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Title: Potential of the desert locust schistocerca gregaria (Orthoptera: Acrididae) as an unconventional source of dietary and therapeutic sterols

Author
item CHESETO, XAVIER - International Centre Of Insect Physiology And Ecology
item KUATE, SERGE - International Centre Of Insect Physiology And Ecology
item TCHOUASSI, DAVID - International Centre Of Insect Physiology And Ecology
item NDUNG'U, MARY - Jomo Kenyatta University
item Teal, Peter
item TORTO, BALDWYN - International Centre Of Insect Physiology And Ecology

Submitted to: PLOS ONE
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/12/2015
Publication Date: 5/13/2015
Citation: Cheseto, X., Kuate, S.P., Tchouassi, D., Ndung'U, M., Teal, P.E., Torto, B. 2015. Potential of the desert locust schistocerca gregaria (Orthoptera: Acrididae) as an unconventional source of dietary and therapeutic sterols. PLoS One. doi: 10.1371/journal.pone.0127171.

Interpretive Summary: The increasing world population has worsened the serious problem of food security especially in developing countries (Pinstrup, 2002; FAO. 2002). Under the new paradigm shift of “insects to feed the world”, insects are increasingly being recognized not only as a source of food to feed the ever growing world population but also as potential sources of new products and therapeutic agents (Pemberton, 1999; Defoliart, 2002; Chapman, 2007 and Chakravorty et al., 2011). In this regard, insects satisfy three important requirements: (i) they are an important source of protein and other nutrients; (ii) their use as food has ecological advantages over conventional meat and, in the long run, economic benefits for mass production as animal feed and food, and (iii) a rich source of drugs for modern medicine (Dettner et al., 1997; Opitz and Müller, 2009; Chakravorty et al., 2011). The desert locust, Schistocerca gregaria (Orthoptera: Acrididae), is an economically damaging pest of a wide range of crops, mainly cereals in the Sahel region of Africa (FAO, 2012). It occurs in many parts of Africa and Asia causing major outbreaks with the recent threats occurring in Eritrea, Somalia, Ethiopia, Djibouti, Yemen, Saudi Arabia and Madagascar (FAO, 2014). Despite its alarming threat to food security, it is an excellent source of dietary components not only in many African resource poor communities (Illgner and Nel, 2000), but also several other countries including; Thailand (Yhoung-Aree et al., 1997), North East India (Pemberton, 1999; Chakravorty et al., 2011) and Latin America (Defoliart, 2002). To date, much of the research on the desert locust has focused on its control, physiology, nutrition, metabolism and biochemistry (Grieneisen, 1994; Svoboda, 1999; Behmer and Nes, 2003; Gilbert, 2004; Behmer et al., 2011). However, an emerging new dimension in the research on S. gregaria is on its potential as a source of compounds of dietary and therapeutic value for food and nutritional security in Africa. Nutrient analysis of the desert locust has shown that, about 62 % of the dry weight of an adult desert locust consists of proteins, 17 % as fats, with the remainder as inorganic constituents (Si, Cu, Fe, Mn, Na, K, Ca, Mg, Ti, Ni, P, S) (Uvarov, 1977; FAO, 2012). Furthermore, the desert locust is easy to rear, requiring no special feeding mode. At the International Centre of Insect Physiology and Ecology, based in Nairobi, we have successfully mass reared a large gregarious colony of the insect on wheat seedlings for over a hundred generations, periodically infusing the colony with field samples to prevent genetic drift. It is well established that dietary plant sterols lower plasma cholesterol concentrations by inhibiting intestinal cholesterol absorption (Loizou et al., 2009; Blásquez et al., 2011). Although vegetable oils and products based on them are generally the richest sources of phytosterols (Piironen et al., 2000), insects can also be potential sources of useful sterols for humans although very little has been done in this context. Documentation of sterols in grasshoppers and the desert locust is narrowed to its use and metabolism by the same insects (Behmer and Nes, 2003). Like most arthropods, the desert locust is incapable of biosynthesizing sterols de novo from isoprenoid precursors, thus necessitating its acquisition from dietary sources (Grieneisen, 1994; Svoboda, 1999; Behmer and Nes, 2003; Gilbert, 2004; Behmer et al., 2011). Sterols are well known to serve various roles in insects such as components of cellular membrane (Grieneisen, 1994; Behmer and Nes, 2003), precursors for several physiologically active metabolites and hormones like ecdysteroids, hedgehog signaling which controls cell proliferation and differentiation (Porter et al., 1996; Briscoe and Therond, 2005). Given the paucity of data on the sterol composition of the

Technical Abstract: Insects are increasingly being recognized not only as a source of food to feed the ever growing world population but also as potential sources of new products and therapeutic agents, among which are sterols. In this study, we sought to profile sterols and their derivatives present in the desert locust, Schistocerca gregaria, after feeding the fifth-instar nymphs on wheat seedlings, focusing on those with potential importance as dietary and therapeutic components for humans. Using coupled gas chromatography-mass spectrometry (GC-MS), we analyzed and compared the quantities of sterols in the different parts of the gut and tissues of the locust. We identified a total of 34 sterols which showed a patchy distribution in the gut, but with a higher composition in the foregut (55%) and midgut (31%). Fed ad libitum on wheat seedlings, five sterols unique to the insects were detected. These sterols were identified as 7-dehydrocholesterol, desmosterol, fucosterol, (3ß, 5a) cholesta-8, 14, 24-triene-3-ol, 4, 4-dimethyl, and (3ß, 20R) cholesta-5, 24-diene-3, 20-diol with the first three having known health benefits in humans. Incubation of the fore-, mid- and hindgut with cholesterol-[4-13C] yielded eight derivatives, three of these were detected in the gut of the desert locust after it had consumed the vegetative diet but were not detected in the diet. Our study shows that the desert locust ingests phytosterols from a vegetative diet and, amplifies and metabolizes them into derivatives with potential salutary benefits and we discuss our findings in this context.