Key words: spirulina, carotene, absorption, liver vitamin A, plasma vitamin A, rats
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1 Plant Foods for Human Nutrition 41: , Kluwer Academic Publishers. Printed in the Netherlands. Spirulina as a source of vitamin A V.V. ANNAPURNA, Y.G. DEOSTHALE & MAHTAB S. BAMJI* National Institute of Nutrition, Indian Council of Medical Research, Jamai Osmania P.O., Hyderabad-5 7, India (*author for correspondence) Received 3 July 199; accepted with minor revisions 15 October 199 Key words: spirulina, carotene, absorption, liver vitamin A, plasma vitamin A, rats Abstract. Experiments were carried out to assess spirulina fusiformis - a blue green algae as a source of vitamin A in rats. In one experiment, the control rats were fed synthetic vitamin A and the experimental rats spirulina as the sole source of vitamin A. The liver vitamin A concentration of spirulina-fed rats of both sexes was found to be significantly higher than that of the control rats. In another experiment the absorption of carotenes from the solvent extract of spirulina and their availability (vitamin A value) as judged by the levels of vitamin A and carotene in plasma and liver were compared with those of synthetic fl-carotene or vitamin A in male rats. The absorption of fl-carotene from spirulina extract tended to be lower than that of crystalline fl-carotene at doses of 55 and 11#g of fl-carotene. The difference became insignificant at lower fl-carotene dose of 275/~g. Spirulina carotene-fed rats did not show a strict dose related increase in the liver or serum vitamin A concentration. The liver vitamin A storage and plasma levels of vitamin A of spirulina carotene-fed rats was much higher than expected. The results of the two studies reported suggest that the algae spirulina can be a valuable source of vitamin A. Introduction The blue green algae Spirulina fusiformis has been considered to be a good source of protein. It has been widely used as a health food with claims of numerous health benefits. Spirulina is a rich source of provitamin A carotenes like fl-carotene. Thus, freshly harvested and spray-dried spirulina (supplied to us by the Murugappa Chettiar Research Centre, Madras, India) has been found to contain 4 mg total carotene and 2 mg/%carotene per gram algal powder. Diets of populations in developing countries like India are qualitatively adequate in proteins, but markedly deficient in micronutrients particularly vitamin A and riboflavin. Thus, while the protein requirement can be met in the process of meeting calorie requirement, the requirement for vitamin A and riboflavin would not be met from the traditional cereal-legume-based diets even if the calorie gap is bridged.
2 126 Green leafy vegetables are the main source of vitamin A in the diets of the poor who cannot afford vitamin A-rich foods of animal origin. The production of vegetables in most developing countries is inadequate to meet the nutritional demands of the population. In this context, spirulina with such high concentration of//-carotene can be a good alternative source of vitamin A. The present investigation was carried out in rats to assess the potential of spirulina as a source of vitamin A. Materials and methods All the solvents and chemicals used in the study were of the highest purity available. Spirulina was obtained from the Murugappa Chettiar Research Centre, Madras, India. The carotene content of the spirulina varied with the batch used. Two experiments were carried out. In both the experiments, weanling rats of Wistar/NIN strain were used. Experiment 1 Fourteen male and!4 female rats were divided equally into control and experimental groups. Both the groups received a diet containing 2% vitamin-free casein, 64% starch, 1% oil, 1% vitamins and 5% minerals [1, 2]. The control group received 137 #g retinyl palmitate per 1 gm diet. Vitamin A was deleted from the diet of the experimental group. This group received 1.27% spirulina in the diet. Since this sample of spirulina was not a fresh sample, it contained only.72mg of total carotene and.22mg of//-carotene per gram of spirulina in 1 gram of diet. This level of spirulina supplementation would provide 24 #g of vitamin E,.8 g of protein and 46mgs of fat in 1 gm diet. Since these quantities are negligible, no additional allowance was made in the diet of the control group of rats, even though these nutrients are known to play a role in the absorption of//-carotene. The efficiency of//-carotene conversion to vitamin A was assumed to be 5% on weight basis, i.e. one mole of vitamin A per mole of //-carotene. Respective diets were fed (ad lib) for 8 weeks. At the end of this period, a sample of blood was drawn with heparinized capillary tubes from the ocular plexus and the rats sacrificed. Plasma and liver were analyzed for vitamin A and carotene. Experiment 2 In this experiment the absorption of solvent-extracted carotenes from spirulina and their availability as judged by the plasma and liver vitamin A
3 127 and carotenes were examined in vitamin A-depleted male rats. The results were compared with rats treated with synthetic//-carotene or vitamin A. The solvent extract of spirulina was prepared by saponifying spray-dried spirulina powder with alkaline ethanol and extracting the carotenes in (6-8~ petroleum ether. The petroleum ether extract was washed with water to remove traces of alkali. The extracts were concentrated by flash evaporation and total carotenes estimated by measuring the absorbance at 45nm in a Schimadzu spectrophotometer using ~l~l~176 value of 25. The /~-carotene fraction of the sample was quantified after chromatographic separation of the petroleum ether extract of carotenes on alumina column [3]. For feeding purposes the petroleum ether extract of Spirulina was evaporated under vacuum using a flash evaporator and reconstituted in appropriate amount of arachis oil. The rats were fed this reconstituted extract orally at the doses mentioned later. Weanling male Wistar]NIN rats were fed a vitamin A-deficient diet for a period of 8 weeks. The composition of the diet was similar to that of experiment 1, exception being the deletion of vitamin A from the vitamin mixture. At the end of this period, the animals were divided in six groups and were given oral supplements daily as follows: Group 1 - no supplement; Group #g vitamin A; Group 3-11/~g //-carotene; Group 4 - spirulina extract containing 27.5#g //-carotene and 45.8#g total carotene; Group 5 - spirulina extract containing 55#g //-carotene and 91.6#g total carotene, and Group 6 - spirulina extract containing 11pg//-carotene and #g total carotene. The vitamin A,//-carotene and spirulina carotene supplements were fed orally in arachis oil (.2 ml per day) for a period of 1 days. Faecal matter was collected daily during the 1 days of supplementation. At the end of this supplementation period all the animals were sacrificed after drawing a sample of blood with heparinized capillary tubes from the ocular plexus. Liver, plasma and pooled faecal samples were analysed for vitamin A, total carotenes and//-carotene. Measurement of liver, plasma and faecal vitamkz A and carotenes Liver was processed according to the method of Ames et al. [4]. Vitamin A was extracted with diethyl ether and measured using the colorimetric method of Tievs and Zentz [5]. Plasma vitamin A was also measured colorimetrically [5] after saponifying the plasma with alcoholic potassium hydroxide and extracting vitamin A into diethyl ether. For the measurement of carotenes in plasma, the diethyl ether extract after evaporating to dryness
4 128 was reconstituted in petroleum ether. Carotene in this extract was measured by taking the absorbance at 45 nm in a spectrophotometer and applying the EIO/o lena of 25 [3]. Powdered faecal matter was saponified and extracted with petroleum ether. Carotene content of the extract was measured spectrophotometrically. The fl-carotene fraction of the sample was quantified after chromatographic separation of the petroleum ether extract on alumina column [3]. Statistical analysis of the data was done by using analysis of variance and Duncan's multiple range test. Results Experiment 1 The spirulina-fed male as well as female rats which received 274#g flcarotene per 1 g diet through spirulina, showed significantly higher weight gain than the control group which received 137 #g vitamin A per 1 g diet. Food intake was similar in the vitamin A-fed control and spirulina-fed rats and hence the feed efficiency of the spirulina-fed male aswell as female rats was significantly higher than that of the control rats (Table 1). The liver vitamin A concentration of spirulina-fed rats was significantly higher than that of control rats. However, the plasma vitamin A levels were similar in the two groups. The plasma carotene levels were higher in the spirulina-fed rats compared to controls. The liver carotene concentration was higher only in spirulina-fed male rats, but not in the female rats compared to the corresponding controls (Table 2). Experiment 2 Data in Table 3 show that the absorption of crystalline fl-carotene was 93%. The absorption of fl-carotene from spirulina extract varied from 88.8% at the lowest dose to 82.9% at he highest dose. The two higher dose values were significantly lower than the crystalline fl-carotene-fed group (Table 3). The liver vitamin A of rats fed 11 #g crystalline fl-carotene over 1 days was about four times higher than that of rats fed 147 #g vitamin A over 1 days (Table 4). This suggests that the vitamin A values of crystalline fl-carotene in rats is approximately 5% of that of vitamin A on weight basis assuming a dose linearity for vitamin A storage. The liver vitamin A content and plasma levels of vitamin A of spirulina carotene-fed rats was much higher than expected. Thus the rats which received 11 #g/3-carotene from spirulina showed mean liver storage of 876 #g per liver whereas rats which
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8 m 132 Table 4. Liver and plasma vitamin A status of rats fed carotene from extract of spirulina* Treatment Total carotene fl-carotene Vitamin A intake intake #g/1 days #g/1 days Plasma Liver #g/1 ml #g/liver Control Vitamin A fed (147 #g/1 days) //-carotene (11#g/1 days) Spirulina carotenes a _.97 b b _ bd _ 2.19 ~d _ 4.31 c _ ~ 9.66 b _ c c c 78.8 d, Values are mean +_ SEM. Data analysed by analysis of variance and Duncan's range test. Values sharing even one common superscript are statistically not signficant. Number in parentheses denotes the number of animals used. multiple received 11/~g of crystalline//-carotene showed liver stores of only 43/~g. Between the three spirulina carotene-fed groups, a strict dose-related increase in liver and plasma vitamin A was not apparent. Group 5 which received 55#g of //-carotene (916#g of total carotene) from spirulina extract, had only slightly higher liver stores of vitamin A than group 4 which received 275 #g of fl-carotene (458 #g total carotene) (Table 4). The carotene levels in plasma and liver were negligible. Discussion In the first experiment, while the control rats received 137 #g of vitamin A per 1 g diet, the experimental rats received 274 #g of//-carotene and 923/~g of total carotene through spirulina per 1 g diet. The liver stores of vitamin A in spirulina-fed animals were more than two-fold higher than the control rats, though plasma levels in the two groups were comparable. These results suggest that the vitamin A potency of spirulina is greater than what can be expected from its//-carotene contents assuming a molar conversion ratio of one. This cannot be entirely explained on the basis of vitamin A activity of some of the other carotenoid pigments present in spirulina. The results of the second experiment where solvent extract of spirulina instead of algal powder was fed revealed a similar trend.
9 133 Several other workers in the past have examined the availability of carotenes from plant sources as judged by their absorption and recovery as retinol in the liver of rats. According to one recent study the availability of carotene from carrots as measured by liver and kidney stores of vitamin A was equal to that of all-trans /%carotene dissolved in cottonseed oil [6]. However, despite similar liver and kidney storage values, the faecal excretion of carotenes in rats receiving carrots was much higher than in animals receiving crystalline fl-carotene. This suggests a more efficient conversion to vitamin A of the absorbed fl-carotene from carrots as compared to crystalline fl-carotene - an observation similar to that of spirulina carotenes. In another study, carotenes extracted from the algae Dunaliella bardawil were found to get absorbed and recovered as retinol in the liver of rats in a proportion similar to that of commercial fl-carotene. However, the vitamin A value cf algal carotenes diminished at higher doses, perhaps due to interference by the xanthophylls and chlorophylls present in the algae [7]. The marginal reduction in fl-carotene absorption at higher doses of spirulina extract (experiment 2) may also be due to such interference from other carotenes present in spirulina extract. In conclusion the results of the two studies reported suggest that the algae spirulina can be exploited as a valuable source of vitamin A. Acknowledgements The authors are grateful to Dr. Vinodini Reddy, Director, National Institute of Nutrition, Hyderabad, for her interest and encouragement. Also thanks are due to Dr. B. Sivakumar, Assistant Director, National Institute of Nutrition, Hyderabad for useful discussions. The financial assistance given for the project by the Murugappa Chettiar Research Centre, Madras India, is gratefully acknowledged. Also the stimulating discussion held with Dr. C.V. Seshadri (Director) and Mr. Seshagiri of the Murugappa Chettiar Research Centre, Madras is appreciated. References 1. Horwitz W, Chichilo P, Clifford PA, Reynolds H (1965) In: Official Methods of Analysis of Official Agricultural Chemists, AOAC, Washington, D.C., 1th edn., pp Campbell JA (1965) In: Report of an International Conference on Protein Malnutrition. Food and Nutrition Board, National Academy of Sciences, National Research Council, Washington D.C., Publicaion No. 11, pp Arroyave G, Chichester CO, Fores H, Glover J, Mejia LA, Olson JA, Simpson KL, Underwood BA (1982) In: Biochemical Methodology for the Assessment of Vitamin A
10 134 Status - A Report of the International Vitamin A Consultative Group, Chapter IX, pp Ames SR, Risely HA, Harris PL (1954) Simplified procedure for extraction and determination of vitamin A in liver. Anal Chem 26: Tievs J, Zentz C (1967) Die mikrobestimmung Von vitamin A in blut serum and leber punktalenmit Fecl 3 in acetyl chloride. Int J Vit Nutri Res 37: Sweeney JP, Marsh AC (1974) Liver storage of vitamin A by rats fed carrots in various forms. J Nutr 14: Mokady S, Cogan U (1988) Nutritional evaluation of a protein concentrate and of carotenes derived from Dunaliella bardawil. J Sci Food Agric 42:
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