Endod, a potential natural pesticide for use in developing countries

Legesse Wolde-Yohannes

Institute of Pathobiology, Addis Ababa University, Addis Ababa, Ethiopia

In recent years, economic and ecological factors have forced many developing countries to consider alternatives to synthetic pesticides, such as the natural molluscicides found in local plants. Since the early 1930s, more than 1 071 plant species have been tested: 48% contained substances toxic to snails, the intermediate hosts of schistosomiasis, some of them as potent as manufactured molluscicides. Endod is one of the most promising plant molluscicides because of its high toxicity to the snails, low toxicity to mammals, stability under various environmental conditions, biodegradability, widespread distribution in tropical Africa, and potential for large-scale cultivation. Results of the first longitudinal studies on the cultivation, yield, and molluscicidal potency of endod types 3, 17, and 44 indicate that they can be cultivated successfully and that type 44 is most suitable for schistosomiasis control.

Plant-derived molluscicides are a reasonable option for the control of schistosomiasis, particularly in developing countries with agricultural economies, where parasitic disease affects at least 200 million people (Adams 1986; Kloos and McCullough 1987; Legesse and Kloos 1990).

Since the early 1930s, 1 071 plant species have been tested for molluscicidal activity (Kloos and McCullough 1987). Few, however, have proven to have the characteristics necessary for widespread use: low toxicity, water soluble, common, easy to cultivate, and consistently high molluscicidal potency (Legesse and Kloos 1990). If other uses could be found for these few species their value would increase (Adams 1986; Legesse et al. 1986; Kloos and McCullough 1987; Kloos et al.1987; Legesse and Kloos 1990).

Commercially available chemical molluscicides are expensive in view of the large quantities required for control programs on a regular basis and currency constraints faced by developing countries (Lambert et al.1985). Compounds, such as copper sulfate and sodium pentachlorphinate, have been used as molluscicides for many decades in Egypt, the Sudan, and other parts of the world to control schistosomiasis.

Recently, however, the ethanolamine salt of niclosamide (bayluscid), has been found to be more effective and is currently the only molluscicide recommended by the World Health Organization (WHO) for global use. However, partly because of its high cost (26 000 USD/t in 1974), most developing countries, especially those in Africa, are not using it to control schistosomiasis. Meanwhile, many well-intentioned agricultural development and water conservation schemes are providing more sites for snails to breed, and schistosomiasis is spreading rapidly.

Endod: a potential pesticide

Endod, a natural molluscicide, is biodegradable. Its active principle decomposes rapidly, breaking down to inert and nonharmful material within a few days. Accordingly, a concerted effort to develop simple methods for the development and safe use of endod could pave the way for use of other plant pesticides in developing countries. Ideally, each country where schistosomiasis is endemic should select local molluscicide-producing species for snail control. In all cases, however, the principle and approach remains the same.

The use of endod berries as a soap, dating back hundreds of years, led to studies of its detergent, antifungal, antiprotozoan, spermicidal, and molluscicidal properties (Lemma et al.1979). The berries have been traditionally used in Ethiopia and other African countries for washing clothes and as a medicine (Hutchinson and Dalziel 1929; Dalziel 1936; Watt and Breyer Bandwik 1962; Humbert 1971; Thiseltch-Dryer 1973; Legesse and Kloos 1990). However, the molluscicidal property of endod has given it international recognition as a potential means of control for snails that transmit schistosomiasis (Lemma et al.1979).

Endod or soapberry plant (Phytolacca dodecandra) is a member of the Phytolaccaceae and is a dioecious scandent shrub or liana averaging 2-3 m in height, but as climber sometimes growing as tall as 10 m. The male flowers are light yellowish green, in long staminate racemes, and bear no fruit. The female flowers are light yellowish green in short staminate racemes, producing fruit that is five lobed and 1 cm in diameter; ripe fruits are pink or red (Hutchinson and Dalziel 1929). Under favourable climatic conditions in Ethiopia, the plant bears fruit from November to June (Legesse 1983).

The molluscicidal property of endod has been studied over the last 25 years at the Institute of Pathobiology at Addis Ababa University, the Tropical Products Institute in London, the Stanford Research Institute in California, the G.W. Hooper Foundation at the University of California, the Harvard School of Public Health in Boston, the Public Health Service Laboratory and Field Station in Puerto Rico, the US Naval Medical Research Unit in Cairo, Carleton

University in Ottawa, and in other laboratories in different parts of the world, and the results are promising (Lambert et al. 1985).

Some 50 scientific papers have been published on the subject and several patents have been secured on different aspects of processing this plant product (Lemma et al. 1979). Chemical studies to isolate and identify the active principle in endod berries led to the discovery of a new compound, oleanolic acid glucoside, which Stanford Research Institute’s chemists have named lemmatoxin (Parkhurst et al. 1974).

Agronomic studies have also been carried out to select endod strains with high molluscicidal potency and high yields as well as those that are easy to cultivate and have a high resistance to insect pests (Legesse and Kloos 1990). Genotypes of endod, two to three times more potent than the original type, have been developed by selection since the 1970s. At present, out of 65 types, 10 have been selected for their high berry yield, high molluscicidal potency, and insect resistance (Legesse and Kloos 1990). Three are in production (Lugs 1981; Legesse 1983; Legesse et al.1986; Legesse and Kloos 1990). The selected types are producing berries with the capacity to kill all snails in a sample within 24 h at a concentration of 7-10 ppm (of dry berry material) (Legesse 1983; Legesse et al. 1986; Legesse and Kloos 1990).

The detergent properties of endod are also promising. Its foaming and thermal stability and cleaning properties equal or exceed most imported or locally made detergents in developing countries. The water extract of endod can be used as an effective substitute for dodecylbenzene sulfonic acid (DDBSA), a petrochemical byproduct used as a surfactant in commercial detergent formulations for washing fine grades of cotton, linen, and wool.

From a point of view of acceptability, endod has been used locally for centuries. People in the Ethiopian highlands have used the berries as a laundering agent for the white cotton shawls (shama) that are a part of the Ethiopian culture.

Addis Ababa University and the National Chemical Corporation are collaborating on research into the detergent properties of endod (“Findings on the viability of utilizing endod (Phytolacca dodecandra) in detergent production.” Unpublished report, 1984). In two pilot projects at Reppi Soap Factory, endod extract was substituted for DDBSA. The cleaning properties of the endod-based product were comparable to those of DDBSA-based detergent. The detergent preparation can also be used without further processing for snail control (Legesse and Kloos 1990). Use of endod is expected to save foreign currency now spent on importing detergent ingredients.

Investigations have also been undertaken on the agrobotanical characteristics of endod in Ethiopia and elsewhere (Table 1). The annual dry-weight yield of endod berries, types 3, 17, and 44, increased over the 4-year study period, especially between the first and third harvests. Mean berry yield per hectare was higher for type 44 (2 040 kg) than for types 17 (1 165 kg) and 3 (829 kg).

Table 1. Berry yields for endod types 3,17, and 44 over 4 years.

Molluscicidal tests indicated that type 44 was most active, achieving 100% kill of Bulinus pfeifferi at 5 ppm for newly harvested berries and 7.5 ppm for 1-year-old and 10 ppm for 4-year-old ground berries (Table 2). At a concentration of 10 ppm, types 3 and 17 killed all snails, but effectiveness decreased considerably after storage.

Table 2. Molluscicidal potency (% mortality) of fresh, l-year, and 4-year crude powdered berries of endod types 3,17, and 44 against B. pfeifferi.

The molluscicidal saponin yield of endod is about 25% of the weight of dry ground berries. Thus, the amount of saponin that can be extracted from the 4th-year harvest is 688 kg/ha for type 44,463 kg/ha for type 17, and 262 kg/ha for type 3.

Field trials are now needed to establish molluscicidal efficacy and effect on nontarget organisms in natural snail habitats in accordance with principles and methods of field evaluation of plant molluscicides described by Sturrock and Duncan (cited in Kloos and McCullough 1987). Assuming that a satisfactory molluscicidal effect can be obtained at a concentration of endod of 20 ppm in the field (Lugs 1981),137 500 m³ of water may be treated in one application using the 4th-year berry yield of 2 750 kg/ha possible with type 44 endod.

Due to differences in plant variety, location, soil, climate, method of extraction, and even seasonal changes, standardization of the plant extract is required to ensure consistent effectiveness (Legesse and Kloos 1990). Toward these objectives, recommendations for an endod standard were made at an international workshop in Swaziland (Makhubu et al. 1986).

Comprehensive and systematic plant molluscicide development and the proposed multiple uses of endod depend to a large degree on intersectoral and interinstitutional collaboration involving ministries of health, agriculture, industry, and universities to assure broad-based botanical, chemical and toxicologic, agronomic, public health, and community-action programs. At the community level, active participation of local people in project planning, production, processing, and application of plant molluscicides and the assessment of their effectiveness in snail control is essential for the development of viable and low-cost, community-based, schistosomiasis-control programs (Kloos and McCullough 1987; Legesse and Kloos 1990).

In March 1983, the Zambian National Council for Scientific Research, in collaboration with Ethiopian scientists, convened an international scientific workshop on endod. Research was reviewed, areas for future research and development were identified, and recommendations were made for specific follow-up activities (Legesse 1983). Following the recommendations, the governments of Ethiopia, Swaziland, and Zambia expressed increased interest and support for collaborative research and development of endod, both as a locally produced molluscicide for schistosomiasis control and as an important additive in commercial detergent formulations for laundry use. Since a second international workshop (Makhubu et al.1986), there has been a rapid increase in interest in this plant and active research is being carried out by many young and talented African scientists in different parts of the continent.

An expert group, organized by the United Nations Financing System for Science and Technology for Development and the International Development Research Centre (IDRC), developed a procedure for preparing water extract of endod (endod-S) to be used as a standard material for testing in different laboratories (UNFSSTD/IDRC 1986). The group also delineated selected basic toxicological tests to be performed to clear endod for field trials.

IDRC has since commissioned studies to establish the basic regulatory requirements for the licencing of endod, including acute mammalian and ecotoxicity studies performed in Canada, the USA, and Europe under “good laboratory practice.” The Institute of Pathobiology, Addis Ababa University, participated in these studies and provided clonal material of endod type 44 grown in isogenic plots at the Institute.

An internationally accepted water preparetion of endod type 44 (endod-S) has been developed and independently checked by laboratories in Canada, Switzerland, and the USA. Using extracts from this procedure, toxicologic tests at the tier 1 level (OECD) of the premarketing guidelines have been completed. According to results to date, endod is no more toxic than bayluscid (Lambert et al. 1991). On the basis of this, IDRC is supporting comprehensive community-based field trials on endod’s effect on schistosomiasis transmission in Zimbabwe.

In addition, scientists from 10 African countries and Brazil have now formally established an endod technical cooperation among developing countries (TCDC) network through which they plan to coordinate their work and collaborate further with other international experts in Canada, the USA, and various European countries. The African partners in the network are Ethiopia, the Gambia, Ghana, Kenya, Nigeria, Sudan, Swaziland, Zambia, and Zimbabwe.

A third international workshop on endod was held in Addis Ababa, Ethiopia, in October 1990. The results of the tier 1 toxicology studies were reviewed and research needs, strategies, and model protocols were determined for facilitating community-based trials, including local agrobotanical studies, ecotoxicologic studies, and integrated schistosomiasis intervention studies. Reports from field studies in Ethiopia, Swaziland, Zambia, and Zimbabwe were also presented at the meeting.

Conclusion

All three types of endod can be successfully cultivated, but type 44 has superior agronomic and molluscicidal characteristics. Endod berries may be produced on a large scale with sustained yield and potency, eliminating a major barrier for plant molluscicide development. The results of this study may facilitate the selection of the most suitable endod types for schistosomiasis control in at least three other African countries where endod cultivation and adaptation trials are being carried out (Adams 1986). This study also clearly indicates that emphasis should be placed on promotion of the multiple uses of endod-derived products.

Adams, R.P. 1986. Report of the working group on agrobotany and extraction. In Makhubu, L.; Lemma, A.; Heyneman, D., ea., Report of the 2nd international workshop on endod. Council on International and Public Affairs, New York, NY, USA. Pp. 36-42.

Dalziel, J.M. 1936. The useful plants of west tropical Africa. Crown Agents, London, UK.

Humbert, H. 1971. Flora de Madagascar et des Comores. Musnational d’histoire naturelle, Laboratoire de phanerogamie, Paris, France.

Hutchinson, J.; Dalziel, J.M.1929. Phytolaccaceae: flora of west tropical Africa (vol. 1, part 1). Crown Agents, London, UK.

Kloos, H.; McCullough, F.S.1987. Plants with recognized molluscicidal activity. In Mott, K.E., ea., Plant molluscicides. John Wiley and Sons, Chichester, Sussex, UK. Pp.45-108

Kloos, H.; Waithaka Thiongo, F.; Ouma, J.H.; Butterworth, A.E.1987. Preliminary evaluation of some wild and cultivated plants for snail control in Machaka District, Kenya. Journal of Tropical Medicine and Hygiene, 90,197-204.

Lambert, J.D.H.; Legesse Wolde-Yohannes; Makhubu, L.P.1985. Endod: potential for controlling schistosomiasis. Bioscience, 35, 364-366.

Lambert, J.D.H.; Temmink, J.H.M.; Marquis, J.; Parkhurst, R.M.; Lugt, C.; Holtze, K.; Warner, J.E.; Schoonen, A.J.M.; Dixon, G.; Legesse Wolde-Yohannes; de Savigny, D.1991. Endod: safety evaluation of a plant molluscicide. Regulatory Toxicology and Pharmacology, 14, 189-201.

Legesse Wolde-Yohannes.1983. Past and ongoing agrobotanical studies of endod (Phytolacca dodecandra) in Ethiopia. In Lemma, A.; Heyneman, D.; Silangwa, S., ea., Endod (Pkytolacca dodecandra): report of the international scientific workshop, Lusaka. Tycooli International Publishing, Dublin, Ireland. Pp.125-129.

Legesse Wolde-Yohannes; Demeke, T.; Lambert, J.D.H. 1986. Cultivation studies of endod (Phytolacca dodecandra) and its implication in schistosomiasis control. Institute of Pathobiology, Addis Ababa University, Addis Ababa, Ethiopia. Publication 3.

Legesse Wolde-Yohannes; Kloos, H.1990. Agronomic and molluscicidal studies of three types of endod (Phytolacca dodecandra). In press.

Lemma, A.; Heyneman, D.; Kloos, H., ed. 1979. Studies on the molluscicidal and other properties of the endod plant (Phytolacca dodecandra). University of California, San Francisco, CA, USA.

Lugt, C.B. 1981. Phytolacca dodecandra berries as means of controlling bilharzia transmitting snails. Institute of Pathobiology, Addis Ababa University, Addis Ababa, Ethiopia.

Makhubu, L.; Lemma, A.; Heyneman, D., ed.1986. Report of the second international workshop on endod. Council of International and Public Affairs, New York, NY, USA.

Parkhurst, R.M.; Thomas, D.W.; Skinner, W.A.; C;ray, L.W. 1974. Molluscicidal saponins of Phytolacca dodecandra. Canadian Journal of Chemistry, 52, 702-705.

Thiseltch-Dryer, W.T.1973. Flora of tropical Africa (vol. VI). Reeve, Ashford, Kent, UK. Section 1, p. 97.

UNFSSTD/IDRC (United Nations Financing System for Science and Technology for Development and International Development Research Centre). 1986. Endod toxicology: report of the Expert Group meeting. UNFSSTD, New York, NY, USA.37 pp.

Watt, J.M.; Breyer Brandwik, M.G. 1962. The medicinal and poisonous plants of southern and eastern Africa. Livingston, Edinburgh, UK.