Mosquitoes are progressively becoming resistant to industrial repellents and insecticides. This is the case for pyrethroids used on bednets.
Most of these products are expensive and African households cannot afford their purchase.
Plants, their extracts and their essential oils have been used during centuries to fight aggressive mosquitoes responsible for malaria, dengue, sleeping sickness but also insects acting as vectors for many other diseases.
Native plants have the advantage of low cost and local availability. Their action is related to several constituents working in synergy ; the probability that they develop resistance is lower as for synthetic insecticides used in monotherapy.
The repellent and insecticidal potential of plant material has been exploited for thousands of years by man, most simply by hanging bruised plants in houses. Many plant volatiles are deterrent or repellent because they have high vapour toxicity to insects.
1. Insecticidal properties
A study made in Italy on anti-plasmodial and insecticidal activities of essential oils of aromatic plants growing in the Mediterranean area showed that thymol from savory (Satureja thymbra) showed the highest larvicidal and adulticidal activities. In essential oil fractions obtained by hydrodistillation carvacrol and terpine-4-ol also showed some activity. (M Dell’Agli et al., Malaria Journal, 2012, 111 :219). Thymol appears to be a neuractive chemical which affects the flight motor activity and wing beat frequency in flies (R Waliwitya et al., Pest Manag Sc, 2009).
An extensive study on the insecticidal properties of thymol is a thesis from the Iowa State University (Sang Kyun Lee, 1997). This thesis compares the mortality of adult Musca domestica (housefly) exposed to 3 phenols, 12 alcohols, 7 ketones, 4 acids and 7 monoterpenes. Thymol is the strongest and comes close to pyrethrins.
Monoterpenoids commonly found in plant essential oils were tested for acute toxicity via topical application to tobacco cutworms, a lepidopter. The most lethal among such compounds was thymol from garden thyme (Thymus vulgaris) Feeding deterrence was determined using a cabbage leaf disk choice test. Thymol again was the most efficient (LA Hummelbrummer et al., J Agricol Food Chem 2001, 49, 715-20). Essential oil or aqueous leaf extract from Azadirachta indica (neem) are also excellent feeding deterrents.
Essential oils of thyme (Thymus numidicus), from Algeria were isolated by steam distillation. The major components were thymol (51.3%), carvacrol (9.4%), linaool (3,3%), caryophyllene, (2.7%). The fraction containing thymol (51%) and linanool (3,2%) showed the highest insecticidal activity against Rhizoperta dominica (F Saidj et al., Ecole Polytechnique, Alger). The same insecticidal properties of thymol in the essential oil of Trachyspermum ammi against Anopheles stephensi have been documented (SK Pandey, Parasitology Research, 2009, 105, 507-512).
A study of monoterpenoids showed that for topical acute toxicity on larvae the most potent were thymol and carvacrol. The most profound synergistic effect was found in the mixture p-cymene, thymol, carvacrol. (Roman Pavela, J Biopest, 2010, 3, 573-78). The same author in another study found in laboratory conditions that the sublethal application of thyme oil to the adults of the housefly significantly reduced their longevity and the natality decreased by 80%, And even larvae which emerged from eggs from female flyies which had been treated, were non vital. In a third study (R Pavela, Phytother Research 2008, 22, 274-8) the same author studied the insecticidal activity of 34 essential oils extracted from plants and found those from Origanum vulgare, majorana, compactum, Ocimum basilicum, Thymus vulgaris were lethal in doses in the microgram range. The advantage of these plants is that they are easy to grow in many countries and have well known nutritional values. Some of the terpenes, like carvacrol, also have strong antiplasmodial properties.
Oregano oils are rich in thymol (38.8%), carvacrol (32.9%), p-cymene (7,9%). They have strong toxicities against Rhizoperta dominica by contact or by fumigation (O Khalfi et al., J Sc Food and Agricul, 2008, 9, 1562-66). Efficient also against drosophila (I Karpouhtsis et al., J Agricult and Food Chem, 1998, 46, 1111-15). Thymol contributes to the acaricidal properties of Ocimum gratissimum.
A thesis from the Kenyatta Universty (Simyiu Silas Khamala, April 2004) evaluated the insecticidal and repellent properties of plants from Kenya. Among the plants studied Artemisia afra showed reasonable insecticidal activity. A afra essential oil attained 100 % mortality at 8% after 4 hours and 86% at 2% concentration after 6 hours. This activity is possibly related to thujone. Coumarins have a knock down effect, scopoletin being the most potent, but do not kill mosquitoes (K Narayanaswamy et al., The Scientific World Journal, 2014)
Saponins which are present in many plants have strong insecticidal properties. In fact, saponins protect plants from phytopathogenic microorganisms, phytophagous mammalian and insects.
The anophelocidic activity of the aqueous, terpenic and steroidic extracts of Artemisia annua were studiend at the laboratory of Lwiro in R.D. Congo (B Z Musaka et al, International J Innovation and Scientific Research, 2014, 10-2, 318-323). The highest mortality is noticed for the aqueous and steroidic extracts, much more than for the terpenic components. Wormwood Artemisia absinthium wetted in seawater and sprayed kills insects in living quarters (CRA Goodfray, Agrochemicals from Natural Products. 1985 NY, Dekker ed)
Thymol, saponins and carvacrol are FDA approved and are included by the Council of Europe in the list of chemical flavourings.
The association ACECI in Burundi (www.aceci.org) has developped a mosquito repellent based on Nepeta cataria (catnip in english, cataire en français, Katzenminze auf deutsch). The study by local students in medicine in collaboration with Montreal’s Ecole Polytechnique together with the Government of Burundi showed that catnip oil reduced the number of bites from mosquitoes by 91.7%. The trial involved 60 volunteers. The results and the analytical data have been submitted for publication.
Trials NCT01160809 in Ethiopia financed by the U.S. National Institute of Health. Daily application of mosquito repellent during the evening followed by the use of LLINs during bedtime at community level has significantly reduced malaria infection. The finding has strong implication particularly in areas where malaria vectors feed mainly in the evening before bedtime. The topical repellent used was Buzz-Off® petroleum jelly and essential oil blend obtained from the GREEN PLC in Addis Ababa,
Ahmed Hassanali from Kenya has shown in a well documented paper (Phytochemistry, 2011, 72, 109-114) that Nepeta cataria was in many aspects (spatial and contact repellency, knockdown) equivalent to the synthetic DEET. A study made by USDA-ARS finds that mosquitoes land mosquitoes land less on surfaces covered with nepetalactone than on a surface covered with DEET (U Bernier et al., J Med Entomol 42, 306-11, 2005). A study from Thailand found that mosquitoes try to escape from a chamber containing catnip oil (S Polsomboon et al., J Am Mosquito Control Assoc. 2008, 24, 513-19). A study from India (O Koul et al., Biopestic Inter, 2008, 4, 63-84) found that nepetalactone repels mosquitoes ten times more than DEET. Another study from the Dupont de Nemours company (NC Spero et al., J Med Entomol, 2010) documents the repellency of catnip oil formulations against black flies and mosquitoes in the field. Hydrogenated catmint oil is registered as biopesticide by EPA. Nepeta oils have a longlasting effect.
Evaluations of catnip oil toxicity were conducted (Zhu JJ et al., Med Vet Entomol. 2009 Sep;23(3):209-16) to provide a broad-spectrum safety profile of catnip oil use as a potential biting and nuisance insect repellent in urban settings. Acute oral, dermal, inhalation, primary dermal and eye irritation toxicity tests were performed and were found to be extremely low. The acute oral LD(50) of catnip oil was found to be 3160 mg/kg body weight (BW) and 2710 mg/kg BW in female and male rats, respectively. The acute dermal LD50 was > 5000 mg/kg BW. The acute inhalation LD50 was observed to be > 10,000 mg/m3.
When comparing with pyrethroids or malathion this is very encouraging because these synthetic repellents applied on bed nets or on indoor walls are toxic for pregnant women and children, and are carcinogenic (H Shukla et al., Cancer Lett. 2002 Aug 8;182:33-41).
A study from India compared the action of essential oils from 23 plants. Top ranking in repellency and knockdown effect were catnip, basil, thyme, citronella (A Uniyal et al., J Entomology and Zoology Studies, 2014, 2, 351-357). Some of them were almost equivalent to Malathion, without creating the adverse effects like irriataion, rashes and allergic reactions.
Ocimum and Moringa are also well known for their repellent properties (K Prabhu et al., Asian Pacific J of Tropical Biomedicine, 2011, 1, 124-129). Ocimum americanum potted plants are often used as repellents inside houses. Ocimum gratissimum and Ocimum basilicum have recently been compared to other plant repellents and generally are top ranking compared to Azadirachta indica, Citrus lemon, Jatropha curcas (TC Kazembe et al., Bull Envir Pharmacol and Life Sciences, 2012, 8, 65,71). In Tanzania trials were run with the essential oil of Ocimum suave against Anopheles gambiae and Culex quinquefasciatus and found that this oil provided personal protection of 90% comparable to DEET (EJ Kweka et al. Parasites and Vectors, 2012, 5. 189).
Citronella, Cymbopogon citratus oils also have good repellent properties but they are not long lasting.
Artemisia vulgaris contains insect repellents which can be released from the plant by combustion. When tested against Aedes aegyptii, myrcene, beta-pinene, limonene, 1,8-cineole were identified as repellents, but the strongest was terpin-4-ol (Yeh-Shen Hwange et al., J Chem Ecology, 1985, 11, 1297-1304). In the study of Roman Pavela described in the previous section for acute fumigant toxicity the most potent terpenes were alpha-terpinene, p-cymene, 1,8-cineole. These are present in Artemisia annua, a plant well known in China for its fumigant properties.
In South-America, Ethiopia, Kenya, China several trials have been run with the essential oil of Eucalyptus maculata citriodora alias Corymbia citriodora leaves and give excellent results equivalent to DEET (E Abiy et al., Malaria Journal 2015 14, 187; N Hill et al., London School of Hygiene and Tropical Medicine, BMJ, Aug 2007 ; SJ Moore et al., Malaria Journal, 2007, 6 101).The essential oil of the lemon-scented gum mainly consists of citronellal (80%), produced largely in Brazil and China. While unrefined oil from the lemon eucalyptus tree is used in perfumery, a refined form of this oil is used in insect repellents. The refined oil's citronellal content is turned into cis- and trans- isomers of p-menthane-3,8-diol (PMD), a process which occurs naturally as the eucalyptus leaves age. This refined oil, which includes related compounds from the essential corymbia citriodora, is known widely by its registered tradename, "Citriodiol", but also by generic names which vary by country or continent: "oil of lemon eucalyptus" or "OLE"(USA); "PMD rich botanic oil" or "PMDRBO"(Europe); "PMD and related oil of lemon eucalyptus compounds" (Canada) ; in Scandinavia « MyggA »; Extract of Lemon Eucalyptus in Australia. Pure PMD is synthesized for commercial production from synthetic citronellal.
The essential oil from Hyptis suaveolens, bush mint, is as efficient as DEET and provides long lasting repellency (AZ Abagli et al., The Open Entomology Journal, 2011, 5, 45-48). Strong repellent properties of piperitenone from Mentha spicata have also been noticed against Anopheles stephensi (AK Tripathi et al., 2004, 41. 691-698). This plant is growing abundantly in Burundi.
All the trials run with plant based topical repellents used in the early evening followed by the use of insecticide treated nets during the night give impressive results of 90% malaria reduction , compared to 40% with the use of bed nets only. The recommendation of the London School of Hygiene and Tropical Diseases strongly recommends that treated bed nets should not used as the only means of preventing malaria in areas where vectors feed mainly in the evening.
Further field tests with these plants extracts should urgently be run. Native plants have the advantage of low cost and local availability and it is important for African countries to develop their own technology in this fight, rather than importing molecules like pyrethroids which initially were of African origin.
Pierre Lutgen, IFBV-BELHERB
Ginette Karirekinyana, ACECI