaleuca 20% oil solutions An. stephensi 100 8
quinquenervia)
essential oil
Olive (O. europaea) 20% oil solutions An. stephensi 71.4 8
essential oil
Black pepper (Piper 20% oil solutions An. stephensi 61.9 3
nigrum) essential
oil
Verbena (Lippia 20% oil solutions An. stephensi 38.1 5.5
citriodora) essen‑
tial oil
tagetes (T. minuta) 20% oil solutions An. stephensi 100 8
essential oil
Violet (Viola odorata) 20% oil solutions An. stephensi 100 8
essential oil
Asadollahi et al. Malar J (2019) 18:436 Page 6 of 20

Table 1 (continued)
Study Year Country Study type Plant extract/ Concentration Anopheles species Repellency % Protection
(essential oil) dose time
(hours)

Sandalwood 20% oil solutions An. stephensi 100 8

(Santalum album)
essential oil
Litsea (Litsea 20% oil solutions An. stephensi 100 8
cubeba) Essential
oil
Helichrysum (Heli- 20% oil solutions An. stephensi 47.6 6
chrysum italicum)
essential oil
Galbanum (Ferula 20% oil solutions An. stephensi 100 8
galbaniflua)
essential oil
Chamomile 20% oil solutions An. stephensi 47.6 5.5
(Chamaemelum
nobile) essential
oil
Amerasan et al. 2012 India Laboratory Cassia tora Linn 1 mg/cm2 An. stephensi 100 2
methanol extract 2.5 mg/cm2 100 2
5.0 mg/cm2 100 2.5
Abiy et al. 2015 Ethiopia Field 20% neem oil Neem and china‑ An. arabiensis 71 3
berry oils were
diluted to 20%
using Niger seed
(noog abyssinia)
oil
20% chinaberry oil Neem and china‑ An. arabiensis 70 1
berry oils were
diluted to 20%
using Niger seed
(noog abyssinia)
oil
Alayo et al. 2015 Nigeria Laboratory Cassia mimosoides Cream 0.5% w/w An. gambiae 48 –
petroleum ether Cream 1% w/w 88 –
extract
Cream 2% w/w 100 0.08
Cream 4% w/w 100 0.08
Cream 6% w/w 100 0.08
Alwala et al. 2010 Kenya Laboratory Mangifera indica 10% solution An. gambiae 100 –
essential Oil
Baskar et al. 2018 India Laboratory Atalantia mono- 50 ppm An. stephensi – 6.85
phylla essential oil
Govindarajan et al. 2010 India Laboratory Sida acuta Burm. F. 2.5 mg/cm2 An. stephensi 100 2.5
extract 5 mg/cm2 An. stephensi 100 3
Govindarajan et al. 2011 India Laboratory Ervatamia coronaria 1 mg/cm2 An. stephensi 100 2.5
extract 2.5 mg/cm2 An. stephensi 100 3
5 mg/cm2 An. stephensi 100 3.5
Caesalpinia pulcher- 1 mg/cm2 An. stephensi 100 2
rima extract
2.5 mg/cm2 An. stephensi 100 2.5
Govindarajan et al. 2011 India Laboratory 5 mg/cm2 An. stephensi 100 3
2.5 mg/cm2 An. subpictus 100 2
5 mg/cm2 An. subpictus 100 2.5
R. officinalis L. essen‑ 1 mg/cm2 An. subpictus 100 1
tial oil
2.5 mg/cm2 An. subpictus 100 1
5 mg/cm2 An. subpictus 100 1.5
Asadollahi et al. Malar J (2019) 18:436 Page 7 of 20

Table 1 (continued)
Study Year Country Study type Plant extract/ Concentration Anopheles species Repellency % Protection
(essential oil) dose time
(hours)

C. citrates Stapf. 1 mg/cm2 An. subpictus 100 1

essential oil 2.5 mg/cm2 An. subpictus 100 1.5
5 mg/cm2 An. subpictus 100 2
C. zeylanicum L. 1 mg/cm2 An. subpictus 100 1
essential oil 2.5 mg/cm2 An. subpictus 100 1
5 mg/cm2 An. subpictus 100 1.5
Govindarajan et al. 2016 India Laboratory Zingiber nimmonii 1 mg/cm2 An. stephensi 100 2
essential oil 2 mg/cm2 An. stephensi 100 2.5
5 mg/cm2 An. stephensi 100 3
Jeyabalan et al. 2003 India Laboratory P. citrosa leaf extract 0.5% An. stephensi 36 –
1% An. stephensi 51 –
2% An. stephensi 78 –
4% An. stephensi 100 –
Karunamoorthi et al. 2008 Ethiopia Laboratory Woira (O. europaea) Burning of 25 g An. arabiensis 79.7 –
smoke of dried plant
materials
Tinjut (Ostostegia Burning of 25 g An. arabiensis 90.1 –
integrifolia) smoke of dried plant
materials
Wogert (Silene mac- Burning of 25 g An. arabiensis 93.6 –
roserene) smoke of dried plant
materials
Kebercho (Echinops Burning of 25 g An. arabiensis 92.4 –
sp.) extract of dried plant
materials
Karunamoorthi et al. 2010 Ethiopia Laboratory C. citratus extract 1 mg/cm2 An. arabiensis 100 3.2
1.5 mg/cm2 An. arabiensis 100 4.4
2 mg/cm2 An. arabiensis 100 5.3
2.5 mg/cm2 An. arabiensis 100 6.3
Govindarajan et al. 2016 India Laboratory Origanum scabrum 1 mg/cm2 An. stephensi 100 2.5
essential oil 2 mg/cm2 An. stephensi 100 3
5 mg/cm2 An. stephensi 100 3.5
Haldar et al. 2014 India Laboratory Ficus krishnae smoke 30 mg/l smoked An. stephensi 18 0.16
60 mg/l smoked An. stephensi 100 0.5
90 mg/l smoked An. stephensi 100 1
Auysawasdi et al. 2015 Thailand Laboratory Curcuma longa 5% An. dirus 100 4
essential oil 10% An. dirus 100 5
15% An. dirus 100 5.5
20% An. dirus 100 5.5
25% An. dirus 100 8
E. globulus essential 5% An. dirus 100 1.7
oil 10% An. dirus 100 2.3
15% An. dirus 100 3
20% An. dirus 100 3
25% An. dirus 100 3.4
Citrus aurantium 5% An. dirus 100 1.8
essential oil 10% An. dirus 100 2.9
15% An. dirus 100 2.9
20% An. dirus 100 3
25% An. dirus 100 3.5
Asadollahi et al. Malar J (2019) 18:436 Page 8 of 20

Table 1 (continued)
Study Year Country Study type Plant extract/ Concentration Anopheles species Repellency % Protection
(essential oil) dose time
(hours)

Barnard et al. 1999 USA Laboratory Clove essential oil 25% An. albimanus 100 1.25
50% An. albimanus 100 1.5
75% An. albimanus 100 2.26
100% An. albimanus 100 3.55
Thyme essential oil 25% An. albimanus 100 0.75
50% An. albimanus 100 0.5
75% An. albimanus 100 1
100% An. albimanus 100 1.75
Kweka et al. 2008 Tanzania Laboratory Citronella 500 mg/m2 An. gambiae 81 –
Ocimum suave 500 mg/m2 An. gambiae 81 –
extract
Ocimum kilimand- 500 mg/m2 An. gambiae 73 –
scharicum extract
Citronella 500 mg/m2 An. arabiensis 85 –
O. suave extract 500 mg/m2 An. arabiensis 89 –
O. kilimandschari- 500 mg/m2 An. arabiensis 75 –
cum extract
Kovendan et al. 2012 India Laboratory A. alnifolia extract 1 mg/cm2 An. stephensi 100 2
3 mg/cm2 An. stephensi 100 2
5 mg/cm2 An. stephensi 100 2.5
Krishnappa et al. 2012 India Laboratory A. digitata crude 2 mg/cm2 An. stephensi 100 3
extract 4 mg/cm2 An. stephensi 100 3.5
6 mg/cm2 An. stephensi 100 3.5
Naine et al. 2014 India Laboratory Streptomyces sp. 1 mg/cm2 An. stephensi 100 2
VITJS4 extract 3 mg/cm2 An. stephensi 100 2
6 mg/cm2 An. stephensi 100 2
Murugan et al. 2012 India Laboratory Orange peel extract 50 ppm An. stephensi 99 –
150 ppm An. stephensi 100 0.5
250 ppm An. stephensi 100 0.05
350 ppm An. stephensi 100 1.5
450 ppm An. stephensi 100 2
Padilha et al. 2003 Brazil Field Ocimum selloi oil 10% v/v An. braziliensis 89 0.5
Konan et al. 2003 Ivory Coast Laboratory Karite nut butter oil 75% An. gambiae 100 2
Palm oil 75% An. gambiae 100 1.38
Coconut oil 75% An. gambiae 100 0.76
Maheswaran et al. 2013 India Laboratory Confertifolin essen‑ 0.62 ppm An. stephensi 100 1
tial oil 1.25 ppm An. stephensi 100 2.5
2.5 ppm An. stephensi 100 3
5 ppm An. stephensi 100 5
10 ppm An. stephensi 100 5.2
Panneerselvam et al. 2013 India Laboratory Andrographis pan- 1 mg/cm2 An. stephensi 100 2
iculata methanol 3 mg/cm2 An. stephensi 100 2.5
leaf extract
6 mg/cm2 An. stephensi 100 3
Cassia occidentalis 1 mg/cm2 An. stephensi 100 2
methanol leaf 3 mg/cm2 An. stephensi 100 2.5
extract
6 mg/cm2 An. stephensi 100 2.5
Asadollahi et al. Malar J (2019) 18:436 Page 9 of 20

Table 1 (continued)
Study Year Country Study type Plant extract/ Concentration Anopheles species Repellency % Protection
(essential oil) dose time
(hours)

Euphorbia hirta 1 mg/cm2 An. stephensi 100 2

methanol leaf 3 mg/cm2 An. stephensi 100 2
extract
6 mg/cm2 An. stephensi 100 2.5
Panneerselvam et al. 2012 India Laboratory Artemisia nilagirica 50 ppm An. stephensi 95 0.5
extract 150 ppm An. stephensi 98 0.5
250 ppm An. stephensi 100 0.5
350 ppm An. stephensi 100 1
450 ppm An. stephensi 100 2
Phasomkusolsil et al. 2011 Thailand Laboratory Cananga odorata oil 0.02 mg/cm2 An. dirus 94 –
0.10 mg/cm2 An. dirus 92 –
0.21 mg/cm2 An. dirus 92 –
C. sinensis oil 0.02 mg/cm2 An. dirus 40 –
0.10 mg/cm2 An. dirus 54 –
0.21 mg/cm2 An. dirus 84 –
2
C. citratus oil 0.02 mg/cm An. dirus 76 –
0.10 mg/cm2 An. dirus 82 –
0.21 mg/cm2 An. dirus 98 –
Cymbopogon nardus 0.02 mg/cm2 An. dirus 92 –
oil 0.10 mg/cm2 An. dirus 92 –
0.21 mg/cm2 An. dirus 98 –
E. citriodora oil 0.02 mg/cm2 An. dirus 52 –
0.10 mg/cm2 An. dirus 74 –
0.21 mg/cm2 An. dirus 86 –
O. basilicum oil 0.02 mg/cm2 An. dirus 66 –
0.10 mg/cm2 An. dirus 74 –
0.21 mg/cm2 An. dirus 96 –
S. aromaticum oil 0.02 mg/cm2 An. dirus 82 –
0.10 mg/cm2 An. dirus 92 –
0.21 mg/cm2 An. dirus 98 –
Prabhu et al. 2011 India Laboratory Moringa oleifera 20% An. stephensi 23 –
extract 40% An. stephensi 43 –
60% An. stephensi 58 –
80% An. stephensi 76 –
100% An. stephensi 90 –
Rajkumar et al. 2007 India Laboratory Centella asiatica 2% An. stephensi – 1
essential oil 4% An. stephensi – 1.78
6% An. stephensi – 2.33
Ipomoea cairica 2% An. stephensi – 2.63
essential oil 4% An. stephensi – 4.13
6% An. stephensi – 5.53
Momordica charan- 2% An. stephensi – 2.38
tia essential oil 4% An. stephensi – 3.93
6% An. stephensi – 5.38
Psidium guajava 2% An. stephensi – 0.93
essential oil 4% An. stephensi – 1.48
6% An. stephensi – 1.98
Asadollahi et al. Malar J (2019) 18:436 Page 10 of 20

Table 1 (continued)
Study Year Country Study type Plant extract/ Concentration Anopheles species Repellency % Protection
(essential oil) dose time
(hours)

Tridax procumbens 2% An. stephensi – 2.33

essential oil 4% An. stephensi – 3.78
6% An. stephensi – 5.28
Rajkumar et al. 2005 India Laboratory Solanum trilobatum 0.001% An. stephensi 100 1.15
extract 0.005% An. stephensi 100 1.3
0.01% An. stephensi 100 1.51
0.015% An. stephensi 100 1.7
0.02% An. stephensi 100 2.03
Rawani et al. 2012 India Laboratory P. tuberosa extract 1% An. stephensi 65 2.3
1.50% An. stephensi 80 4
2% An. stephensi 90 5
Reegan et al. 2015 India Laboratory Cliona celata extract 1 mg/cm2 An. stephensi 100 1.08
2.5 mg/cm2 An. stephensi 100 1.71
5 mg/cm2 An. stephensi 100 1.21
Swathi et al. 2012 India Laboratory Datura stramonium 0.1% An. stephensi – 0.35
extract 0.5% An. stephensi – 0.72
1% An. stephensi – 1.9
Seyoum et al. 2002 Kenya Semi-field Neem (A. indica) Periodic thermal An. gambiae 24.5 –
expulsion
Lemon eucalyptus Periodic thermal An. gambiae 74.5 –
(Corymbia citrio- expulsion
dora)
Wild spikenard Periodic thermal An. gambiae -13.3 –
(Hyptis suaveolens) expulsion
Lantana (Lantana Periodic thermal An. gambiae 42.4 –
camara) expulsion
Fever tea (Lippia Periodic thermal An. gambiae 45.9 –
uckambensis) expulsion
Lime basil (Ocimum Periodic thermal An. gambiae 43.1 –
americanum) expulsion
Rican blue basil (O. Periodic thermal An. gambiae 52.0 –
kilimandschari- expulsion
cum)
Tree basil (O. suave) Periodic thermal An. gambiae 53.1 –
expulsion
Khaki weed (T. Placing branches An. gambiae 54.8 –
minuta) or whole plants
inside houses
Sanghong et al. 2015 Thailand Laboratory L. sinense ethanolic 25% An. minimus – 11.5
preparations
Das et al. 2003 India Laboratory Cymbopogan mar- 1 ml without dilu‑ An. sundaicus 98 6
tinii martinii var tion
sofia oil
Nour et al. 2009 Sudan Laboratory Basil (O. basilicum L.) 0.1 ml 100 1.5
essential oil
Trongtokit et al. 2005 Thailand Laboratory C. nardus essential 10% An. dirus – 0.66
oil 50% – 0.5
100% – 1.16
P. cablin essential oil 10% An. dirus – 1.33
50% – 2
100% – 2.83
Asadollahi et al. Malar J (2019) 18:436 Page 11 of 20

Table 1 (continued)
Study Year Country Study type Plant extract/ Concentration Anopheles species Repellency % Protection
(essential oil) dose time
(hours)

Mullilam (Zanth- 10% An. dirus – 1

oxylum limonella) 50% – 2.16
essential oil
100% – 3.16
Clove (Syzygium 10% An. dirus – 1.33
aromaticum) 50% – 2.66
essential oil
100% – 3.5
Yogananth et al. 2015 India Laboratory R. mucronata oil 1 mg/cm2 An. stephensi 73 7.2
2 mg/cm2 An. stephensi 86 7.8
3 mg/cm2 An. stephensi 92 8.5
4 mg/cm2 An. stephensi 97 9.1
Tawatsin et al. 2000 Thailand Laboratory Turmeric (C. longa) 3 ml An. dirus 100 6
volatile oil
Citronella 3 ml An. dirus 100 6
Hairy basil oil 3 ml An. dirus 100 6
Singh et al. 2005 India Laboratory Cyperus rotundus 2.50% An. stephensi 95 –
Linn hexane 5% An. stephensi 99 –
extract
10% An. stephensi 100 6
Mayeku et al. 2013 Kenya laboratory Conyza newii essen‑ 0.01 g/ml An. gambiae 38 –
tial oil 0.1 g/ml An. gambiae 68 –
1 g/ml An. gambiae 100 –
Phasomkusolsil et al. 2009 Thailand Laboratory Phlai (Z. cassumu- 100 μl An. minimus – 2
nar) oil
Turmeric (C. longa) 100 μl An. minimus – 1
oil
Mah-Khwuaen (Z. 100 μl An. minimus – 0.66
limonella) oil
Citronella grass (C. 100 μl An. minimus – 2.16
nardus) oil
Orange oil (Citrus 100 μl An. minimus – 0.83
sinensis) oil
Eucalyptus (E. citrio- 100 μl An. minimus – 0.5
dora) oil
Clove (S. aromati- 100 μl An. minimus – 2
cum) oil
Trongtokit et al. 2004 Thailand Laboratory Clove oil 20% gel An. dirus – 4.5
cream 20% An. dirus – 4.8
Birkett et al. 2011 Kenya Laboratory N. cataria 0.01 mg An. gambiae 17 –
0.1 mg An. gambiae 97 –
1 mg An. gambiae 100 –
Kamaraj et al. 2011 India Laboratory A. concinna extract 500 ppm An. stephensi 21 –
Solomon et al. 2012 Ethiopia Laboratory Citronella extract 20% An. Arabiensis 73 –
Soonwera et al. 2015 Thailand Laboratory C. odorata oil 1% An. dirus 92 –
5% An. dirus 92 –
10% An. dirus 94 –
Sritabutra et al. 2011 Thailand Laboratory Eucalyptus (E. glob- 0.1 ml An. dirus – 1.58
ules) essencial oil
Peppermint (M. 0.1 ml An. dirus – 1.08
piperita) essencial
oil
Garlic (A. sativum) 0.1 ml An. dirus – 0.68
essencial oil
Asadollahi et al. Malar J (2019) 18:436 Page 12 of 20

Table 1 (continued)
Study Year Country Study type Plant extract/ Concentration Anopheles species Repellency % Protection
(essential oil) dose time
(hours)

Orange (C. sinensis) 0.1 ml An. dirus – 0.83

essencial oil
Citronella grass (C. 0.1 ml An. dirus – 0.8
nardus) essencial
oil
Lemongrass (C. 0.1 ml An. dirus – 1.63
citratus) essencial
oil
Clove (S. aromati- 0.1 ml An. dirus – 1
cum) essencial oil
Sweet basil (O. 0.1 ml An. dirus – 0.75
basilicum) essen‑
cial oil
Tavassoli et al. 2001 iran Laboratory Marigold (Calendula 50% An. stephensi – 2.15
officinalis) essen‑
tial oil
Myrtle essential oil 50% An. stephensi – 4.36
Younoussa et al. 2016 Cameroon Laboratory Annona senegalensis 4.0 mg/cm2 An. gambiae – 0.5
leaf extract 8.0 mg/cm2 An. gambiae – 1
12.0 mg/cm2 An. gambiae – 1.5
Boswellia dalzielii 4.0 mg/cm2 An. gambiae 46
leaf extract 8.0 mg/cm2 An. gambiae – 0.5
12.0 mg/cm2 An. gambiae – 1
Govindarajan et al. 2011 India Laboratory Coccinia indica 1 mg/cm2 An. stephensi 100 3
extract 2.5 mg/cm2 An. stephensi 100 3
5 mg/cm2 An. stephensi 100 3.5
Govindarajan et al. 2012 India Laboratory Cardiospermum 1 mg/cm2 An. stephensi 100 2
halicacabum oil 2.5 mg/cm2 An. stephensi 100 2.5
5 mg/cm2 An. stephensi 100 3
Govindarajan et al. 2014 India Laboratory Asparagus racemo- 1 mg/cm2 An. stephensi 100 2.5
sus crude extract 2 mg/cm2 An. stephensi 100 2.5
5 mg/cm2 An. stephensi 100 3
Govindarajan et al. 2015 India Laboratory Delonix elata crude 1 mg/cm2 An. stephensi 100 2.5
extract 2.5 mg/cm2 An. stephensi 100 3
5 mg/cm2 An. stephensi 100 3.5
Innocent et al. 2014 Kenya Laboratory Uvariodendron gor- 0.01 w/v An. gambiae 29 –
gonis essential oil 0.1 w/v An. gambiae 48 –
1 w/v An. gambiae 57 –
10 w/v An. gambiae 64 –
Clausena anisata 0.01 w/v An. gambiae 13 –
essential oil 0.1 w/v An. gambiae 21 –
1 w/v An. gambiae 42 –
10 w/v An. gambiae 56 –
Lantana vibunoides 0.01 w/v An. gambiae 26 –
essential oil 0.1 w/v An. gambiae 46 –
1 w/v An. gambiae 54 –
10 w/v An. gambiae 62 –
Asadollahi et al. Malar J (2019) 18:436 Page 13 of 20

Table 1 (continued)
Study Year Country Study type Plant extract/ Concentration Anopheles species Repellency % Protection
(essential oil) dose time
(hours)

Kumar et al. 2012 India Laboratory Sargassum wightii 2 mg/l An. sundaicus 26 –
Greville metha‑
nolic extract 4 mg/l An. sundaicus 40 –
6 mg/l An. sundaicus 57 –
8 mg/l An. sundaicus 71 –
10 mg/l An. sundaicus 89 –
Madhiyazhagan 2014 India Laboratory O. canum extract 0.49 mg/l An. stephensi 63 –
et al. 0.99 mg/l An. stephensi 77 –
1.99 mg/l An. stephensi 86 –

eucalyptus, lemongrass, lemon-scented eucalyptus, 9.6 and 7.3 h, respectively and the corresponding per-
amyris, narrow-leaved eucalyptus, carotin, cedarwood, centage repellency were 100%, 92.3% and 83.1%. In
chamomile, cinnamon oil, juniper, cajeput, soya bean, another study [6], 20% oil solutions of peppermint had
rosemary, niaouli, olive, tagetes, violet, sandalwood, 57% repellency and complete protection time for 6.5 h
litsea, galbanum, and Curcuma longa also showed good against An. stephensi. The study by Sritabutra et al. [47]
repellency with 8 h complete repellency against different also found that 0.1 ml of peppermint essential oil pro-
species of Anopheles genus. Here, the repellency impacts tect against An. dirus for 1.08 h.
of most frequent examined repellents against Anopheles
species are reported.
Cinnamomum
Citronella Cinnamomum is a genus in the Laurel family, Laura-
The repellency effect of citronella was investigated in sev- ceae, several of which are investigated for their antibac-
eral studies. Citronella is an essential oil extracted from terial activity by means of essential oils from bark and
the stems and leaves of different species of lemongrass leaves [67]. Amer et al. [6] reported that 20% oil solu-
(Cymbopogon spp.) [65]. Ansari et al. [11] found that cit- tions of both camphor (Cinnamomum camphora) and
ronella obtained from lemongrass has a 100% repellency cinnamon (Cinnamomum zeylanicum) had 100% repel-
effect against Anopheles culicifacies for 11 h. Amer et al. lency affect against An. stephensi. While, in the study
[6] and Tawatsin et al. [44] also reported that citronella conducted by Govindarajan et al. [22], C. zeylanicum at
could repel Anopheles stephensi and Anopheles dirus for 8 1 mg/cm2 showed 1 h protection against An. subpictus.
and 6 h, respectively. Moreover, 100 μl and 0.1 ml of cit-
ronella grass essential oil showed 2.16 and 0.8 h complete
protection time against An. minimus [45] and An. dirus Catnip (Nepeta cataria)
[47], respectively. The percentage repellency of citronella Catnip is a perennial plant that belongs to the mint fam-
in other studies. [6, 52, 59], depending on the concentra- ily, Labiatae. This herb is spread from central Europe
tion of extracts and Anopheles species, was reported to to central Asia and the Iranian plateaus [68]. The 20%
be 52 to 85%. oil solution of catnip in the study carried out by Amer
et al. [6], with 100% protection against An. stephensi for
8 h, had a good effectiveness in preventing Anopheles
Peppermint mosquitoes. Nevertheless, Birkett et al. [56] in Kenya
Peppermint is a hybrid mint from cross-breeding reported that the percentage repellency of catnip is dose-
spearmint (Mentha spicata) and water mint (Men- dependent as 0.01 mg, 0.1 mg, and 1 mg solutions of this
tha aquatica), which contains biologically active con- herb had repellency percentage of 17%, 97%, and 100%,
stituents and has high menthone, menthol and methyl respectively, against Anopheles gambiae.
esters. The plant, indigenous to Europe, is now wide-
spread in cultivation worldwide [66]. The effect of pep- Thyme (Thymus serpyllum)
permint on Anopheles was explored in 3 studies. Ansari Thyme is one of nine species belonging to T. serpyllum,
et al. [12] in a field trial revealed that 1 ml peppermint a perennial aromatic plant of the Mediterranean flora
oil without dilution completely repels Anopheles annu- [69]. Thymus species have been reported to possess
laris, An. culicifacies and Anopheles subpictus for 11,
Asadollahi et al. Malar J (2019) 18:436 Page 14 of 20

Table 2 Stratification of potential of plant based repellents

Protection time (hours) Plant name Concentration/dose Anopheles species

11.5 L. sinense ethanolic extract 25% An. minimus

11 Pine oil (Pinus) 1 ml without dilution An. culicifacies
Citronella (lemongrass oil) 1 ml without dilution An. culicifacies
D. sissoo oil 1 ml without dilution An. annularis
Peppermint oil 1 ml without dilution An. annularis
8 < to < 10 D. sissoo oil 1 ml without dilution An. culicifacies
Peppermint oil 1 ml without dilution An. culicifacies
R. mucronata oil 4 mg/cm2 An. stephensi
R. mucronata oil 3 mg/cm2 An. stephensi
8 D. sissoo oil 1 ml without dilution An. subpictus
Citronella (C. winterianus) essential oils 20% oil solution An. stephensi
Lavender (L. angustifolia) essential oils 20% oil solution An. stephensi
Camphor (C. camphora) essential oils 20% oil solution An. stephensi
Catnip (N. cataria) essential oils 20% oil solution An. stephensi
Geranium (P. graveolens) essential oils 20% oil solution An. stephensi
Jasmine (J. grandiflorum) essential oils 20% oil solution An. stephensi
Broad-leaved eucalyptus (E. dives) essential oils 20% oil solution An. stephensi
Lemongrass (C. citratus) essential oil 20% oil solution An. stephensi
Lemon-scented eucalyptus (E. citriodora) 20% oil solution An. stephensi
Amyris (A. balsamifera) essential oil 20% oil solution An. stephensi
Narrow-leaved eucalyptus (E. radiata) essential oil 20% oil solution An. stephensi
Carotin oil (G. soja) essential oil 20% oil solution An. stephensi
Cedarwood (J. virginiana) essential oil 20% oil solution An. stephensi
Chamomile (A. nobilis) essential oil 20% oil solution An. stephensi
Cinnamon (C. zeylanicum) essential oil 20% oil solution An. stephensi
Juniper (J. communis) essential oil 20% oil solution An. stephensi
Cajeput (M. leucadendron) essential oil 20% oil solution An. stephensi
Soya bean (G. max) essential oil 20% oil solution An. stephensi
Rosemary (R. officinalis) essential oil 20% oil solution An. stephensi
Niaouli (M. quinquenervia) essential oil 20% oil solution An. stephensi
Olive (O. europaea) essential oil 20% oil solution An. stephensi
Tagetes (T. minuta) essential oil 20% oil solution An. stephensi
Violet (V. odorata) essential oil 20% oil solution An. stephensi
Sandalwood (S. album) essential oil 20% oil solution An. stephensi
Litsea (L. cubeba) essential oil 20% oil solution An. stephensi
Galbanum (F. galbaniflua) essential oil 20% oil solution An. stephensi
C. longa essential oil 25% An. dirus
7 < to < 8 R. mucronata oil 2 mg/cm2 An. stephensi
Thyme (T. serpyllum) essential oils 20% oil solutions An. stephensi
Peppermint oil 1 ml without dilution An. subpictus
R. mucronata oil 1 mg/cm2 An. stephensi
7 Lemon (C. limon) essential oil 20% oil solution An. stephensi
6 < to < 7 A. monophylla essential oil 50 ppm An. stephensi
rosewood (A. rosaeodora) essential oils 20% oil solution An. stephensi
myrtle (M. communis) essential oil 20% oil solution An. stephensi
peppermint (M. piperita) essential oil 20% oil solution An. stephensi
Asadollahi et al. Malar J (2019) 18:436 Page 15 of 20

Table 2 (continued)
Protection time (hours) Plant name Concentration/dose Anopheles species

6 Helichrysum (H. italicum) essential oil 20% oil solution An. stephensi
C. martinii martinii var sofia oil 1 ml without dilution An. sundaicus
Turmeric (C. longa) volatile oil 3 ml An. dirus
Citronella 3 ml An. dirus
Hairy basil oil 3 ml An. dirus
C. rotundus Linn hexane extract 10% An. stephensi
5 < to < 6 I. cairica essential oil 6% An. stephensi
Eucalyptus (E. globulus) essential oils 20% oil solution An. stephensi
Verbena (L. citriodora) essential oil 20% oil solution An. stephensi
Chamomile (C. nobile) essential oil 20% oil solution An. stephensi
C. longa essential oil 15% An. dirus
C. longa essential oil 20% An. dirus
M. charantia essential oil 6% An. stephensi
C. citratus extract 2 mg/cm2 An. arabiensis
T. procumbens essential oil 6% An. stephensI
Confertifolin essential oil 10 ppm An. stephensi
5 Frankincense (B. carteri) essential oil 20% oil solution An. stephensi
Sage (S. sclarea) essential oil 20% oil solution An. stephensi
C. longa essential oil 10% An. dirus
Confertifolin essential oil 5 ppm An. stephensi
P. tuberosa extract 2% An. stephensi
4 < to < 5 Clove oil Cream 20% An. dirus
Clove oil 20% gel An. dirus
C. citratus extract 1/5 mg/cm2 An. arabiensis
Myrtle essential oil 50% An. stephensi
I. cairica essential oil 4% An. stephensi
4 C. longa essential oil 5% An. dirus
P. tuberosa extract 1.5% An. stephensi
Stratification of potential of plant based repellents by complete protection times, up to July 2018

various beneficial effects, such as antiseptic, carminative, also supported that burning of 25 g of dried O. europaea,
antimicrobial, and antioxidant properties [70]. The 20% comparable to Amer et al. [6], has a percentage repel-
oil solution of thyme in the study conducted by Amer lency of 79.7 against Anopheles arabiensis.
et al. [6], with 100% protection against An. stephensi for
7.5 h, had a good effectiveness in preventing Anopheles Eucalyptus
mosquitoes. Nevertheless, another study [58] reported Eucalyptus is a significant short rotation pulpy
that the complete protection time of thyme at its maxi- woody plant, grown generally in tropical regions [72]. A
mum concentration (100%) is 1.7 h against Anopheles total of 5 studies examined the repellency effect of dif-
albimanus. ferent sub-species of eucalyptus. In the laboratory trial
by Amer et al. [6], narrow-leaved eucalyptus, lemon-
Olive (Olea europaea) scented eucalyptus, and broad-leaved eucalyptus pro-
Olive (O. europaea) is one of the most ancient cultivated tected against An. stephensi for 8 h, while Eucalyptus
fruit tree species in the Mediterranean basin which is a globulus complete protection time was reported to be
source of several phenolic compounds with important 5.5 h. Auysawasdi et al. [41] used E. globulus essential oil
properties [71]. The 20% oil solution of olive in the study at 5%, 10%, 15%, 20% and 25% concentrations against An.
conducted by Amer et al. [6], with a mean percentage of dirus. All concentrations of E. globulus provided com-
repellency (71.4%) and complete protection time against plete repellency ranging from 1.7 to 3.4 h, depending on
An. stephensi for 8 h, had a good effectiveness in prevent- the concentration applied. Eucalyptus globulus at 0.1 ml
ing An. stephensi mosquitoes. Karunamoorthi et al. [50] dose in a study [47] repelled An. dirus for 1.58 h. Besides,
Asadollahi et al. Malar J (2019) 18:436 Page 16 of 20

100 μl Eucalyptus citriodora repelled An. minimus for Nevertheless, Seyoum et al. found that Neem extract is
0.5 h [45]. In contrast, Seyoum et al. found that lemon not affective against An. gambiae [54].
eucalyptus extract is not affective against An. gambiae
[54]. Rosemary (Rosmarinus officinalis)
Rosemary is an evergreen aromatic shrub with a Medi-
Myrtle (Myrtus communis) terranean origin, which belongs to Lamiaceae (Labiatae)
Myrtle is a member of the Myrtaceae family which is family [77]. In 2 studies, repellency effectiveness of rose-
botanically linked to eucalyptus [73]. In 2 studies, repel- mary was reported. The 20% oil solution of rosemary in
lency effectiveness of myrtle was investigated. The 20% the study conducted by Amer et al. [6], with 100% protec-
oil solution of myrtle in the study conducted by Amer tion against An. stephensi for 8 h, had a good effective-
et al. [6], with mean percentage repellency of 42.8% and ness in preventing Anopheles mosquitoes. Govindarajan
complete protection time against An. stephensi for 6.5 h, et al. [22] also supported that rosemary at 1, 2.5 and
had a good effectiveness in preventing Anopheles mos- 5 mg/cm2 concentrations completely repels An. subpictus
quitoes. Tavassoli et al. [62] also supported that myrtle at for 1, 1, and 1.5 h, respectively.
50% concentration repels An. stephensi for 4.36 h.
Clove (Syzygium aromaticum)
Basil Clove is a naturally occurring spice which has been
Basil is an annual plant of the Ocimum genus, which shown to possess anti-bacterial, anti-oxidant, anti-
belongs to the Lamiaceae family and is used in traditional pyretic, anti-candidal, and aphrodisiac activities [78].
medicine in many parts of the world [74]. In 6 studies, The repellency effect of clove against different species
repellency effectiveness of basil against different Anoph- of Anopheles was investigated in 6 studies. In the study
eles species was investigated. In the laboratory trial by by Phasomkusolsil et al. [42], clove at 0.02, 0.10 and
Amer et al. [6], 20% oil solution of basil essential oil, with 0.21 mg/cm2 with a dose-dependent trend, showed 82%,
mean percentage repellency of 66.7%, had 100% protec- 92%, and 98% repellency against An. dirus. Barnard et al.
tive impact against An. stephensi for 3.5 h. Phasomku- [58] used clove essential oil at 25%, 50%, 75%, and 100%
solsil et al. [42] used basil essential oil at 0.02, 0.10, and concentrations against An. albimanus and found that all
0.21 mg/cm2 concentrations against An. dirus. The per- concentrations of clove provided complete repellency
centage repellency was dose–response and was reported ranging from 1.25 to 3.55 h, depending on the concentra-
to be 66%, 74% and 96%, respectively. Basil at 0.1 ml dose tion applied. Consistently, clove at 10%, 50%, and 100%
in other studies [47, 61] repelled Anopheles for 1.5 h and concentrations, with a dose-dependent trend, showed
0.75 h, whereas, Tawatsin et al. [44] found that hairy basil 1.33, 2.66, and 3.5 h complete repellency against An. dirus
oil provides 100% protection against An. dirus for 6 h. In [43]. Anopheles dirus was repelled by clove for 1 h in lab-
contrast, in the study by Seyoum et al. [54], no remark- oratory conditions in Thailand [47]. Another study [45]
able repellency effect against An. gambiae was identified. reported that clove repels An. minimus for 2 h. Moreover,
20% gel of clove protected against An. dirus for 4.5 h [46].
Tagetes (Tagetes minuta) All these findings support that clove can be a considered
Tagetes minuta is a very important member of Tagetes as moderate repellent.
genus belonging to Asteraceae family [75]. In 2 studies,
repellency effectiveness of tagetes was explored. The 20% Orange oil (Citrus sinensis)
oil solution of T. minuta in the study conducted by Amer Orange is a plant member of the Citrus genus and mostly
et al. [6], with complete protection time for 8 h, had a cultivated in subtropical areas [79]. The repellency effect
good effectiveness in preventing against An. stephensi. In of orange against different species of Anopheles was
contrast, Seyoum et al. found that tagetes extract is not investigated in 4 studies. In the study by Murugan et al.
affective against An. gambiae [54]. [27], orange extract at 50, 150 and 250, 350, and 450 ppm
showed 0, 0.5, 0.5, 1.5 and 2 h complete protection time
Neem (Azadirachta indica) repellency (100%) against An. stephensi, respectively.
Neem is a versatile tree broadly grown in tropical areas While, in another study [45], it repelled An. minimus for
of India [76]. The repellency effect of Neem against dif- 0.83 h. Similarly, Sritabutra et al. [47] showed that orange
ferent species of Anopheles was investigated in 2 stud- repels An. dirus for 0.83 h. Phasomkusolsi et al. [42] also
ies. The 20% Neem oil in a field trial conducted by Amer found that orange at 0.02, 0.10, and 0.21 mg/cm2, with a
et al. [6], with mean percentage repellency 71% had a dose-dependent trend, has 44%, 54%, and 84% repellency
complete protection time for 3 h against An. arabiensis. against An. dirus, respectively.
Asadollahi et al. Malar J (2019) 18:436 Page 17 of 20

Turmeric (C. longa) terpine [85], but contrasts with the inhibitory influence
The medicinal plant turmeric, which is a perennial herb, of DEET [86]. Although the protection time of citron-
and a member of Zingiberacae family, is commonly used ella oil is shorter than that of DEET. Citronella oil could
as a spice in human food [80]. In 3 studies, repellency provide sufficient protection time against mosquitoes.
effectiveness of turmeric was examined. Auysawasdi et al. For other plants, the underlying mechanism remains to
[41] used turmeric essential oil at 5%, 10%, 15%, 20%, and be elucidated. Possibly, the most important aspect in
25% concentrations against An. dirus. All concentrations increasing the permanence of such repellents that are
of turmeric, with a dose–response manner, provided effective but volatile is improving formulations of plant
complete repellency ranging from 4 to 8 h, depending on extracts to elevate their longevity through the develop-
the concentration applied. Other studies also found that ment of nanoemulsions, improved formulations, and
turmeric oil repels An. dirus for 6 h [44] and An. minimus fixatives. While alternative uses such as excite-repellency
[45] for 1 h. and spatial activity have also been examined [87].
Some caution is important when interpreting the find-
Discussion ings. First, a poorly inspected confounding aspect is the
A high level of insecticide resistance has made because effect of sweating on the effectiveness and protection
of the chemical control of the pests and vectors. To over- time of repellents, which are approximately all water-sol-
come this problem, it is essential to research for alter- uble, and this might limits the comparability of repellents.
native approaches to vector control. The field of herbal Second, in field trial studies, the number of human vol-
repellents is extremely fertile as people demand mos- unteers as well as the season during which the trial had
quitoes’ repellents that are safe, pleasant to usage and been performed differed among the included studies. Cli-
ecologically maintainable. As cost is a significant fac- mate could also affect mosquito behaviour and the vari-
tor, examination of the use of local florae as repellents is ance is controlled by standardizing humidity temperature
highly suggested. Essential oils and extracts of plants are in ‘arm-in-cage’ trials; however, these parameters are not
emerging as potential agents for Anopheles spp. control, always similar in different trials or conform to the mos-
with easy-to-administer, low-cost, and risk-free proper- quito environment standards. Third, it should be high-
ties. In the present systematic review the highest repel- lighted that some plant compounds are irritating to the
lency effect against Anopheles mosquitoes was found skin and/or highly toxic to mammals, and natural does
from L. sinense extract, followed by citronella, pine, D. not equate to safe. Thus, plants with potential repellency
sissoo, peppermint and R. mucronata oils with complete properties should be tested for their possible unpleas-
protection time ranging from 9.1 to 11.5 h. Essential oils ant side effects before introducing as alternative prod-
from plants such as lavender, camphor, catnip, geranium, ucts. Fourth, some studies have shown that formulation
jasmine, broad-leaved eucalyptus, lemongrass, lemon- play a significant role in the effectiveness of a repellents
scented eucalyptus, amyris, narrow-leaved eucalyptus, [88]. However, studies have focused more on the search
carotin, cedarwood, chamomile, cinnamon oil, juniper, for active compounds than on optimal formulations
cajeput, soya bean, rosemary, niaouli, olive, tagetes, vio- [8, 29]. Moreover, in this study, many investigated cita-
let, sandalwood, litsea, galbanum, and C. longa also tions showed the effectiveness of plant repellents against
showed good repellency with 8 h complete repellency Anopheles spp. mosquitoes. However, when focusing on
against different species of Anopheles genus. Anopheles subspecies, there were only a few publications
The exact mechanism of action of these plants in pre- indicating the efficacy of each plant, which resulted in a
venting Anopheles spp. bites has not yet been completely difficulty to reach a robust conclusion regarding the best
clarified. For citronella, as one of the most explored plant herbal candidates to develop new commercial repellents.
for repellency effect against various mosquitoes, it is This is another area for additional research. Finally,
reported that active compounds in citronella extract for current studies are difficult to be compared and the
repelling mosquitoes are eugenol, eucalyptol, camphor, repellency effectiveness may also differ among subspe-
linalool, citral, and citronellal [81]. Some data proposes cies. Unfortunately, a few studies aimed to compare
that these agents interfere with olfactory receptors of repellency efficacy of a special plant on subspecies of
mosquitoes [82]. A recent study revealed that An. gam- Anopheles. The heterogeneity in the results of the pre-
biae is able to detect citronellal molecules by olfactory vious studies might be stem from differences in com-
neurons in the antenna controlled by the TRPA1 gene, pound concentrations, application dosages, mosquito
activated directly by the molecule with high potency species, formulations and the assessment method
[83, 84]. Another study found that citronellal directly of repellency, as in some trials the protection time
activates channels of cation [83], which is similar to the until mosquitoes landed was recorded, whereas in the
excite-repellent impact of pyrethrin another plant based majority of studies the time until mosquitoes bite was
Asadollahi et al. Malar J (2019) 18:436 Page 18 of 20

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