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. 2019 Dec 21;18:436. doi: 10.1186/s12936-019-3064-8

Effectiveness of plant-based repellents against different Anopheles species: a systematic review

Amin Asadollahi 1, Mehdi Khoobdel 2,✉, Alireza Zahraei-Ramazani 1,✉, Sahar Azarmi 1, Sayed Hussain Mosawi 3
PMCID: PMC6925501  PMID: 31864359

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 development 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 repellency 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 protection 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 complete 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 development 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

Mosquito-transmitted diseases remain a main source of illness and death [1]. Despite decades of malaria control efforts, malaria continues to be a major worldwide public health issue with 3.3 billion persons at risk in 106 countries and territories in the tropical and subtropical areas [2]. It is one of the significant reasons for maternal and childhood morbidity and mortality, including low birth weight, stillbirths, and early infant death in sub-Saharan Africa [3]. Among 500 species of Anopheles mosquitoes known globally, more than 50 species can transmit malaria from the 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 available [5]. Thus, protection from mosquito bites is one of the best approaches to reduce the disease incidence.

The use of repellents to protect people from bites of mosquitoes previously has been acknowledged as part of an overall integrated insect-borne disease control programme [6]. Most commercial repellents are produced by using chemical components such as N, N-diethyl-meta-toluamide (DEET), Allethrin, N, N-diethyl mendelic acid amide, and Dimethyl phthalate [1]. It has been identified that chemical repellents are not safe for public health and should be used with caution because of their detrimental impacts on synthetic fabric and plastic as well as toxic reactions, such as allergy, dermatitis, and cardiovascular and neurological side effects, which have been reported generally after misapplication [4]. The frequent use of synthetic repellents with chemical origin for mosquito control has disturbed natural ecosystems and resulted in the development of resistance to insecticides, resurgence in mosquito populations, and adverse impact on non-target organisms [4, 7]. Accordingly, the idea of using natural mosquito repellent products as an alternative to develop new eco-friendly repellents could be an amicable solution to scale back the undesirable effects on environment and human health.

In recent years, interest in plant-based repellents has been revived, as they contain a rich source of bioactive phytochemicals that are safe and biodegradable into non-toxic by-products, which could be screened for insecticidal activities and mosquito repellent. Many studies have reported evidence of repellant activities of plant extracts or essential oils against malaria vectors around the world. The present systematic review was performed to reveal which plant-based repellent can be relied on to provide a prolonged and predictable protection from species of Anopheles mosquitoes without causing side effects on human health.

For this systematic review, all eligible studies on the repellency effects of plant-based repellants against Anopheles spp. published up to July 2018 were systematically searched through electronic databases PubMed, MEDLINE, Web of Science, Literature retrieval System of the Armed Forces Pest Management Board, Scopus and Google Scholar using the following Medical Subject Headings (Mesh) and keywords: (((Plant [Title/Abstract]) OR Plants [Title/Abstract]) OR herbal [Title/Abstract]) AND (botanical [Title/Abstract]) AND ((extract [Title/Abstract]) OR extracts [Title/Abstract]) AND ((“essential oil” [Title/Abstract]) OR “essential oils” [Title/Abstract]) AND (((((“Insect repellent” [Mesh]) OR repellents) OR repellent) OR repellence) OR repellency) AND ((“Anopheles” [Mesh]) OR “Anopheles” [Title/Abstract]). The search was limited to English publications. In addition, a manual search was conducted to identify further pertinent articles using references from retrieved studies.

Eligibility criteria

Studies were included in the present systematic review if they met these criteria: (i) full-text publication was written in English, (ii) inspected the repellency effects of plant extracts and essential oils against malaria vectors, Anopheles spp. mosquitoes, and, (iii) reported the percentage of repellency or complete protection time. Following studies were excluded: studies exploring the repellency effect of chemical-based products, studies examining the repellency effect of animal extracts, animal studies (studies not on human subjects), articles without full texts, reviews, duplicate articles, abstracts, republished data, comments, conference papers, editorials, and studies with insufficient data. In addition, studies were excluded if the information could not be extracted. A screening of titles and abstracts followed by a full-text review was performed by two investigators. All titles and abstracts were screened by two independent investigators for eligibility. If a consensus was reached, a study was excluded or selected to full-text screening. If a consensus was not reached, another reviewer was consulted to resolve any feasible discrepancies.

Data extraction

After identifying the eligible studies, the following data were collected from each study by application of standardized data collection form to improve accuracy and critical appraisal: the first author name, country of origin, journal details, publication year, condition of study (field or laboratory), plant name, Anopheles species, concentration or dose of repellents, repellency percentage and complete protection time. All data were independently extracted by two reviewers and disagreements were solved by discussion, and if necessary, a third author was involved.

A total of 383 studies were found by the initial literature search of the databases. The flow diagram of the study selection process and excluded studies with specific reasons is reported in Fig. 1. Of the 324 excluded citations, 102 were duplicated studies; 149 were not relevant to the repellency effect of plants on Anopheles spp. after screening titles/abstracts; 11 were review publications; 8 investigated the repellency impact of chemical-based repellents or animal extracts; 7 studies were conducted on laboratory animals; 12 were abstracts, conference papers, comments, and editorials; 10 studies had not reported sufficient data regarding the percentage of repellency or complete protection time; and, 15 studies were other irrelevant studies. The primary eligibility process yielded 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 different countries, including India [7–40], Thailand [4, 5, 41–48], Ethiopia [49–52], Kenya [53–57], Germany [6], Nigeria [1], USA [58], Tanzania [59], Brazil [60], Sudan [61], Iran [62], Cameron [63] and Ivory Coast [64] were eventually included in the systematic review based on the inclusion criteria for the effect of plant-based repellents on species of Anopheles mosquitoes. The included studies were published between 1999 and 2018. Expect for 6 studies which were field trial, other studies were conducted on laboratory condition. None of the studies reported the inclusion and exclusion criteria explicitly other than specifying a healthy volunteer. Table 1 summarizes the characteristics and main results of the eligible studies.

Fig. 1.

Fig. 1

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Study selection process, up to July 2018

Table 1.

Characteristics of studies. Characteristics of studies included in the systematic review, up to July 2018

Study Year Country Study type Plant extract/(essential oil) Concentration dose Anopheles species Repellency % Protection time (hours)
Ansari et al. 2005 India Field Pine oil (Pinus) 1 ml without dilution An. culicifacies 100 11
Citronella (lemongrass oil) 1 ml without dilution An. culicifacies 100 11
Ansari et al. 2000 India Field D. sissoo oil 1 ml without dilution An. culicifacies 96.1 10.3
D. sissoo oil 1 ml without dilution An. annularis 100 11
D. sissoo oil 1 ml without dilution An. subpictus 89.7 8
Ansari et al. 2000 India Field Peppermint oil 1 ml without dilution An. culicifacies 92.3 9.6
Peppermint oil 1 ml without dilution An. annularis 100 11
Peppermint oil 1 ml without dilution An. subpictus 83.1 7.3
Amer et al. 2006 Germany Laboratory Citronella (Cymbopogon winterianus) essential oils 20% oil solutions An. stephensi 52.4 8
Rosewood (Aniba rosaeodora) essential oils 20% oil solutions An. stephensi 4.8 6.5
Lavender (Lavandula angustifolia) essential oils 20% oil solutions An. stephensi 80.9 8
Camphor (C. camphora) essential oils 20% oil solutions An. stephensi 42.8 8
Catnip (N. cataria) essential oils 20% oil solutions An. stephensi 100 8
Geranium (Pelargonium graveolens) essential oils 20% oil solutions An. stephensi 61.9 8
Thyme (T. serpyllum) essential oils 20% oil solutions An. stephensi 33.3 7.5
Eucalyptus (E. globulus) essential oils 20% oil solutions An. stephensi 28.6 5.5
Jasmine (Jasminum grandiflorum) essential oils 20% oil solutions An. stephensi 100 8
Broad-leaved eucalyptus (Eucalyptus dives) essential oils 20% oil solutions An. stephensi 38.1 8
Lemongrass (Cymbopogon citratus) essential oil 20% oil solutions An. stephensi 100 8
Lemon-scented eucalyptus (E. citriodora) essential oil 20% oil solutions An. stephensi 52.4 8
Fichtennadel (Picea excelsa) essential oil 20% oil solutions An. stephensi 19 3
Amyris (Amyris balsamifera) essential oil 20% oil solutions An. stephensi 100 8
Lemon (Citrus limon) essential oil 20% oil solutions An. stephensi 9.5 7
Narrow-leaved eucalyptus (Eucalyptus radiata) essential oil 20% oil solutions An. stephensi 42.8 8
Carotin oil (Glycina soja) essential oil 20% oil solutions An. stephensi 9.5 8
Cedarwood (Juniperus virginiana) essential oil 20% oil solutions An. stephensi 38.1 8
frankincense (Boswellia carteri) essential oil 20% oil solutions An. stephensi 19 5
Dill (Anethum graveolens) essential oil 20% oil solutions An. stephensi 71.4 3.5
Myrtle (M. communis) essential oil 20% oil solutions An. stephensi 42.8 6.5
Chamomile (Anthemis nobilis) essential oil 20% oil solutions An. stephensi 76.2 8
Cinnamon (C. zeylanicum) essential oil 20% oil solutions An. stephensi 100 8
Juniper (Juniperus communis) essential oil 20% oil solutions An. stephensi 76.2 8
Sage (Salvia sclarea) essential oil 20% oil solutions An. stephensi 19 5
Peppermint (Mentha piperita) essential oil 20% oil solutions An. stephensi 57.1 6.5
Basil (Ocimum basilicum) essential oil 20% oil solutions An. stephensi 66.7 3.5
Cajeput (Melaleuca leucadendron) essential oil 20% oil solutions An. stephensi 100 8
Soya bean (Glycina max) essential oil 20% oil solutions An. stephensi 76.2 8
Rosemary (R. officinalis) essential oil 20% oil solutions An. stephensi 100 8
Niaouli (Melaleuca quinquenervia) essential oil 20% oil solutions An. stephensi 100 8
Olive (O. europaea) essential oil 20% oil solutions An. stephensi 71.4 8
Black pepper (Piper nigrum) essential oil 20% oil solutions An. stephensi 61.9 3
Verbena (Lippia citriodora) essential oil 20% oil solutions An. stephensi 38.1 5.5
tagetes (T. minuta) essential oil 20% oil solutions An. stephensi 100 8
Violet (Viola odorata) essential oil 20% oil solutions An. stephensi 100 8
Sandalwood (Santalum album) essential oil 20% oil solutions An. stephensi 100 8
Litsea (Litsea cubeba) Essential oil 20% oil solutions An. stephensi 100 8
Helichrysum (Helichrysum italicum) essential oil 20% oil solutions An. stephensi 47.6 6
Galbanum (Ferula galbaniflua) essential oil 20% oil solutions An. stephensi 100 8
Chamomile (Chamaemelum nobile) essential oil 20% oil solutions An. stephensi 47.6 5.5
Amerasan et al. 2012 India Laboratory Cassia tora Linn methanol extract

1 mg/cm2

2.5 mg/cm2

5.0 mg/cm2

 An. stephensi

100

100

100

2

2

2.5
Abiy et al. 2015 Ethiopia Field 20% neem oil Neem and chinaberry oils were diluted to 20% using Niger seed (noog abyssinia) oil An. arabiensis 71 3
20% chinaberry oil Neem and chinaberry oils were diluted to 20% using Niger seed (noog abyssinia) oil An. arabiensis 70 1
Alayo et al. 2015 Nigeria Laboratory Cassia mimosoides petroleum ether extract Cream 0.5% w/w An. gambiae 48 –
Cream 1% w/w 88 –
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 essential Oil 10% solution An. gambiae 100 –
Baskar et al. 2018 India Laboratory Atalantia monophylla essential oil 50 ppm An. stephensi – 6.85
Govindarajan et al. 2010 India Laboratory Sida acuta Burm. F. extract 2.5 mg/cm2 An. stephensi 100 2.5
5 mg/cm2 An. stephensi 100 3
Govindarajan et al. 2011 India Laboratory Ervatamia coronaria extract

1 mg/cm2

2.5 mg/cm2

5 mg/cm2

An. stephensi

An. stephensi

An. stephensi

100

100

100

2.5

3

3.5
Caesalpinia pulcherrima extract 1 mg/cm2 An. stephensi 100 2
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

5 mg/cm2

An. subpictus

An. subpictus

100

100

2

2.5
R. officinalis L. essential oil 1 mg/cm2 An. subpictus 100 1
2.5 mg/cm2 An. subpictus 100 1
5 mg/cm2 An. subpictus 100 1.5
C. citrates Stapf. essential oil 1 mg/cm2 An. subpictus 100 1
2.5 mg/cm2 An. subpictus 100 1.5
5 mg/cm2 An. subpictus 100 2
C. zeylanicum L. essential oil 1 mg/cm2 An. subpictus 100 1
2.5 mg/cm2 An. subpictus 100 1
5 mg/cm2 An. subpictus 100 1.5
Govindarajan et al. 2016 India Laboratory Zingiber nimmonii essential oil 1 mg/cm2 An. stephensi 100 2
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) smoke Burning of 25 g of dried plant materials An. arabiensis 79.7 –
Tinjut (Ostostegia integrifolia) smoke Burning of 25 g of dried plant materials An. arabiensis 90.1 –
Wogert (Silene macroserene) smoke Burning of 25 g of dried plant materials An. arabiensis 93.6 –
Kebercho (Echinops sp.) extract Burning of 25 g of dried plant materials An. arabiensis 92.4 –
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 essential oil 1 mg/cm2 An. stephensi 100 2.5
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 essential oil 5% An. dirus 100 4
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 oil 5% An. dirus 100 1.7
10% An. dirus 100 2.3
15% An. dirus 100 3
20% An. dirus 100 3
25% An. dirus 100 3.4
Citrus aurantium essential oil 5% An. dirus 100 1.8
10% An. dirus 100 2.9
15% An. dirus 100 2.9
20% An. dirus 100 3
25% An. dirus 100 3.5
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 extract 500 mg/m2 An. gambiae 81 –
Ocimum kilimandscharicum extract 500 mg/m2 An. gambiae 73 –
Citronella 500 mg/m2 An. arabiensis 85 –
O. suave extract 500 mg/m2 An. arabiensis 89 –
O. kilimandscharicum extract 500 mg/m2 An. arabiensis 75 –
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 extract 2 mg/cm2 An. stephensi 100 3
4 mg/cm2 An. stephensi 100 3.5
6 mg/cm2 An. stephensi 100 3.5
Naine et al. 2014 India Laboratory Streptomyces sp. VITJS4 extract 1 mg/cm2 An. stephensi 100 2
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 essential oil 0.62 ppm An. stephensi 100 1
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 paniculata methanol leaf extract 1 mg/cm2 An. stephensi 100 2
3 mg/cm2 An. stephensi 100 2.5
6 mg/cm2 An. stephensi 100 3
Cassia occidentalis methanol leaf extract 1 mg/cm2 An. stephensi 100 2
3 mg/cm2 An. stephensi 100 2.5
6 mg/cm2 An. stephensi 100 2.5
Euphorbia hirta methanol leaf extract 1 mg/cm2 An. stephensi 100 2
3 mg/cm2 An. stephensi 100 2
6 mg/cm2 An. stephensi 100 2.5
Panneerselvam et al. 2012 India Laboratory Artemisia nilagirica extract 50 ppm An. stephensi 95 0.5
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 –
C. citratus oil 0.02 mg/cm2 An. dirus 76 –
0.10 mg/cm2 An. dirus 82 –
0.21 mg/cm2 An. dirus 98 –
Cymbopogon nardus oil 0.02 mg/cm2 An. dirus 92 –
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 extract 20% An. stephensi 23 –
40% An. stephensi 43 –
60% An. stephensi 58 –
80% An. stephensi 76 –
100% An. stephensi 90 –
Rajkumar et al. 2007 India Laboratory Centella asiatica essential oil 2% An. stephensi – 1
4% An. stephensi – 1.78
6% An. stephensi – 2.33
Ipomoea cairica essential oil 2% An. stephensi – 2.63
4% An. stephensi – 4.13
6% An. stephensi – 5.53
Momordica charantia essential oil 2% An. stephensi – 2.38
4% An. stephensi – 3.93
6% An. stephensi – 5.38
Psidium guajava essential oil 2% An. stephensi – 0.93
4% An. stephensi – 1.48
6% An. stephensi – 1.98
Tridax procumbens essential oil 2% An. stephensi – 2.33
4% An. stephensi – 3.78
6% An. stephensi – 5.28
Rajkumar et al. 2005 India Laboratory Solanum trilobatum extract 0.001% An. stephensi 100 1.15
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 extract 0.1% An. stephensi – 0.35
0.5% An. stephensi – 0.72
1% An. stephensi – 1.9
Seyoum et al. 2002 Kenya Semi-field Neem (A. indica) Periodic thermal expulsion An. gambiae 24.5 –
Lemon eucalyptus (Corymbia citriodora) Periodic thermal expulsion An. gambiae 74.5 –
Wild spikenard (Hyptis suaveolens) Periodic thermal expulsion An. gambiae -13.3 –
Lantana (Lantana camara) Periodic thermal expulsion An. gambiae 42.4 –
Fever tea (Lippia uckambensis) Periodic thermal expulsion An. gambiae 45.9 –
Lime basil (Ocimum americanum) Periodic thermal expulsion An. gambiae 43.1 –
Rican blue basil (O. kilimandscharicum) Periodic thermal expulsion An. gambiae 52.0 –
Tree basil (O. suave) Periodic thermal expulsion An. gambiae 53.1 –
Khaki weed (T. minuta) Placing branches or whole plants inside houses An. gambiae 54.8 –
Sanghong et al. 2015 Thailand Laboratory L. sinense ethanolic preparations 25% An. minimus – 11.5
Das et al. 2003 India Laboratory Cymbopogan martinii martinii var sofia oil 1 ml without dilution An. sundaicus 98 6
Nour et al. 2009 Sudan Laboratory Basil (O. basilicum L.) essential oil 0.1 ml 100 1.5
Trongtokit et al. 2005 Thailand Laboratory C. nardus essential oil 10% An. dirus – 0.66
50% – 0.5
100% – 1.16
P. cablin essential oil 10% An. dirus – 1.33
50% – 2
100% – 2.83
Mullilam (Zanthoxylum limonella) essential oil 10% An. dirus – 1
50% – 2.16
100% – 3.16
Clove (Syzygium aromaticum) essential oil 10% An. dirus – 1.33
50% – 2.66
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) volatile oil 3 ml An. dirus 100 6
Citronella 3 ml An. dirus 100 6
Hairy basil oil 3 ml An. dirus 100 6
Singh et al. 2005 India Laboratory Cyperus rotundus Linn hexane extract 2.50% An. stephensi 95 –
5% An. stephensi 99 –
10% An. stephensi 100 6
Mayeku et al. 2013 Kenya laboratory Conyza newii essential oil 0.01 g/ml An. gambiae 38 –
0.1 g/ml An. gambiae 68 –
1 g/ml An. gambiae 100 –
Phasomkusolsil et al. 2009 Thailand Laboratory Phlai (Z. cassumunar) oil 100 μl An. minimus – 2
Turmeric (C. longa) oil 100 μl An. minimus – 1
Mah-Khwuaen (Z. limonella) oil 100 μl An. minimus – 0.66
Citronella grass (C. nardus) oil 100 μl An. minimus – 2.16
Orange oil (Citrus sinensis) oil 100 μl An. minimus – 0.83
Eucalyptus (E. citriodora) oil 100 μl An. minimus – 0.5
Clove (S. aromaticum) oil 100 μl An. minimus – 2
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. globules) essencial oil 0.1 ml An. dirus – 1.58
Peppermint (M. piperita) essencial oil 0.1 ml An. dirus – 1.08
Garlic (A. sativum) essencial oil 0.1 ml An. dirus – 0.68
Orange (C. sinensis) essencial oil 0.1 ml An. dirus – 0.83
Citronella grass (C. nardus) essencial oil 0.1 ml An. dirus – 0.8
Lemongrass (C. citratus) essencial oil 0.1 ml An. dirus – 1.63
Clove (S. aromaticum) essencial oil 0.1 ml An. dirus – 1
Sweet basil (O. basilicum) essencial oil 0.1 ml An. dirus – 0.75
Tavassoli et al. 2001 iran Laboratory Marigold (Calendula officinalis) essential oil 50% An. stephensi – 2.15
Myrtle essential oil 50% An. stephensi – 4.36
Younoussa et al. 2016 Cameroon Laboratory Annona senegalensis leaf extract 4.0 mg/cm2 An. gambiae – 0.5
8.0 mg/cm2 An. gambiae – 1
12.0 mg/cm2 An. gambiae – 1.5
Boswellia dalzielii leaf extract 4.0 mg/cm2 An. gambiae 46
8.0 mg/cm2 An. gambiae – 0.5
12.0 mg/cm2 An. gambiae – 1
Govindarajan et al. 2011 India Laboratory Coccinia indica extract 1 mg/cm2 An. stephensi 100 3
2.5 mg/cm2 An. stephensi 100 3
5 mg/cm2 An. stephensi 100 3.5
Govindarajan et al. 2012 India Laboratory Cardiospermum halicacabum oil 1 mg/cm2 An. stephensi 100 2
2.5 mg/cm2 An. stephensi 100 2.5
5 mg/cm2 An. stephensi 100 3
Govindarajan et al. 2014 India Laboratory Asparagus racemosus crude extract 1 mg/cm2 An. stephensi 100 2.5
2 mg/cm2 An. stephensi 100 2.5
5 mg/cm2 An. stephensi 100 3
Govindarajan et al. 2015 India Laboratory Delonix elata crude extract 1 mg/cm2 An. stephensi 100 2.5
2.5 mg/cm2 An. stephensi 100 3
5 mg/cm2 An. stephensi 100 3.5
Innocent et al. 2014 Kenya Laboratory Uvariodendron gorgonis essential oil 0.01 w/v An. gambiae 29 –
0.1 w/v An. gambiae 48 –
1 w/v An. gambiae 57 –
10 w/v An. gambiae 64 –
Clausena anisata essential oil 0.01 w/v An. gambiae 13 –
0.1 w/v An. gambiae 21 –
1 w/v An. gambiae 42 –
10 w/v An. gambiae 56 –
Lantana vibunoides essential oil 0.01 w/v An. gambiae 26 –
0.1 w/v An. gambiae 46 –
1 w/v An. gambiae 54 –
10 w/v An. gambiae 62 –
Kumar et al. 2012 India Laboratory Sargassum wightii Greville methanolic extract 2 mg/l An. sundaicus 26 –
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 et al. 2014 India Laboratory O. canum extract 0.49 mg/l An. stephensi 63 –
0.99 mg/l An. stephensi 77 –
1.99 mg/l An. stephensi 86 –
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Effectiveness of plant-based products against Anopheles spp.

Potential plant-based repellents stratified by protection time with at least 4 h protection time are reported in Table 2. The highest repellency effect was identified from Ligusticum sinense extract, followed by citronella, pine, Dalbergia sissoo, peppermint and Rhizophora mucronata oils with complete protection time ranging from 9.1 to 11.5 h. Ethanolic 25% extract of L. sinense was able to completely repel Anopheles minimus for 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 genus. Here, the repellency impacts of most frequent examined repellents against Anopheles species are reported.

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)

Citronella (lemongrass oil)

D. sissoo oil

Peppermint oil

1 ml without dilution

1 ml without dilution

1 ml without dilution

1 ml without dilution

An. culicifacies

An. culicifacies

An. annularis

An. annularis
8 < to < 10

D. sissoo oil

Peppermint oil

R. mucronata oil

R. mucronata oil

1 ml without dilution

1 ml without dilution

4 mg/cm2

3 mg/cm2

An. culicifacies

An. culicifacies

An. stephensi

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
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

P. tuberosa extract

5 ppm

2%

An. stephensi

An. stephensi
4 < to < 5

Clove oil

Clove oil

C. citratus extract

Myrtle essential oil

I. cairica essential oil

Cream 20%

20% gel

1/5 mg/cm2

50%

4%

An. dirus

An. dirus

An. arabiensis

An. stephensi

An. stephensi
4 C. longa essential oil 5% An. dirus
P. tuberosa extract 1.5% An. stephensi
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Stratification of potential of plant based repellents by complete protection times, up to July 2018

Citronella

The repellency effect of citronella was investigated in several studies. Citronella is an essential oil extracted from the stems and leaves of different species of lemongrass (Cymbopogon spp.) [65]. Ansari et al. [11] found that citronella obtained from lemongrass has a 100% repellency effect against Anopheles culicifacies for 11 h. Amer et al. [6] and Tawatsin et al. [44] also reported that citronella could repel Anopheles stephensi and Anopheles dirus for 8 and 6 h, respectively. Moreover, 100 μl and 0.1 ml of citronella grass essential oil showed 2.16 and 0.8 h complete protection time against An. minimus [45] and An. dirus [47], respectively. The percentage repellency of citronella in other studies. [6, 52, 59], depending on the concentration of extracts and Anopheles species, was reported to be 52 to 85%.

Peppermint

Peppermint is a hybrid mint from cross-breeding spearmint (Mentha spicata) and water mint (Mentha aquatica), which contains biologically active constituents and has high menthone, menthol and methyl esters. The plant, indigenous to Europe, is now widespread in cultivation worldwide [66]. The effect of peppermint on Anopheles was explored in 3 studies. Ansari et al. [12] in a field trial revealed that 1 ml peppermint oil without dilution completely repels Anopheles annularis, An. culicifacies and Anopheles subpictus for 11, 9.6 and 7.3 h, respectively and the corresponding percentage repellency were 100%, 92.3% and 83.1%. In another study [6], 20% oil solutions of peppermint had 57% repellency and complete protection time for 6.5 h against An. stephensi. The study by Sritabutra et al. [47] also found that 0.1 ml of peppermint essential oil protect against An. dirus for 1.08 h.

Cinnamomum

Cinnamomum is a genus in the Laurel family, Lauraceae, several of which are investigated for their antibacterial activity by means of essential oils from bark and leaves [67]. Amer et al. [6] reported that 20% oil solutions of both camphor (Cinnamomum camphora) and cinnamon (Cinnamomum zeylanicum) had 100% repellency affect against An. stephensi. While, in the study conducted by Govindarajan et al. [22], C. zeylanicum at 1 mg/cm2 showed 1 h protection against An. subpictus.

Catnip (Nepeta cataria)

Catnip is a perennial plant that belongs to the mint family, Labiatae. This herb is spread from central Europe to central Asia and the Iranian plateaus [68]. The 20% 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 mosquitoes. Nevertheless, Birkett et al. [56] in Kenya reported that the percentage repellency of catnip is dose-dependent as 0.01 mg, 0.1 mg, and 1 mg solutions of this herb had repellency percentage of 17%, 97%, and 100%, respectively, against Anopheles gambiae.

Thyme (Thymus serpyllum)

Thyme is one of nine species belonging to T. serpyllum, a perennial aromatic plant of the Mediterranean flora [69]. Thymus species have been reported to possess various beneficial effects, such as antiseptic, carminative, antimicrobial, and antioxidant properties [70]. The 20% oil solution of thyme in the study conducted by Amer et al. [6], with 100% protection against An. stephensi for 7.5 h, had a good effectiveness in preventing Anopheles mosquitoes. Nevertheless, another study [58] reported that the complete protection time of thyme at its maximum concentration (100%) is 1.7 h against Anopheles albimanus.

Olive (Olea europaea)

Olive (O. europaea) is one of the most ancient cultivated fruit tree species in the Mediterranean basin which is a source of several phenolic compounds with important properties [71]. The 20% oil solution of olive in the study conducted by Amer et al. [6], with a mean percentage of repellency (71.4%) and complete protection time against An. stephensi for 8 h, had a good effectiveness in preventing An. stephensi mosquitoes. Karunamoorthi et al. [50] also supported that burning of 25 g of dried O. europaea, comparable to Amer et al. [6], has a percentage repellency of 79.7 against Anopheles arabiensis.

Eucalyptus

Eucalyptus is a significant short rotation pulpy woody plant, grown generally in tropical regions [72]. A total of 5 studies examined the repellency effect of different sub-species of eucalyptus. In the laboratory trial by Amer et al. [6], narrow-leaved eucalyptus, lemon-scented eucalyptus, and broad-leaved eucalyptus protected against An. stephensi for 8 h, while Eucalyptus globulus complete protection time was reported to be 5.5 h. Auysawasdi et al. [41] used E. globulus essential oil at 5%, 10%, 15%, 20% and 25% concentrations against An. dirus. All concentrations of E. globulus provided complete repellency ranging from 1.7 to 3.4 h, depending on the concentration applied. Eucalyptus globulus at 0.1 ml dose in a study [47] repelled An. dirus for 1.58 h. Besides, 100 μl Eucalyptus citriodora repelled An. minimus for 0.5 h [45]. In contrast, Seyoum et al. found that lemon eucalyptus extract is not affective against An. gambiae [54].

Myrtle (Myrtus communis)

Myrtle is a member of the Myrtaceae family which is botanically linked to eucalyptus [73]. In 2 studies, repellency effectiveness of myrtle was investigated. The 20% oil solution of myrtle in the study conducted by Amer et al. [6], with mean percentage repellency of 42.8% and complete protection time against An. stephensi for 6.5 h, had a good effectiveness in preventing Anopheles mosquitoes. Tavassoli et al. [62] also supported that myrtle at 50% concentration repels An. stephensi for 4.36 h.

Basil

Basil is an annual plant of the Ocimum genus, which belongs to the Lamiaceae family and is used in traditional medicine in many parts of the world [74]. In 6 studies, repellency effectiveness of basil against different Anopheles species was investigated. In the laboratory trial by Amer et al. [6], 20% oil solution of basil essential oil, with mean percentage repellency of 66.7%, had 100% protective impact against An. stephensi for 3.5 h. Phasomkusolsil et al. [42] used basil essential oil at 0.02, 0.10, and 0.21 mg/cm2 concentrations against An. dirus. The percentage repellency was dose–response and was reported to be 66%, 74% and 96%, respectively. Basil at 0.1 ml dose in other studies [47, 61] repelled Anopheles for 1.5 h and 0.75 h, whereas, Tawatsin et al. [44] found that hairy basil oil provides 100% protection against An. dirus for 6 h. In contrast, in the study by Seyoum et al. [54], no remarkable repellency effect against An. gambiae was identified.

Tagetes (Tagetes minuta)

Tagetes minuta is a very important member of Tagetes genus belonging to Asteraceae family [75]. In 2 studies, repellency effectiveness of tagetes was explored. The 20% oil solution of T. minuta in the study conducted by Amer et al. [6], with complete protection time for 8 h, had a good effectiveness in preventing against An. stephensi. In contrast, Seyoum et al. found that tagetes extract is not affective against An. gambiae [54].

Neem (Azadirachta indica)

Neem is a versatile tree broadly grown in tropical areas of India [76]. The repellency effect of Neem against different species of Anopheles was investigated in 2 studies. The 20% Neem oil in a field trial conducted by Amer et al. [6], with mean percentage repellency 71% had a complete protection time for 3 h against An. arabiensis. Nevertheless, Seyoum et al. found that Neem extract is not affective against An. gambiae [54].

Rosemary (Rosmarinus officinalis)

Rosemary is an evergreen aromatic shrub with a Mediterranean origin, which belongs to Lamiaceae (Labiatae) family [77]. In 2 studies, repellency effectiveness of rosemary was reported. The 20% oil solution of rosemary in the study conducted by Amer et al. [6], with 100% protection against An. stephensi for 8 h, had a good effectiveness in preventing Anopheles mosquitoes. Govindarajan et al. [22] also supported that rosemary at 1, 2.5 and 5 mg/cm2 concentrations completely repels An. subpictus for 1, 1, and 1.5 h, respectively.

Clove (Syzygium aromaticum)

Clove is a naturally occurring spice which has been shown to possess anti-bacterial, anti-oxidant, anti-pyretic, anti-candidal, and aphrodisiac activities [78]. The repellency effect of clove against different species of Anopheles was investigated in 6 studies. In the study by Phasomkusolsil et al. [42], clove at 0.02, 0.10 and 0.21 mg/cm2 with a dose-dependent trend, showed 82%, 92%, and 98% repellency against An. dirus. Barnard et al. [58] used clove essential oil at 25%, 50%, 75%, and 100% concentrations against An. albimanus and found that all concentrations of clove provided complete repellency ranging from 1.25 to 3.55 h, depending on the concentration applied. Consistently, clove at 10%, 50%, and 100% concentrations, with a dose-dependent trend, showed 1.33, 2.66, and 3.5 h complete repellency against An. dirus [43]. Anopheles dirus was repelled by clove for 1 h in laboratory conditions in Thailand [47]. Another study [45] reported that clove repels An. minimus for 2 h. Moreover, 20% gel of clove protected against An. dirus for 4.5 h [46]. All these findings support that clove can be a considered as moderate repellent.

Orange oil (Citrus sinensis)

Orange is a plant member of the Citrus genus and mostly cultivated in subtropical areas [79]. The repellency effect of orange against different species of Anopheles was investigated in 4 studies. In the study by Murugan et al. [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 repellency (100%) against An. stephensi, respectively. While, in another study [45], it repelled An. minimus for 0.83 h. Similarly, Sritabutra et al. [47] showed that orange repels An. dirus for 0.83 h. Phasomkusolsi et al. [42] also found that orange at 0.02, 0.10, and 0.21 mg/cm2, with a dose-dependent trend, has 44%, 54%, and 84% repellency against An. dirus, respectively.

Turmeric (C. longa)

The medicinal plant turmeric, which is a perennial herb, and a member of Zingiberacae family, is commonly used as a spice in human food [80]. In 3 studies, repellency effectiveness of turmeric was examined. Auysawasdi et al. [41] used turmeric essential oil at 5%, 10%, 15%, 20%, and 25% concentrations against An. dirus. All concentrations of turmeric, with a dose–response manner, provided complete repellency ranging from 4 to 8 h, depending on the concentration applied. Other studies also found that turmeric oil repels An. dirus for 6 h [44] and An. minimus [45] for 1 h.

Discussion

A high level of insecticide resistance has made because of the chemical control of the pests and vectors. To overcome this problem, it is essential to research for alternative approaches to vector control. The field of herbal repellents is extremely fertile as people demand mosquitoes’ repellents that are safe, pleasant to usage and ecologically maintainable. As cost is a significant factor, examination of the use of local florae as repellents is highly suggested. Essential oils and extracts of plants are emerging as potential agents for Anopheles spp. control, with easy-to-administer, low-cost, and risk-free properties. In the present systematic review the highest repellency effect against Anopheles mosquitoes was found from L. sinense extract, followed by citronella, pine, D. sissoo, peppermint and R. mucronata oils with complete protection time ranging from 9.1 to 11.5 h. 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 C. longa also showed good repellency with 8 h complete repellency against different species of Anopheles genus.

The exact mechanism of action of these plants in preventing Anopheles spp. bites has not yet been completely clarified. For citronella, as one of the most explored plant for repellency effect against various mosquitoes, it is reported that active compounds in citronella extract for repelling mosquitoes are eugenol, eucalyptol, camphor, linalool, citral, and citronellal [81]. Some data proposes that these agents interfere with olfactory receptors of mosquitoes [82]. A recent study revealed that An. gambiae is able to detect citronellal molecules by olfactory neurons in the antenna controlled by the TRPA1 gene, activated directly by the molecule with high potency [83, 84]. Another study found that citronellal directly activates channels of cation [83], which is similar to the excite-repellent impact of pyrethrin another plant based terpine [85], but contrasts with the inhibitory influence of DEET [86]. Although the protection time of citronella oil is shorter than that of DEET. Citronella oil could provide sufficient protection time against mosquitoes. For other plants, the underlying mechanism remains to be elucidated. Possibly, the most important aspect in increasing the permanence of such repellents that are effective but volatile is improving formulations of plant extracts to elevate their longevity through the development of nanoemulsions, improved formulations, and fixatives. While alternative uses such as excite-repellency and spatial activity have also been examined [87].

Some caution is important when interpreting the findings. First, a poorly inspected confounding aspect is the effect of sweating on the effectiveness and protection time of repellents, which are approximately all water-soluble, and this might limits the comparability of repellents. Second, in field trial studies, the number of human volunteers as well as the season during which the trial had been performed differed among the included studies. Climate could also affect mosquito behaviour and the variance is controlled by standardizing humidity temperature in ‘arm-in-cage’ trials; however, these parameters are not always similar in different trials or conform to the mosquito environment standards. Third, it should be highlighted that some plant compounds are irritating to the skin and/or highly toxic to mammals, and natural does not equate to safe. Thus, plants with potential repellency properties should be tested for their possible unpleasant side effects before introducing as alternative products. Fourth, some studies have shown that formulation play a significant role in the effectiveness of a repellents [88]. However, studies have focused more on the search for active compounds than on optimal formulations [8, 29]. Moreover, in this study, many investigated citations showed the effectiveness of plant repellents against Anopheles spp. mosquitoes. However, when focusing on Anopheles subspecies, there were only a few publications indicating the efficacy of each plant, which resulted in a difficulty to reach a robust conclusion regarding the best herbal candidates to develop new commercial repellents.

This is another area for additional research. Finally, current studies are difficult to be compared and the repellency effectiveness may also differ among subspecies. Unfortunately, a few studies aimed to compare repellency efficacy of a special plant on subspecies of Anopheles. The heterogeneity in the results of the previous studies might be stem from differences in compound concentrations, application dosages, mosquito species, formulations and the assessment method of repellency, as in some trials the protection time until mosquitoes landed was recorded, whereas in the majority of studies the time until mosquitoes bite was considered. Given to the sources of heterogeneity in the current systematic review, future research assessing the repellent impacts should provide clear definitions of repellents, characteristics of volunteers in field trials, mosquito species, and outcome measures.

Conclusion

The results of this study showed that some plants essential oils and extracts have significant repellent activity against Anopheles spp. mosquitoes. The studies in the last two decades have focused on the search for new natural repellents and some plants displayed good repellent activities, but few natural products have been developed so far [88, 89]. This review calls for the attention of entomologists and people in the field of mosquito-transmitted diseases for understanding the value and potential position of the plant-derived repellents and their role in disease control.

Acknowledgements

Not applicable.

Abbreviation

DEET

N, N-diethyl-meta-toluamide

Authors’ contributions

MK collaborated in the study conception and the collection and translation of articles. AA performed collecting of articles and writing the manuscript. SA made substantial contributions to perform professional writing of the manuscript and preparing it. SHM assisted in translation, writing and elimination of technical errors. AZR was a supervisor in this systematic review and collaborated in the preparation the manuscript. All authors read and approved the final manuscript.

Funding

None.

Availability of data and materials

All data generated or analysed during this study are included in this published article.

Ethics approval and consent to participate

Not applicable.

Consent for publication

Not applicable.

Competing interests

The authors declare that they have no competing interests.

Footnotes

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Contributor Information

Mehdi Khoobdel, Email: khoobdel@yahoo.com.

Alireza Zahraei-Ramazani, Email: alirezazahraei@yahoo.com.

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