Journal of Food Composition and Analysis 30 (2013) 120–124 Contents lists available at SciVerse ScienceDirect Journal of Food Composition and Analysis journal homepage: www.elsevier.com/locate/jfca Original Research Article Nutrient composition of four species of winged termites consumed in western Kenya John N. Kinyuru a,*, Silvenus O. Konyole b, Nanna Roos c, Christine A. Onyango a, Victor O. Owino d, Bethwell O. Owuor e, Benson B. Estambale b, Henrik Friis c, Jens Aagaard-Hansen c, Glaston M. Kenji a a Jomo Kenyatta University of Agriculture and Technology, Kenya University of Nairobi, Kenya University of Copenhagen, Denmark d Winfood Project, University of Nairobi, Kenya e Catholic University of Eastern Africa, Kenya b c A R T I C L E I N F O A B S T R A C T Article history: Received 22 February 2012 Received in revised form 13 February 2013 Accepted 17 February 2013 The objective of this study was to gain knowledge on the nutrient composition of Macrotermes subhylanus, Pseudacanthotermes militaris, Macrotermes bellicosus and Pseudacanthotermes spiniger termite species consumed in western Kenya. Proximate, iron, zinc, calcium and fatty acid composition were analysed in order to ascertain their potential in food-based strategies to improve nutritional health. The fat content was 44.82–47.31 g/100 g, protein 33.51–39.74 g/100 g, available carbohydrate 0.72–8.73 g/ 100 g, iron 53.33–115.97 mg/100 g and zinc 7.10–12.86 mg/100 g. The level of unsaturated fatty acids was 50.54–67.83%, while n-6:n-3 ratio ranged between 5.80:1.00 and 57.70:1.00, signifying potential nutritional and public health significance. The termites may be exploited to provide high-quality diets especially in the developing countries, which have been plagued by iron and zinc deficiencies as well as poor supply of dietary polyunsaturated fatty acid sources. ß 2013 Elsevier Inc. All rights reserved. Keywords: Entomophagy Edible insects Nutrition Iron Zinc Polyunsaturated fatty acids Food analysis Food composition Biodiversity and nutrition Indigenous food 1. Introduction According to FAO (2010), more than 2.5 billion people, mainly in Africa and Asia, commonly eat insects. Currently attention is being drawn to this valuable traditional food resource, which if tapped or exploited is likely to be a more sustainable solution for nutrient deficiency. Edible winged termites form an important part of the food culture in the Lake Victoria region of East Africa (DeFoliart, 1999; Ayieko, 2007). In many households termites are a delicacy enjoyed by almost all ethnic communities in western Kenya. There are different species of edible winged termites collected for human consumption in western Kenya. Depending on the termite species and season, methods of harvesting vary (Ayieko et al., 2010). In the western Kenya region, termites are collected * Corresponding author at: Department of Food Science and Technology, Jomo Kenyatta University of Agriculture and Technology, P.O. Box 62000-00200, Nairobi, Kenya. Tel.: +254 723667432. E-mail addresses: jkinyuru@gmail.com, jkinyuru@agr.jkuat.ac.ke (J.N. Kinyuru). 0889-1575/$ – see front matter ß 2013 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.jfca.2013.02.008 during the April and October rainy seasons. They are prepared by blanching in boiling water then drying in the sun, and then frying in their own fat. They are consumed as part of a meal or as a complete meal with tapioca, bread, roast corn, or simply eaten as snack food. Some mothers even grind the dried termites into flour and use it as a sprinkle in baby porridge (Bergeron et al., 1988). Termites are also eaten raw directly from the emergence hole (Christensen et al., 2006; Ayieko et al., 2010). Although termite harvest begins with the onset of the rains and the swarming of the winged termites, villagers have shown that some termites could be induced to emerge even during the dry seasons, making them available throughout the year. This has created attachment to the termite enterprise by locals to the extent that in some parts of the region, termite mounds are owned by individuals and sometimes form part of inheritance when one dies (Banjo et al., 2006). It is postulated that termites contain high-quality nutrients including highly digestible proteins (Kinyuru et al., 2010a), as well as minerals, which are more bioavailable than minerals from plant foods (Omotoso, 2006). They may therefore be utilised to manage the widespread nutrient deficiency in developing countries J.N. Kinyuru et al. / Journal of Food Composition and Analysis 30 (2013) 120–124 (FAO/WHO, 2001) practising entomophagy. Most of the literature concerning the comprehensive nutrient composition of insects in western Kenya has focused on other insects such as grasshoppers (Ruspolia differens) [Kinyuru et al., 2010b] and black ants (Calebara vidua) (Ayieko et al., 2012). Christensen et al. (2006) summarised the mineral content of ‘oyala’ ‘ogawo’ and ‘agoro’ termites from Lake Victoria region of Kenya. Another study focused on the culture of harvesting and consuming Macrotermes subhylanus termite in western Kenya (Ayieko et al., 2010). Therefore, this report provides a more comprehensive summary of the proximates, mineral and fatty acid composition of four termite species commonly consumed in western Kenya. 2. Materials and methods 2.1. Sampling design Representative samples of sun-dried M. subhylanus, P. militaris, M. bellicosus and P. spiniger termite species were collected from markets in six major towns namely Maseno, Luanda, Mumias, Bungoma, Webuye and Kakamega. Samples were collected from six vendors in each town during the wet season between April and October in 2010. From each vendor, samples weighing 0.25 to 2 kg of each termite species were obtained. A single sample per town for each species was obtained by pooling 100 g from each vendor. This formed six composite samples for analysis for each termite species representing western Kenya. The samples were packaged in standard gauge polythene bags and stored in cool boxes lined with ice packs. They were transported to the Food Biochemistry laboratory at Jomo Kenyatta University of Agriculture and Technology within 12 h after collection. 121 Japan) according to AOAC (1996) using external standards (Sigma– Aldrich Chemie, Steinheim, Germany). In-house control material was used to determine the precision and accuracy of the results. The in-house control sample was vacuum-packed in polythene bags and stored at 20 8C. The stability of this material was tested regularly. 2.5. Fatty acid composition Fatty acid composition was determined by gas chromatography. The extraction of the lipids was performed by Folch extraction method (Folch et al., 1957). Prior to methylation, the extracted lipid was redissolved to a concentration of 10 mg/mL in chloroform:methanol (2:1, v/v). The samples were methylated according to Bligh and Dyer (1959) and 0.2 mL were injected into the Gas Chromatograph (GC) capillary column (Supelcowax, internal diameter 30 m 0.53 mm) maintained at an injection/ detection temperature of 220 8C under a flame ionisation detector. Identification of the fatty acid methyl esters was by comparison of retention times with standards (Sigma Chemical Co) and was expressed as percentages of total methyl esters The polyunsaturated fatty acids/saturated fatty acids ratio (PU/SA) and n-6:n-3 fatty acids ratios were calculated (Mann, 1993; Nurhasan et al., 2010). 2.6. Data analysis Data were reported as mean standard deviation for each termite species. 3. Results and discussion 2.2. Sample preparation and analysis 3.1. Proximate composition Once in the laboratory, the composite samples were dewinged and moisture content determined. The rest of the samples were freeze-dried, homogenized and stored at 20 8C for further analysis. All the reagents for analysis were of analytical grade. Table 1 shows the proximate composition of the edible termites. Moisture content for termites was found to be 6.50– 8.76 g/100 g, values which were higher than those reported in National Food Composition Tables for Kenya (NFCT) [Sehmi, 1993] for sun-dried termite consumed in western Kenya (1.70 g/100 g). The level of moisture content in any dried food is highly dependent on the drying environment among other factors. Some of the foods are dried on bare ground; water may therefore accumulate around it instead of draining away during the drying process making the drying process cumbersome (Owaga et al., 2010). These are some of the reasons why there may have been a difference in the moisture content observed between the species. The fat content of the termites (44.82–47.31 g/100 g) was lower than the values reported in NFCT (Sehmi, 1993) for sun-dried termite (53.40 g/100 g) but higher than the values reported for other termite species studied by Banjo et al. (2006) (19.70–24.10 g/ 100 g) in Nigeria. The values of the studied termites were also higher than that of Nausitermes spp. termite (40.23 g/100 g) reported by Oyarzun et al. (1996). The protein content of the four termite species (33.51–39.74 g/ 100 g) was within the range reported for dried termite (35.70 g/ 100 g) reported in the NFCT (Sehmi, 1993). The protein content 2.3. Proximate composition Moisture content was analysed by the drying method, crude fat by Soxhlet extraction method and crude protein by semimicro-Kjeldhal method (AOAC, 1996). Protein content was calculated by utilising 6.25 as the protein: nitrogen ratio. Crude ash was determined by incinerating in a muffle furnace at 550 8C (AOAC, 1996). Dietary fibre was determined by enzymatic gravimetric method – Prosky (AOAC, 1995). Available carbohydrate value was calculated as the difference between 100 and the sum of the percentages of water, protein, lipids, ash and dietary fibre. 2.4. Iron, zinc and calcium content Quantification of iron, zinc and calcium was performed by atomic absorption spectrometry (AAS) (Shimadzu AA-6200, Tokyo, Table 1 Proximate composition of the edible winged termites (g/100 g). Termite Moisture Proteina Fata Total asha Dietary fibrea Available carbohydratea Macrotermes subylanus; dewinged Pseudacanthotermes militaris; dewinged Macrotermes bellicosus; dewinged Pseudacanthotermes spiniger; dewinged 6.50 0.02 5.04 0.15 5.13 0.18 8.76 1.61 39.34 0.12 33.51 0.85 39.74 0.61 37.54 0.12 44.82 2.89 46.59 2.13 47.03 1.04 47.31 0.13 7.58 0.05 4.58 0.06 4.65 0.09 7.22 0.38 6.37 1.18 6.59 0.07 6.21 2.04 7.21 0.44 1.89 0.76 8.73 1.87 2.37 0.98 0.72 0.01 Values are mean SD; n = 6. a Values are on dry weight basis. J.N. Kinyuru et al. / Journal of Food Composition and Analysis 30 (2013) 120–124 122 Table 2 Mineral composition of the edible winged termites (mg/100 g). Iron fibre and some definitions include chitin as dietary fibre (Michaelsen et al., 2009). Termite Calcium Zinc Macrotermes subylanus; dewinged Pseudacanthotermes militaris; dewinged Macrotermes bellicosus; dewinged Pseudacanthotermes spiniger; dewinged 58.72 1.29 53.33 1.46 8.10 2.80 48.31 7.09 60.29 1.11 12.86 0.92 63.60 6.53 115.97 3.46 10.76 1.93 42.89 1.75 64.77 2.66 7.10 1.82 Values are mean SD on dry weight basis; n = 6. exhibited by the termites in this study was higher than that of red meats reported by Williams (2007) and therefore they may offer an affordable source of protein. Other studies have reported that termites have high protein quality beneficial for human nutrition (Ramos-Elorduy et al., 1997; Verkerk et al., 2007; Kinyuru et al., 2010a), especially in an otherwise plant-dominated diet, typical in western Kenya The ash content of the studied termites (6.21–7.21 g/100 g) was higher than values reported for dried termite (4.80 g/100 g) in NFCT (Sehmi, 1993). The higher ash content in the termites may be due to residual soil contamination during harvesting and drying although care was taken to avoid soil contamination after sampling. Sorting is however a procedure to remove any visible soil, dust and other physical contaminants before analysis of such food samples. The carbohydrate content of the studied termites (0.72–8.73 g/100 g) was within the range of the value reported for dried termite (3.50 g/100 g) according to NFCT (Sehmi, 1993). However, carbohydrate in insects, including termites, has been reported in a highly variable range of 1.00–29.00 g/100 g of dry weight (Verkerk et al., 2007). This variability is evident among the species analyzed (0.72–8.73 g/100 g) in this study. The dietary fibre content of the studied termites was 6.21–7.21 g/100 g, however, there are no fibre values in NFCT (Sehmi, 1993) reported for sun-dried termite to compare with. Various authors have suggested that the fibre in insects represents chitin because it is similar structurally to cellulose (Finke, 2002, 2007; Barker et al., 1998). Therefore, high fibre content in insects may be due to chitin. However, there is no universally accepted definition of dietary 3.2. Calcium, iron and zinc Calcium, iron and zinc content were the minerals of interest as shown in Table 2. M. bellicosus termite had the highest calcium and iron content while P. militaris termite had the highest zinc content. The NFCT (Sehmi, 1993) reports calcium and iron contents of dried termite species to be 91.00 mg/100 g and 21.00 mg/100 g respectively. Values for zinc content are missing completely from the NFCT (Sehmi, 1993). The levels of calcium, iron and zinc of the insects obtained in this study are in agreement with previous studies on termites (Oyarzun et al., 1996; Christensen et al., 2006; Onigbinde and Adamolekun, 1998). However there was wide variability in iron content between M. bellicosus (115.97 mg/100 g) and the other species analyzed (53.33–64.77 mg/100 g). This difference could be attributed to species difference as well as possible soil contamination during harvesting. However, this variability deserves further investigation. Consumption of soil especially from termite moulds in western Kenya is a common practise (Geissler et al., 1997) and so possibility of insect contamination with soil does not hinder local consumption. Contrary to the high zinc and iron contents in insects, calcium content has been reported to be relatively low in other termite species as well as in other insects (Oyarzun et al., 1996; Onigbinde and Adamolekun, 1998; Kinyuru et al., 2010a; Banjo et al., 2006; Ekpo and Onigbinde, 2007). Of specific importance while focusing on the nutritional significance from edible insects is the contribution of micronutrients, which are well documented to be deficient and causing severe public health problems in poor populations in Kenya (Hongo, 2003). Deficiencies of iron and zinc are core public health problems, especially for child and maternal health (Michaelsen et al., 2009). Reports on contents of zinc and iron in various insects generally indicate that insects are a valuable source of these minerals (Yhoungaree et al., 1997; Christensen et al., 2006). In addition, Christensen et al. (2006) suggests that bioavailability of these minerals from the insects is likely to be higher than from the plant foods. Therefore, cereal-based diets used for feeding infants Table 3 Fatty acid composition of the edible winged termites. Fatty acid (% of total lipids) Macrotermes subylanus Pseudacanthotermes militaris Caprylic acid (C10:1) Capric acid (C10:0) Lauric acid (C12:0) Myristic acid (C14:0) Palmitic acid (C16:0) Palmitoleic acid (C16:1) Stearic acid (C18:0) Oleic acid (C18:1) Linoleic acid (C18:2) Linolenic acid (C18:3) Total saturateda Total unsaturatedb Monounsaturatedc Polyunsaturatedd PU/SA ratio n-6: n-3 nd nd nd 1.06 0.04 27.65 3.53 4.17 0.40 6.34 0.04 48.60 3.59 10.75 0.66 1.43 0.13 35.05 0.89 64.95 0.94 52.77 0.22 12.18 2.13 0.34 0.24 7.50: 1.00 nd 0.21 0.04 nd nd 26.04 2.34 5.84 0.30 5.92 0.48 50.26 1.60 11.54 0.44 0.20 0.02 32.17 0.57 67.83 0.50 56.10 0.63 11.73 0.30 0.36 0.05 57.70: 1.00 All values as means SD on dry weight basis; n = 6. nd – not detected. Limit of detection = 0.05% of total lipid. a Sum total percentage of 10:0, 12:0, 14:0, 16:0, 18:0. b Sum total percentage of 16:1, 18:1, 18:2, 18:3. c Sum total percentage of 16:1, 18:1. d Sum total percentage of 18:2, 18:3. Macrotermes bellicosus 0.42 0.25 0.24 0.05 0.18 0.09 1.16 0.15 38.35 3.37 0.63 0.05 9.53 0.54 41.74 2.61 5.03 0.12 0.87 0.01 49.46 0.29 50.54 0.23 44.64 0.28 5.90 0.15 0.12 0.05 5.80: 1.00 Pseudacanthotermes spiniger 0.39 0.02 0.31 0.01 0.22 0.01 0.76 0.01 28.04 0.12 3.24 0.02 6.12 0.10 49.27 0.02 10.48 0.08 0.78 0.05 35.84 0.04 64.16 0.04 52.90 0.02 11.26 0.07 0.31 0.02 13.40: 1.00 J.N. Kinyuru et al. / Journal of Food Composition and Analysis 30 (2013) 120–124 and young children in developing countries could receive a boost with the addition of insects to the diets. 3.3. Fatty acid composition The results presented in Table 3 show that all termite oils contained more unsaturated fatty acids than polyunsaturated fatty acids (PUFA). Oleic acid was the predominant fatty acid in the lipid fraction of the studied termite species (41.74–50.26%), palmitic acid was the second major fatty acid (26.04–38.85%), and linoleic acid was third (5.03–11.54%). Oyarzun et al. (1996) reported that oleic acid was the major fatty acid (51.10%) in Nasutitermes spp. of termites collected in Venezuela. In addition, Ekpo and Onigbinde (2007) found that oleic and palmitic acids are the major fatty acids in Macrotermes bellicosus termite oil. The findings of this study therefore correlated well with other studies. Other researchers have reported significant amounts of linolenic and linoleic acids (DeFoliart, 1991; Ekpo and Onigbinde, 2007). Oil from M. subhylanus species had higher content of n-3 fatty acids (1.43%of total lipids) as compared to the other species analyzed. P. Militaris contained the lowest amount of n-3 fatty acids (0.20%) but relatively high concentrations of n-6 fatty acids (11.54%). The n-6:n-3 ratios ranged between 5.8:10 and 57.7:10 in the termites analyzed. P. militaris had a marginally high n-6:n-3 ratio (57.70:10), while M. bellicosus had the lowest (5.80:10). Based on n-6:n:3 ratio, the termites offer high-quality fat for the human diet among the communities practising entomophagy. The Codex recommendation for a n-6:n-3 ratio is between 5.00 and 15.00:1.00 in infant formula (Koletzko et al., 2005) and therefore the termites maybe a moderate source of n-3 fatty acids which have been associated with human growth and health implications (Michaelsen et al., 2011). PU/SA ratio under 0.20 has been associated with high cholesterol level and high risk of coronary heart disorders (Mann, 1993). All the insects analyzed had PU/SA ratios above 0.20 except M. bellicosus termite. Oyarzun et al. (1996) reported a PU/SA ratio of 0.20 for Nasutitermes spp. of termite from Venezuela, while Ekpo and Onigbinde (2007) reported a PU/SA ratio of 0.80 for a Macrotermes spp. of termite from Nigeria. The PU/SA ratios of >0.20 for most of the termites analyzed suggest that the insects can be associated with a lower risk for certain coronary heart diseases. 4. Conclusion This study provides an overview of the nutrient composition of selected termites in western Kenya. The termites contain significant proportions of proteins, fats and minerals. The oil is of high quality with significant contribution of n-3 fatty acids and hence possible nutritional significance. The termites have unique nutrition qualities that can be exploited to provide high-quality diets, especially in the developing countries, which have been plagued by iron and zinc deficiencies as well as poor supply of dietary polyunsaturated fatty acid sources. 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