Spirulina platensis,a super food?

Abstract

Spirulina platensis, a multicelluar, photosynthetic prokaryote (algae) contains a high amount of proteins, vitamins and minerals superior to many foods as e.g. soybeans. Thus, Spirulina platensis was recognized as nutritious food by the United Nations World Food Conference. Due to the high amount of nutritive ingredients Spirulina has a long history as dietary supplement. In addition, spirulina platensis is also efficiently used as forage with known effects on flesh, egg and plumage color, milk yield and fertility. The versatile utilization of the alga can be explained on the one hand with the nutrient levels and on the other hand with recognized effects as anti-viral, anti-bacterial, anti-oxidant, anti-diabetic, anti-cancer and anti-inflammatory substance. Therefore, this alga is named as “superfood”. Beyond, these algae convert carbon dioxide into organic substances and produce oxygen during their growth in alkaline and saline water thereby not wasting fresh water allowing the production in barren areas.

Despite this diverse use of Spirulina platensis due to its beneficial properties, many basic mechanisms on a molecular and cellular level are not well understood and should be explored in future studies.

Keywords

Spirulina health effects dietary supplements liver protection virus infection HIV nutrition animal feeding

1 Background

Compared to other foods or by weight, Spirulina is recognized as one of the most nutritious foods on the planet: high in proteins, containing all essential amino acids, also high in B vitamins, iron, magnesium, potassium and many other vitamins and minerals, as well as antioxidants. Therefore, spirulina was declared by the United Nations World Food Conference already in 1974 as the best food for the future.

Spirulina platensis is a multicellular blue-green microalga (prokaryote) (length: 50–500 μm, width: 3–4 μm) belonging to the phylum Cyanophyta (Cyanobacteria). Its name derives from the nature of its filaments, characterized by cylindrical, multicellular trichomes in an open left-handed helix. Taxonomically, “Spirulina” describes mainly two species of Cyanobacteria, Arthrospira platensis and Arthrospira maxima. Both have been used as food, dietary supplement, and feed supplement [1]. These and other Arthrospira species forming helical trichomes were once classified into a single genus, Spirulina [2]. Before this classification by Geitler et al., depending on the presence of septa, the two genera were placed separately: The Spirulina species being without septa and the Arthrospira species with septa. Recent morphological, physiological, and biochemical studies have shown that these two genera are distinctively different and that the edible forms commonly referred to as Spirulina platensis have little in common with other much smaller species. This distinction has been also based on results from the complete sequence of the 16S ribosomal RNA gene and the internal transcribed spacer (ITS) between the 16S and 23S rRNA genes determined for two Arthrospira strains and one Spirulina strain [3] showing that the two Arthrospira strains formed a close cluster distant from the Spirulina strain. Habitats for Spirulina include the Pacific Ocean near Japan and Hawaii, and large freshwater lakes, including Lake Chad in Africa, Klamath Lake in North America, Lake Texcoco in Mexico, and Lake Titikaka in South America.

Spirulina has long been used as a dietary supplement by people living close to alkaline lakes where it is naturally found. It was used as food in Mexico by the Aztecs and other Mesoamericans until the 16th century. One of Hernan Cortés’ soldiers described the harvest of algae at the lake Texcoco and the sale as cakes called “tecuitlatl” [4 –6]. It has and is still being used as food by the ethnic group of Kanembu at the lake Chad area of the Republic of Chad where it is sold as dried bread called “dihe” [7]. This traditional food was rediscovered in Chad by a European scientific mission and is now widely cultured throughout the world with gained popularity in the human health food industry. In many African countries it is collected from natural water, dried and eaten, as a major source of protein and in many countries of Asia it is used as protein supplement and as health food. Spirulina has been used as a complementary dietary ingredient of feed for fish, shrimp and poultry, and increasingly as a protein and vitamin supplement to aquafeeds.

2 Biochemical composition

Spirulina has high quality protein content (55–70 percent of the dry weight), which is more than other commonly used plant sources such as dry soybeans (35 percent), peanuts (25 percent) or grains (8–10%). The biochemical composition of Spirulina can be summarized as follows [5]:

2.1 Proteins

Spirulina contains unusually high amounts of protein, between 55 and 70 percent by dry weight, depending upon the source [8]. It is a complete protein, containing all essential amino acids, though with reduced amounts of methionine, cystine, and lysine, as compared to standard proteins such as that from meat, eggs, or milk; it is, however, superior to all standard plant protein, such as that from legumes.

2.2 Essential fatty acids

Spirulina has a high amount of polyunsaturated fatty acids (PUFAs), 1.5–2.0 percent of 5 - 6 percent total lipid. In particular, Spirulina is rich in γ-linolenic acid (36 percent of total PUFAs), and also provides α-linolenic acid (ALA), linoleic acid (LA, 36 percent of total PUFAs), stearidonic acid (SDA), eicosapentaenoic acid (EPA), docosahexaenoic acid (DHA) and arachidonic acid (AA).

2.3 Vitamins

Spirulina contains vitamin B1 (thiamine), B2 (riboflavin), B3 (nicotinamide), B6 (pyridoxine), B9 (folic acid), B12 (cyanocobalamin), vitamin C, vitamin D and vitamin E.

2.4 Minerals

Spirulina is a rich source of potassium, and also contains calcium, chromium, copper, iron, magnesium, manganese, phosphorus, selenium, sodium and zinc.

2.5 Photosynthetic pigments

Spirulina contains many pigments including chlorophyll a, xanthophyll, beta-carotene, echinenone, myxoxanthophyll, zeaxanthin, canthaxanthin, diatoxanthin, 3-hydroxyechinenone, beta-cryptoxanthin, oscillaxanthin, plus the phycobiliproteins c-phycocyanin and allophycocyanin.

The detailed biochemical composition of Spirulina may vary according to the growing conditions especially in response to the salinity of the growing medium; it grows in fresh water (pH 7) but also in highly alkaline environments (pH 9–11) of tropical and subtropical areas [9, 10]. Vonshak et al. [11] reported that salt-adapted cells had a modified biochemical composition with a reduced protein and chlorophyll content, and increased carbohydrate content. In addition, algae produced under laboratory conditions differ from those collected in natural environment or in mass culture systems using different agro-industrial waste effluent.

Nowadays, Spirulina is produced in at least 22 countries: Benin, Brazil, Burkina Faso, Chad, Chile, China, Costa Rica, Côte d’Ivoire, Cuba, Ecuador, France, India, Madagascar, Mexico, Myanmar, Peru, Israel, Spain, Thailand, Togo, United States of America, Taiwan and Vietnam [5]. About 1000 tons are produced in algae farms in the USA, Hawaii, Mexico, South America. However, production in China was first recorded at 19,080 tons in 2003 and rose sharply to 41,570 tons in 2004. Unfortunately, a full monitoring of worldwide production is lacking [5, 12].

The production mostly takes place under controlled conditions, so that toxic components (from other blue-green algae), pesticides or heavy metal pollution are largely excluded. However, there is an unmet role for national governments — as well as intergovernmental organizations like UN or FAO — to evaluate the potential of spirulina to fulfill food security needs.

The general composition of spirulina varies by location and type of production, but is approximately as follows:

Proteins	55–70%
Carbohydrates	15–25%
Lipids	6–8%
Minerals	7–13%
Humidity (dried algae)	3–7%
Dietary fibers	8–10%

Remarkable on the one hand is the high proportion of proteins and on the other hand of essential fatty acids (especially the polyunsaturated fatty acid gamma-linolenic acid) of 1.3% [13]. The high protein content consists of eight essential amino acids (isoleucine, leucine, lysine, methionine, phenylalanine, threonine, tryptophan, valine) as well as the non-essential amino acids (alanine, arginine, aspartate acid, cystine, glycine, histidine, proline, serine, tyrosine, and glutamic acid) [14].

In addition, spirulina contains almost all the essential vitamins. The following table indicates the vitamin content in 10 g spirulina.

Vitamin A	23000 IU	Vitamin B1	0.35 mg
β-Carotene	14 mg	Vitamin B2	0.40 mg
Vitamin C	0.8 mg	Vitamin B3	1.4 mg
Vitamin D	1200 IU	Vitamin B6	60 μg
Vitamin E	1.0 mg	Folic acid	1.0 μg
Vitamin K	200 μg	Vitamin B12	20.0 μg
Biotin	0.5 μg	Pantothenic acid	10.0 μg
Inositol	6.4 mg

10 g Spirulina contain the following amount of minerals [15]:

Calcium	70 mg	Manganese	0.5 mg
Iron	15 mg	Chrome	25 μg
Phosphorus	60 mg	Molybdenum	–
Iodine	55 μg	Chloride	–
Magnesium	40 mg	Sodium	90 mg
Zinc	0.3 mg	Potassium	140 mg
Selenium	10 μg	Germanium	60 μg
Copper	120 μg	Boron	–

The amount of natural pigments in Spirulina is extremely high. Spirulina consists of 14% phycocyanin (blue pigment), 1% chlorophyll (green pigment) and 0.5% carotenoids (yellow, orange, or red pigments). All vital substances in Spirulina have a high bioavailability; that is, they can absorb optimally and without much loss. On the one hand, all nutrients are balanced and, on the other hand, these microalgae species are - in contrast to other algae - only enclosed by a typical Gram-negative cell wall consisting mainly of peptidoglycan which can easily be absorbed by the human body (digestibility of 86% [16]) and does not require chemical or physical processing in order to become digestible [17].

The current use of this resource has four precedents: tradition, scientific and technological development, and the so-called, “green tendency” [18]. From 1970, the nutritional and medicinal studies on Spirulina have steadily increased [19]. From the last 20 years, there are a number of studies that make it suitable for use as a feed, or even as a drug in veterinary medicine [20, 21]. This was already indicated by the analysis of the ingredients: chlorophyll, phycobiliproteins (phycocyanin, allophycocyanin, phycoerythin), carotenoids like β-carotene and various xanthophylls (zeaxanthin, echinenone, canthaxanthin, cryptoxanthin, myxoxanthophyll), cyanophycin and starch-like compounds (cyanophycean starch) [22].

Aware of theses aspects, the World Health Organization predicts that spirulina will become one of the most curative and prophylactic foods in the twenty-first century.

3 Health effects of spirulina

A lot of studies on spirulina have been performed as an alternative feed for animals (see review in [5]). Spirulina can be fed up to 10% for poultry [23]. An increase in the spirulina content up to 40 g/kg for 16 days in 21-day-old broiler male chicks, resulted in yellow and red coloration of flesh may be due to the accumulation of the yellow pigment, zeaxanthin [24]. Similar to poultry, pigs and rabbits can also receive up to 10% of the feed [25, 26]. In cattle, an increase of the spirulina content resulted in an increased milk yield and weight [26, 27]. Spirulina as an alternative feedstock and immune booster for big-mouth buffalo [27], milk fish, cultured striped jack [29], carp [30], red sea bream [31], tilapia [32], catfish [33], yellow tail [34], zebrafish [35], shrimp [36, 37], and abalone [38] was established with a safely recommendation of up to 2% spirulina per day in aquaculture feed [5].

In basic studies different biological and health effects have been described (see Fig. 1).

Fig.1

Reported biological and health effects of Spirulina.

3.1 Anti-bacterial and anti-viral activity of Spirulina

Spirulina exhibits potent anti-bacterial activities against pathogenic bacteria [39 –42]. Administration of 0.1% Spirulina resulted in heightened bacterial clearance (E. coli & S. aureus) 30 minutes post-injection with almost negligible bacterial counts in the blood. This heightened bacterial clearance was attributed to the immune-potentiating effects of Spirulina [43]. The methanol extract of S. platensis showed more potent anti-microbial activity than dichloromethane, petroleum ether, ethyl acetate extracts and volatile anti-bacterial components [39].

In lower concentrations Spirulina reduced viral replication while blocking the replication of viruses at higher concentration. In addition, it could be shown that water soluble extract of Spirulina inhibited viral cell-penetration and replication of the Herpes Simplex Virus Type 1 (HSV-1) in cultured HeLa cells in a dose dependent manner. At just 1 mg/ml, the extract is shown to inhibit viral protein synthesis without suppressing host cell functions. Spirulina fed hamsters had prolonged survival times and higher survival rates when challenged with the HSV-1 [44]. The anti-viral activity was attributed to sulphated polysaccharide termed “Calcium Spirulan” (Ca-Sp), which has been shown to inhibit replication of many enveloped viruses by inhibition of viral penetration into target cells without host toxicity. Presently, Ca-SP has been shown to exhibit activity against human cytomegalovirus, measles virus, mumps virus, influenza A virus, human immunodeficiency virus (HIV-1) as well as HSV-1 [44]. The active Ca-Sp could be a good candidate for therapeutic intervention against HIV-1 and other viruses because of its low anticoagulant activity, long half-life in the blood, and dose-dependent bioactivity [46 –48].

3.2 Detoxification of toxic minerals

Spirulina has a unique quality to detoxify (neutralize) or to chelate toxic minerals, a characteristic that is not yet confirmed in any other microalgae [49, 50]. Spirulina can be used to detoxify arsenic from water and food. At the Beijing University bioactive molecules from spirulina have been extracted which could neutralize or detoxify toxic and poisonous effect of heavy metals, and which showed anti-tumor activity. Therefore, spirulina could also be used to chelate or detoxify the poisonous effect of heavy metals (minerals) from water, food and environment. Fukino could show that Spirulina successfully counteracted poisoning of the kidneys by heavy metals assisting the detoxification [51].

3.3 Anti-inflammatory activity

In experimental models the phycocyanin extract of Spirulina exhibited anti-inflammatory activity [52 –54]. The anti-inflammatory effect seemed to be a result of phycocyanin which inhibited the formation of leukotriene B4, an inflammatory metabolite of arachidonic acid [55]. C-phycocyanin is a free radical scavenger [9] and has significant hepatoprotective effects [56]. In mouse and in chicken an increased phagocytic activity could be proved [57, 43]. This was confirmed by two further studies, showing a reduction of chronic diffuse liver disease [58] or a selective inhibition of cyclooxygenase-2 by C-phycocyanin [59]. It also prevented inflammatory stomach and intestinal diseases [60], a condition for a complete absorption of nutrients.

3.4 Immuno-modulatory effects

Spirulina is described to be a powerful tonic for the immune system [61]. In studies on mice, hamsters, chickens, turkeys, cats and fish, Spirulina consistently improved immune system function. Spirulina stimulated the immune system and actually enhanced the body’s ability to generate new blood cells. The spleen and thymus glands showed enhanced function. Macrophages, T-cells and Natural killer (NK) cells exhibited enhanced activity following Spirulina administration. Feeding of even small amounts of Spirulina to mice resulted in following immuno-modulatory functions [62 –64]:

Mice fed Spirulina showed increased numbers of splenic antibody-producing cells in the primary immune response to sheep red blood cells,

The percentage of phagocytic cells in peritoneal macrophages from mice fed a Spirulina diet was significantly increased,

The proliferation of spleen cells by either Concanavalin A (Con A) or phytohemagglutinin (PHA) was significantly increased,

Addition of a hot water extract of Spirulina (SHW) to an in vitro culture of spleen cells significantly increased proliferation of these cells with no effect on thymus cells,

The hot water extract of Spirulina also significantly enhanced interleukin-1 production from peritoneal macrophages, and

Addition of the hot water extract of Spirulina to an in vitro spleen culture and the supernatant of macrophages resulted in enhancement of antibody production.

Food supplementation with polysaccharides/phycocyanin (ingredients of Spirulina) stimulated T-lymphocytes [65] and also Natural Killer cells [66], so that bacteria and viruses could much more actively be combated [43]. Blinkova reported that Spirulina was able to improve the function of spleen and thymus gland, supporting the killing of invading pathogens [67]. In line with these observations, Hayashi’s group reported that Spirulina prevented the penetration of viruses into the membrane of the host cells [44, 45]. This was discussed to make spirulina-fed birds and poultry more resistant to infections [68].

In addition, the humoral immune system is also strengthened by increasing the production of antibodies and cytokines [62 , 70].

Overall, the number of possible pathogens such as Escherichia coli and Candida, was reduced while the growth of beneficial species of the intestinal flora (especially lactobacilli and bifidus bacteria) was stimulated [67, 71].

3.5 Anti-oxidant activity

Several studies have demonstrated that Spirulina possesses significant anti-oxidant activity both in vitro and in vivo. Manoj et al. [72] reported that the alcohol extract of Spirulina inhibited lipid peroxidation more significantly (65%) than chemical anti-oxidants like α-tocopherol (35%), butylated hydroxy anisol (45%) and β-carotene (48%). The water extract of Spirulina is also shown to have more anti-oxidant effect (76%) than gallic acid (54%) and chlorogenic acid (56%). Phycocyanin also inhibited liver microsomal lipid peroxidation. Zhi-Gang et al. [73] studied the anti-oxidant effects of two fractions of a hot water extract of Spirulina using three systems that generate superoxide, lipid, and hydroxyl radicals. Both fractions showed significant capacity to scavenge hydroxyl radicals (the most highly reactive oxygen radical) but no effect on superoxide radicals. One fraction had significant activity in scavenging lipid radicals at low concentrations.

Spirulina anti-oxidant activity was analyzed against lead acetate-induced hyperlipidemia and oxidative damage in the liver and kidney of male rats. Animals were fed on a standard laboratory diet with or without 5% Spirulina maxima in the standard laboratory diet and treated with three doses of lead acetate (25 mg each/weekly, intraperitoneal injection) The results showed that Spirulina prevented the lead acetate-induced significant changes on the anti-oxidant status of the liver and kidney. On the other hand, Spirulina maxima succeeded to improve the biochemical parameters of the liver and kidney towards the normal values of the control group [74].

4 Spirulina platensis as supplement of animal feed

Because of the nutrients and effects reported above, fishmeal, groundnut meal or soybean meal can be partially replaced by spirulina in forage of fish, poultry, cattle and domestic animals [28 , 76]. Fishmeal and peanut cake in a commercial diet containing both protein sources may be replaced on an isonitrogenous basis with dried spirulina 140 and 170 g/kg (starter), and 120 and 128 g/kg (finisher) for broiler chicks [75]. A vitamin or mineral supplement was not added to the two algal diets because spirulina is rich in these nutrients. All the growth parameters of chicks were similar fed diets with spirulina. Meat color was not affected by diet except for a more intensely colored meat in broilers fed on spirulina containing diets. Spirulina administered to poultry led to shiny and more durable plumage, which was primarily attributed to the ingredient gamma-linolenic acid. With high administration of spirulina - if a hereditary predisposition for red lipochrome is present - a red coloring or an increase in the red coloring of the plumage can occur. Red canaries have an enzyme which can produce canthaxanthin from certain carotenoids (in the case of spirulina this might be zeaxanthin) by gene introduction as a result of mating with hooded siskin. (Zeaxanthin itself, however, leads to an orange rather than to a red coloration [77]). However, there are also small amounts of canthaxanthin directly contained in spirulina, which are stored unchanged and could therefore also cause a red coloration. Red coloring or orange coloring has not been observed with yellow-ground canaries; provided a dosage of 3 g spirulina per kg of egg feed is maintained. In the above-mentioned studies on poultry up to 170 g spirulina per kg of feed was given (e.g. [75]).

Comparative studies on poultry clearly showed that fertility of animals treated with spirulina was clearly higher than in the comparison group [78]. Whether the growth of young animals will also be faster is not yet certain. There are studies that prove this [79] as well as others in which this was not found.

Spirulina has already been used several times to influence both the color of egg yolks [78] and the flesh of poultry. It was shown that already at a dose of 40 g/kg the colour of the muscle meat (due to the storage of zeaxanthin) clearly increased [24, 75].

5 Quality-related safety and toxicology

Spirulina is a form of cyanobacterium, of which some are known to produce toxins such as microcystins, β-methylamino-L-alanine (BMAA), and others. Some spirulina supplements have been found to be contaminated with microcystins, albeit at levels below the limit set by the Oregon Health Department [80]. Microcystins can cause gastrointestinal disturbances, and in the long term, liver damage [81].

These toxic compounds are not produced by spirulina itself but may occur as a result of contamination of spirulina batches with other toxin-producing blue-green algae. Adverse events caused by Spirulina are not known up to now [20]. As spirulina is considered as a dietary supplement in the U.S., no active, industry-wide regulation of its production occurs and no enforced safety standards exist for its production or purity. The U.S. National Institutes of Health describes spirulina supplements as “possibly safe”, provided they are free of microcystin contamination, but “likely unsafe” (especially for children) if contaminated [82]. Given the lack of regulatory standards in the U.S., some public-health researchers have raised the concern that consumers cannot be certain that spirulina and other blue-green algae supplements are free of contamination. Since the risk for contamination with toxin-producing microalgae is higher in open pond systems than in closed bioreactors, increased quality control for open ponds algae products must be realized. Heavy-metal contamination of spirulina supplements has also raised concern. The Chinese State Food and Drug Administration reported that lead, mercury, and arsenic contamination was widespread in spirulina supplements marketed in China very likely due to water pollution. One study reported the presence of lead up to 5.1 ppm in a sample from a commercial supplement [5]. Therefore, it is extremely important to use Spirulina only from providers which produce under stringent and standardized conditions.

Spirulina doses of 10 to 19 grams per day over several months have been used safely. Furthermore, there is evidence that regular consumption in several regions of Africa reaches up to 40 g [9] and no adverse effects have been reported. Adverse effects may include nausea, diarrhea, fatigue, or headache [80].

6 Sustainability of Spirulina

With the high proportion of proteins, beta-carotene and iron, Spirulina can exactly replenish and compensate deficits, which might occur in areas with poor and/or unbalanced animal fodder (e.g. Sahel area in Africa, waste lands in India, China, South America). In addition, Spirulina can be cultivated in otherwise rather barren areas without consuming valuable, clean fresh water, because it thrives best even in highly saline water. An important aspect from the sustainability point of view. Another benefit includes the process of photosynthesis performed by Spirulina during their growth. In that way carbon dioxide is converted into a broad spectrum of organic substances powered by light energy. On a theoretical basis one kg of algae can break down up to 1.8 kilos of carbon dioxide (CO₂) while roughly one kilo of oxygen is released by the hydrolysis of water. Microalgae such as Spirulina are characterized by a basic morphological cell structure and have evolved efficient uptake and concentrating mechanisms of inorganic carbon. Those features make them superior to terrestrial photosynthetic organisms in terms of CO₂ fixation capacity and biomass productivity.

7 Outlook

While there are a series of field reports in animals and humans, the scientific evaluation of the different effects of spirulina on a molecular biology level on human cells is underexplored. Especially molecular effects on the detoxifying system, on liver cells or on endothelial cells, important organs involved in the detoxification of the organism, and on the regulation of blood pressure and anti-coagulation, are nearly completely unknown. There are first studies showing that spirulina seems to protect against effects of endotoxins e.g. on neural stem cells or also may have an influence on the phagocytic activity in stimulated U937 cells [63]. In addition, Zhang reported a chemo-protective and radio protective capability, and described a spirulina extract to be a potential adjunct to cancer therapy [83].

Future studies will show whether spirulina can inhibit harmful effects of cytostatic agents in endothelial- and liver cells [84, 85].

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