Iran Red Crescent Med J. 2016 February;18(2): e22361. doi: 10.5812/ircmj.22361 Review Article Published online 2016 February 13.

An Evidence-Based Review on Medicinal Used as Insecticide and Insect Repellent in Traditional Iranian Medicine

1,2 3 Mina Cheraghi Niroumand, Mohammad Hosein Farzaei, Elahe Elahe Karimpour-Raz- 2 1,4 1,2,4 2,4,5 kenari, Gholamreza Amin, Mahnaz Khanavi, Tahmineh Akbarzadeh, and Moham- 1,2,4,* mad Reza Shams-Ardekani

1Department of Traditional Pharmacy, Faculty of , Tehran University of Medical Sciences, Tehran, IR Iran 2Persian Medicine and Pharmacy Research Center, Tehran University of Medical Sciences, Tehran, IR Iran 3Pharmaceutical Sciences Research Center, Kermanshah University of Medical Sciences, Kermanshah, IR Iran 4Department of Pharmacognosy, Faculty of Pharmacy, Tehran University of Medical Sciences, Tehran, IR Iran 5Department of Medicinal Chemistry, Faculty of Pharmacy, Tehran University of Medical Sciences, Tehran, IR Iran *Corresponding Author : Mohammad Reza Shams-Ardekani, Persian Medicine and Pharmacy Research Center, Tehran University of Medical Sciences, Tehran, IR Iran. Tel/Fax: +98-9123443344, E-mail: [email protected] Received ; Revised ; Accepted 2014 August 5 2014 September 2 2014 September 28.

Abstract Context: Insects can be the cause of major ecological problems; they can transmit microbes and parasites that affect humans, and damage food crops, , and homes. The total economic cost of insect-related damage and disease is immeasurable. In traditional Iranian medicine (TIM), several medicinal plants have been identified as insecticides or insect repellents, but many of them are still unknown. Therefore, the aim of this study was to review the insecticidal or insect repellent activity of certain medicinal plants described in TIM. Evidence Acquisition: Information about medicinal plants proposed as insecticides and insect repellents in the TIM was collected from the TIM literature, and searched in modern medical databases to find studies that confirmed their efficacy. Results: Allium sativum Artemisia Modern investigations have supported the claims of the insecticidal activity of several plants, including , absinthium Citrullus colocynthis nobilis pulegium communis oleander Ocimum basilicum Origanum , , , , , , , and majorana Iris florentina Malva sylvestris . However, in the cases of plants like and , there is not enough evidence in modern medicine to prove their effectiveness with regard to their insecticidal and insect repellent activities. Conclusions: This study confirmed the Iranian traditional medicine claims of the insecticidal and insect repellent activity of certain plants. Further pharmacological and clinical studies are recommended to evaluate the overall efficacy and possible mechanisms underlying these . Keywords: Medicinal Plants, Insecticide, Insect Repellent, Traditional Medicine

1. Context

Insects have evolved into over one-million named source for insecticides is botanical, which can provide a species that occupy fundamental places in the world’s simple and sustainable method of insect control (2). ecosystems. However, some insects carry parasites and Herbal medicines have been used for thousands of microbes that affect humans through various diseases, years as sources of bioactive and therapeutic substances including malaria, Chagas’ disease, Lyme disease, bubon- with industrial and agricultural purposes (3, 4). Medici- ic plague, and dengue fever. They can also affect animals nal plants, and their derivatives or , have been and damage food crops (locusts), trees (gypsy moths), evaluated for different pest control strategies, assess- and homes (termites). The total economic cost of insect- ing their toxic, lethal, repellent, antifeedant, fumigant, caused damage and disease is immeasurable; therefore, growth regulation, and deterrent effects on oviposition some genetically altered insect-resistant crops and vari- (5). Moreover, despite conventional insecticides, which ous insecticides have been developed to manage insects are based on a single active ingredient, botanical insec- and insect-related damage and disease (1). However the ticides containing mixtures of chemical compounds use of a wide range of synthetic insecticides has been can affect both behavioral and physiological processes. restricted recently, due to the high cost, harmful envi- Thus, the chance of pests developing resistance to such ronmental effects, their non-biodegradable nature, and substances is very low. It seems that seeking bio-insecti- increasing insecticidal resistance. An efficient alternative cides which are efficient, as well as being suitable and

Copyright © 2016, Iranian Red Crescent Medical Journal. This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCom- mercial 4.0 International License (http://creativecommons.org/licenses/by-nc/4.0/) which permits copy and redistribute the material just in noncommercial us- ages, provided the original work is properly cited. Cheraghi Niroumand M et al. adaptive to ecological conditions, is essential in obtain- lated to the pharmacological effects and mechanisms of ing sufficient insect control (2). action of the plants are reviewed in Table 2. Overall, these Traditional Iranian medicine (TIM) is a reasonable scien- plants belong to 16 different families and, among them, tific resource, which encompasses unique information in Lamiaceae is represented by the greatest number of taxa order to prevent and treat diseases (6, 7). For this study, (4), followed by Apiaceae (2). the chapter entitled “Tard al Havam” in the Al Qanun Based on the traditional resources, insecticidal or insect Fil Tibb and the Alaghraz altabyh va almabahesololayee repellent plants have been used in various routes of ap- were completely reviewed, and all of the plants reported plication, including the crude , decoction, incense, as possessing insecticidal activity in the Makhzan Al Ad- powder, , embrocation, and local administration. vieh were studied (8-10). The TIM resources have divided the plants into two In the present research, those plants which showed in- groups: I) plants which exhibit a general anti-insect effect, secticidal and insect repellent activity in the TIM (8-10) and II) plants that act against a specific insect, like bees, were reviewed individually, and evidence of their pos- ants, mosquitoes, flies, moths, fleas, termites, and scorpi- sible efficacy in the literature was gathered. ons. According to the Iranian traditional texts, the plants had either insecticidal or insect repellent actions, whereas 2. Evidence Acquisition modern phytotherapy describes different mechanisms of action for these purposes. The biological mechanisms Several medicinal plants have been perceived to have of these plants were searched in the literature using the insecticidal and insect repellent properties in TIM. following terms: repellency, insecticidal, larvicidal, acari- Therefore the present review was conducted to verify cidal, ovicidal, adulticidal, oviposition, fumigant toxicity, the insecticidal activity of some of the medicinal plants arrestant, and antifeedant effects against insects. used frequently in TIM. The authors searched the TIM lit- Among the 20 studied plants, four of them showed erature for “medicinal plants,” “insecticide,” and “insect greater activity against insects, and the most active repellent.” Additionally, information from important plants are discussed below: TIM books was collected and added to scientific reports derived from modern medical databases like PubMed, 3.1. Allium sativum L. Scirus, ScienceDirect, Google Scholar, and Scopus. All of A. sativum the retrieved articles were published between 1997 and has demonstrated numerous insecticidal ac- 2014, and any in vitro, in vivo, or clinical evidence for ef- tivities on a wide range of insect ; for example, its Delia radicum ficacy and pharmacological mechanisms related to the juice had insecticidal activity against and Musca domestica insecticidal and insect repellent properties of plants (11). extract has shown larvicidal Anopheles stephensi Culex quinquefas- were considered for inclusion. Those studies chosen for effects against and ciatus inclusion in this review revealed either the apparent ben- mosquitoes (12), and acaricidal activity against Tetranychus cinnabarinus eficial function of these remedies or demonstrated their (13). In addition, the extract of effectiveness indirectly on the mechanisms involved in has shown larvicidal activity against the eggs, lar- Callosobruchus maculatus insecticidal and insect repellent activity. Only published vae, and adults of (14). Essential Culex pipiens articles written in English were included in this review. oil bulbs exhibited larvicidal activity against Camptomyia corticalis The search terms included “insecticide” or “insect repel- (15), fumigant toxicity against (16), Lycoriella lent” in the title and abstract, and the name of each men- insecticidal and larvicidal potential against ingenue tioned plant in the whole text. The primary search results (17), and acaricidal properties against all stages Boophilus annulatus were evaluated by 2 independent investigators. Those of (18). Moreover, the leaf (ASAI) and A. sativum articles in languages other than English, review studies, bulb (ASAII) agglutinins from exhibited insec- Spodoptera papers that evaluated a mixture of the plant with drugs ticidal activity against the cotton leafworm, littoralis other than herbs, case reports, and case control studies (19). The garlic lectins, ASAI and ASAII, have also Acyrthosiphon were excluded. The references of the included papers revealed insecticidal properties against pisum were also reviewed for additional, suitable studies. Final- (pea aphids) (20). ly, the included papers were reviewed for mention of the scientific names of the plant, their parts, and extracts, as 3.2. Citrullus colocynthis L. Schrad. well as the active components and species of insects. Citrullus colocynthis leaf extracts have shown larvicidal, Culex quin- ovicidal, and repellency properties against the 3. Results quefasciatus mosquito (21), and larvicidal effects against Aedes aegypti Culex In this study, 20 herbal species were reported as insec- the early fourth instar larvae of and quinquefasciatus ticides or insect repellents in the Persian medical litera- (22). In addition, the extract of the whole ture. Table 1 shows all of the data pertaining to the plant plant has been examined in different studies, and showed species, listed according to the scientific name, family, larvicidal activity against the early fourth instar larvae of Anopheles stephensi Aedes aegypti Culex quin- common name, traditional Iranian name, mode of appli- (23, 24), , and quefasciatus cation, and traditional use. Moreover, all of the details re- (23). Its extracts have suppressed the

2 Iran Red Crescent Med J. 2016;18(2):e22361 Cheraghi Niroumand M et al.

Bactrocera zonata Artemia salina overall egg laying ability of (25), caused cytotoxicity toward (34). Finally, the essen- Lipaphis erysimi ( ) Aedes aegypti mortality against adult stages of 26 , tial oil of the branches repelled (35), while Tribolium custaneum and had insecticidal activity against the dust of the leaves caused insecticidal effects against Sitophilus zeamais (27). The seed extracts have revealed larvicidal proper- adults (36). Culex quinquefasciatus ties against the 3rd instar larvae of , Anopheles stephensi Aedes aegypti , and (28). 3.4. Ocimum basilicum L. Ocimum basilicum The of the plant has shown 3.3. Laurus nobilis L. Acyrthosiphon pisum Myzus per- insecticidal activity against , Laurus nobilis sicae Musca domestica The pure essential oil of has shown aphi- (37), and (38). It has also exhibited Brevicoryne brassicae Aedes aegypti Anopheles stephensi Culex dicidial activity against (29). More- repellency against , , quinquefasciatus Culex pipiens over, the essential oil of the leaves has shown fumigant (39), and adult female (40), Tribolium confusum Lymantria dispar toxicity against all of the life stages of as well as antifeedant properties against Tribolium custaneum Sitophilus oryzae (30); repellent potential against , (41). In addition, volatile toxicity against , Rhyzopertha dominica Tenebrio molitor Rhyzopertha dominica Cryptolestes pusillus (31), and larvae (32); , and has been Sitophilus zeamais insecticidal effects against adult (33), observed (42). Furthermore, the stem extract has revealed Rhyzopertha dominica Tribolium castaneum Culex quinquefasciatus , and (31); and larvicidal activity against (43).

Table 1. Anti-Insect Plants in Traditional Iranian Medicine Scientific Name Family Common Name TIM Name Mode of Application Traditional Use Allium sativum L. Liliaceae Garlic Som Decoction; Incense Lousicide; Bee repellent Artemisia absinthium L. [XE Asteraceae Wormwood Afsantin Powder Poultice Insect repellent “Artemisia absinthium L.”] Mosquito repellent Boswellia carterii Bir. [XE “Bo- Burseraceae Frankincense Kondor Decoction Killing flies swellia carterii Bir.”] Citrullus colocynthis L. Schrad. Cucurbitaceae Colocynth Hanzal Decoction Killing fleas Repelling fleas Dorema ammoinacum D.Don. Apiaceae Ammoniacum Oshagh Embrocating Insect repellent, Used in insecticide mixtures Ferula L. Apiaceae Asafetida Anjodan Incense Powder Insect repellent Ant rubbed onto surface repellent Iris germanica L. Iridaceae Orris Susan Incense of root Insect repellent Laurus nobilis L. Ghaar Incense Powder; Insect repellent; Smoke of leaves and Insecticide Malva sylvestris L. Malvaceae High mallow Khobazi Extract Bee repellent Mentha pulegium L. Lamiaceae Pennyroyal Fudanaj Burning the plant; Insecticide; Insect re- Incense Powder; Entire pellent; Clothes moth plant repellent Myrtus communis L. Myrtaceae Myrtle Aas Incense of leaves Insect repellent (espe- cially for mosquitoes) Nerium oleander L. Apocynaceae Oleander Defli Leaves Flea repellent Ocimum basilicum L. Lamiaceae Shahasfaram Fragrance Insect repellent Origanum majorana L. Lamiaceae Marzanjush Incense Insect repellent Peganum harmala L. Nitrariaceae African rue Harmal Incense Mosquito repellent Picea orientalis (L.) Peterm. Pinaceae Oriental spruce Senobar Wood ashes; Smoke of Insect repellent; wood Mosquito repellent Platanus orientalis L. [XE Platanaceae Oriental planetree Dolb Incense of leaves Termite repellent “Platanus orientalis L.”] Punica granatum L. Lythraceae Romman Incense Powdering Insect repellent surfaces L. Rutaceae Common rue Sodab Decoction Mosquito repellent Vitexagnus-castus L. Lamiaceae Chaste Banjankosht Incense Powdering Insect repellent surfaces Insecticide

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Table 2. Efficiency of Action of Traditional Iranian Anti-Insect Plants Part/extract Active Constituent Efficiency Ref Allium sativum Delia radicum Musca domestica Garlic juice - Insecticidal against and -(11) Anopheles stephensi Culex quinquefasciatus Tuber extract - Larvicidal against and (12) Tetranychus cinnabarinus Fruit extract - Acaricidal against (13) Callosobruchus Cloves extract - Larvicidal against eggs, larvae, and adults of (14) maculates Culex pipiens Essential oil of bulbs - Larvicidal against (15) Camptomyia corticalis Essential oil of bulbs - Fumigant toxicity against (16) Lycoriella ingenua Essential oil of bulbs - Insecticidal and larvicidal against (17) Boophilus annulatus Essential oil of bulbs - Acaricidal on all stages of (18) Spodoptera littoralis Leaves and bulb Lectins, (ASAI) (ASAII) Insecticidal against (19) Acyrthosiphon pisum Garlic lectins ASAI and ASAII Insecticidal against (20) Artemisia absinthium[XE “Arte- misia absinthiumL.”] Rhodnius prolixus Essential oil - Repellency against (44) Ixodes ricinus Essential oil of leaves Oxygenated monoterpenes Repellency against (45) Sarcoptes scabieivar. suis Leaf extract - Developmental inhibition of (46) Boswellia carterii[XE "Boswellia carterii."] Lycoriella ingenua Essential oil of resin - Larvicidal against (17) Sitophilus oryzae Essential oil of resin - Fumigant toxicity against (47) Aedes aegypti Anopheles stephensi Culex Essential oil - Larvicidal against , , and (48) quinquefasciatus Aedes aegypti Culex quinquefasciatus Essential oil - Repellency against and (39) Citrullu scolocynthis Culex quinquefasciatus Leaf extract - Larvicidal, ovicidal, and repellency against (21) Aedes aegypti Culex quinquefasciatus Leaf extract - Larvicidal against and (22) Aedes aegypti Anopheles stephensi Culex Whole plant extract Oleic acid and linoleic acid Larvicidal against , , and (23) quinquefasciatus Anopheles stephensi Whole plant extract - Larvicidal against the (24) Bactrocera zonata Fruit extract - Suppress overall egg laying of (25) Lipaphis erysimi Fruit extract - Insecticidal against adult stage of (26) Tribolium castaneum Fruit extract - Insecticidal against (27) Culex quinquefasciatus Anopheles stephensi Seed extract - Larvicidal against , , (28) Aedes aegypti and Ferula asafetida Leptinotarsa decemlineata Stem extract - Moderate antifeedant against larvae (49) Anabasis aphylla Root extract - Toxicity against (50) Laurus nobilis Brevicoryne brassicae Pure essential oil (purchased) - Aphidicidial activity against (29) Tribolium confusum Essential oil of leaves - Fumigant toxicity against all life stages of (30) Rhyzopertha dominica Tribo- Essential oil of leaves 1,8-cineole, , and Repellency and toxicity against and (31) isovaleraldehyde lium castaneum Tenebrio molitor Essential oil of leaves - Repellency against larvae (32) Sitophilus zeamais Essential oil of leaves - Insecticidal against adult (33) Artemia salina Essential oil of leaves - Cytotoxicity toward (34)

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Aedes aegypti Essential oil of branches - Repellency against (35) Sitophilus zeamais Dust of leaves - Insecticidal against adult (36) Mentha pulegium Dermatophagoides farinae D.pteronyssinus Essential oil (Purchased) - Acaricidal on and (51) Camptomyia corticalis Essential oil (Purchased) - Fumigant toxicity against (16) Musca domestica Essential oil of leaves - Fumigant and insecticidal against (38) Spodoptera littoralis Essential oil of leaves - Larvicidal (fumigation) against (52) Myrtus communis Culex quinquefasciatus Essential oil of Leaves - Repellency against (39) Aedes aegypti, Anopheles stephensi Culex Essential oil of Leaves - Larvicidal against , and (48) quinquefasciatus Ephestia kuehniella Plodia interpunc- Essential oil of Leaves Linalool Insecticidal against adults of , (53) tella Acanthoscelides obtectus , and Nerium oleander Anopheles stephensi Leaf extract - Larvicidal against the larvae and pupae of (54) Sitophilus zeamais Dust of and its suspen- - Insecticidal and repellency against adult (36) sion Ceratovacuna lanigera Plant (leaves, roots, and stem) - Inhibitory effect on the development of (55) extract Ocimum basilicum Acyrthosiphon pisum Myzus persicae Essential oil (aerial parts) - Insecticidal against and (37) Musca domestica Essential oil of the plant - Insecticidal against (38) Aedes aegypti Anopheles stephensi Culex Essential oil (purchased) - Repellency against , , and (39) quinquefasciatus Culex pipiens Essential oil of leaves - Repellency against the adult females of (40) Lymantria dispar Essential oil of leaves Linalool Antifeedant properties against (41) Sitophilus oryzae Rhyzopertha dominica Essential oil of leaves Methyl , estragole, Volatile toxicity against , , (42) Cryptolestes pusillus and linalool chemotypes and Culex quinquefasciatus Stem extract - Larvicidal against (43) Origanum majorana Ephestia kuehniella Essential oil of leaves Linalool Fumigant toxicity against eggs and adults (56) Camptomyia corticalis Essential oil (purchased) - Moderate fumigant toxicity against (16) Spodoptera littoralis Aerial part extract - Insecticidal and larvicidal against (52) Musca domestica Aerial part extract - Insecticidal against L. (38) Thrips tabaci Aerial part extract - Repellency against (57) Peganum harmala Bactrocera zonata Seeds extract - Repellency against (25) Plodia interpunctella - Harmaline Larvicidal against (58) Tribolium castaneum Seeds extract - Insecticidal against (59) Punica granatum Sitophilus zeamais Tribolium castaneum Fruit pericarp extract - Antifeedant against and (60) Tetranychus cinnabarinus Leaves extract - Acaricidal against (13) Ruta graveolens Aedes aegypti Essential oil of aerial parts - Repellency and larvicidal against (61) Vitexagnus-castus Ixodes ricinus Rhipicephalus sanguineus Seeds extract - Repellency against and (62) Pediculus humanus capitis Seeds extract - Repellency against (63)

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4. Conclusions uted to the development of the protocol and writing the manuscript. Elahe Karimpour Razkenari collected the In order to stop the spread of insect borne diseases and data. Mohammad Reza Shams-Ardekani and Gholamreza damage, save the environment, and improve the quality Amin contributed to the development of the protocol. of public health, significant effort should be made to find Mahnaz Khanavi and Tahmineh Akbarzadeh suggested new insect control strategies. The main approaches to in- the topic of the article and contributed to the develop- sect control have consisted of using synthetic pesticides ment of the protocol. such as organochlorine and organophosphorus com- Funding/Support: This research has been supported by pounds, which have not been very successful, especially a Tehran University of Medical Sciences grant. from an ecological point of view (2). Synthetic insecti- cides not only kill insects, but contaminate the food and cause air, water, and soil pollution. 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