EFEK SPIRULINA (Ganggang Biru Hijau) PADA KEKEBALAN
Thus, multiple studies on whole blue-green-algae in humans, mice, rats, cats, and chickens have demonstrated an effect on phagocytosis, NK cell function, and inﬂammation. Some differences exist in the data, including the mild reduction of phagocytic activity in humans after algae consumption, in contrast to the increase of phagocytosis among bronchoalveolar macrophages. The cell types and experimental set-ups vary, and further studies are needed to establish the exact biochemical mechanisms involved.
EFFECTS OF BLUE-GREEN ALGAE ON SPECIFIC IMMUNITY
Hayashi et al7 examined the effect of an algae-supple-mented diet on the ability to build a speciﬁc immune response
Table 2. Immuno-Modulatory and Anti-Inﬂammatory Effects of Whole Blue-Green Algae
|Spirulina sp.||Food||Human||Reversal of tobacco-induced oral cancer||Mathew et al, 1995|
|Food||Mouse||Proportional reduction of IgE, increase of IgA||Hayashi et al, 1998|
|Food||Mouse||Increased phagocytic activity Increased spleen cell proliferation Increased antibody production||Hayashi et al, 1994|
|Food||Chicken||Increased phagocytic activity Increased NK cell-mediated anti-tumor activity Increased antibody production||Qureshi et al, 1996|
In vitro, cat
|Increased phagocytic activity||
Qureshi & Ali, 1996
|IP injection||Rat||Inhibition of mast cells Decrease in local allergic reaction Decrease in serum histamine levels Reduced allergy-induced mortality||Kim et al, 1998 Yang et al, 1997|
|Aphanizomenon ﬂos-aquae||Food||Human||Increased transient recruitment of NK cells into tissue Increased mobilization of T and B cells into blood Mild modulation of PMN-mediated phagocytic response||Jensen et al, 2000|
|Food||Rat||Decreased serum levels of arachidonic acid||Kushak et al, 2000|
|Food||Rat||Source of linolenic acid (omega-3) Increased serum levels of EPA and DHA||Kushak et al, 2000|
In vitro, rat
|Activation of macrophages (NF-kappaB, cytokines)||Pasco, in press|
to sheep red blood cells. After immunizing mice (either once to measure the primary response or twice for the secondary response), they found that mice fed with the algae-supple-mented diet showed increased numbers of splenic IgM anti-body-producing cells when compared to control animals. Interestingly, this ﬁnding only held true for the primary immune response, as the IgG antibody production in the secondary immune response was hardly affected. In experiments involving chickens, there were no differences observed in anti-sheep red blood cell antibodies during primary responses, while antibody titers for the secondary response in algae-fed chickens were augmented compared to control animals.8 The differences may reﬂect the anatomical differences between the rodent and chicken immune systems.
Hayashi et al10 examined other antibody classes such as IgA and IgE in the context of mice orally immunized with a crude shrimp extract. They found that whereby both IgA (intestinal) and IgE (in serum) levels increased with antigen challenge, only IgA levels showed a greater enhancement in secretion with concurrent treatment with Spirulina extract (ﬁve-week feeding regimen).10 From this study they concluded that bluegreen algae does not seem to induce or enhance food allergic IgE-dependent reactions. Furthermore, they suggest that when ingested along with or before a potential antigenic threat, bluegreen algae may enhance IgA anti- body levels to protect against food allergies.
Along the same lines, further studies have suggested that blue-green algae may inhibit mast cell-mediated type I allergic reactions and even the anaphylactic reaction in rats.11,12 By injecting a blue-green algae extract intraperitoneally (100-1000mg/g body weight) one hour prior to an allergic challenge, mortality induced by the anaphylactic compound 48/80 was decreased, local allergic reaction activated by antidinitrophenyl (anti-DNP) IgE was inhibited, and serum histamine levels were decreased. In vitro experiments from this group provided similar results.
The effects of blue-green-algae on IgE-production and allergic reactions are encouraging, and warrant further studies in humans.
EFFECTS OF BLUE-GREEN ALGAE ON LEUKOCYTE TRAFFICKING
Much attention with regards to dietary modulation of the immune system has been given to stimulating activity of various immune cell types such as the phagocytic activity of macrophages, or the tumoricidal activity of natural killer cells. However, immune cell trafficking and the recruitment of immune cells from the systemic circulation are of equal importance. A recent study by Jensen et al5 involving
Table 3. Bio-modulatory Effects of Puriﬁed Compounds from Blue-Green Algae
|All blue-green algae||C-Phycocyanin||Anti-inﬂammatory (reduces leukotriene B4) Free radical scavenger Selective inhibition of COX-2 Reduced tissue damage in acetic acid-induced colitis Hepatoprotective effect||Romay 1999 Bhat & Madyastha 2000 Reddy et al, 2000 Gonzalez et al, 1999 Vadiraja et al, 1998|
|Spirulina||Calcium Spirulan (Ca-Sp)||Selectively inhibits penetration of virus into host cell (Herpex Simplex, human cytomegalovirus, measles, mumps, Inﬂuenza A, HIV-1)||Hayashi et al, 1996|
|Reduces lung metastasis of melanoma cells by inhibition of tumor cell invasion of basal membrane||Mishima et al, 1998|
|Cyanovirin-N||Irreversible inactivation of several strains of HIV (inhibited cell-to-cell and virus-to-cell fusion)||Boyd, 1997|
|Promotion of lactic acid bacteria growth in vitro||Parada et al, 1998|
|Aphanizomenon ﬂos aquae||Unknown Polysaccharide||Induces apoptosis in some human tumor cell lines Stimulate the macrophage activity||Jensen, msp in prep Pasco et al, in press.|
|Lyngbya lagerheimii Phormidium tenue||Sulfolipid||Inhibits syncytium formation upon HIV infection||Gustafson et al, 1989|
|Inhibition of chemically induced skin tumors||Tokuda et al, 1996|
humans demonstrated that the blue-green alga Aphanizomenon ﬂos-aquae was able to trigger within two hours the migration of nearly 40% of the circulating natural killer cells. This effect was signiﬁcantly more pronounced in long-term consumers than in naïve subjects. In the same study, Aphanizomenon ﬂos-aquae was also shown to stimulate the mobilization of T and B lymphocytes. This effect appeared cell-type speciﬁc since no changes were observed on polymorph nucleated cells.
ANTI-INFLAMMATORY PROPERTIES OF BLUEGREEN ALGAE
Blue-green algae in general contain a significant amount of carotenoids, namely beta carotene, lycopene, and lutein, providing it with good antioxidant properties. By their quenching action on reactive oxygen species, antioxidants carry intrinsic anti-inflammatory properties. However, blue green algae also contains speciﬁc antiinﬂammatory properties as a result of their high phycocyanin content. Phycocyanin is a photoharvesting pigment that provides the intense blue color in blue green algae. It can constitute up to 15% of the dry weight of a blue green algae harvest. C-phycocyanin is a free radical scavenger,26 and has signiﬁcant hepatoprotective effects.27 Phycocyanin was shown to inhibit inﬂammation in mouse ears28 and pre-tory effect seemed to be a result of phycocyanin to inhibit the formation of leukotriene B4, an inﬂammatory metabolite of arachidonic acid.28
In a study performed in rats, the blue-green algae Aphanizomenon ﬂos-aquae was also shown to decrease the plasma level of arachidonic acid.30 Aphanizomenon ﬂosaquae contains signiﬁcant amounts of the omega-3 alpha-linolenic acid. Omega-3 fatty acids have been shown to inhibit the formation of inﬂammatory prostaglandins and arachidonate metabolites. Since Spirulina contains signiﬁcant amounts of omega-6 gamma-linolenic acid, the antiinﬂammatory properties of Spirulina must be due to different biochemical pathways.
As part of its program aimed at discovering new antitumor and anti-viral agents in natural sources, the National Cancer Institute isolated extracts of blue-green algae (Lyngbya lagerheimii and Phormidium tenue) that were found to protect human lymphoblastoid T cells from the cytopathic effect of HIV infection. Upon further investigation, a new class of HIV inhibitory compounds called the sulfonic acid-containing glycolipids were isolated; the pure compounds were found to be strikingly active against the HIV virus in the p24 viral protein and syncytium formation assays.13 Since this discovery, there has been further investigation into other species of blue-green algae for compounds with anti-viral properties. Some compounds worthy of mention include a protein called cyanovirin-N which appears to irreversibly inactivate diverse strains of the HIV virus and to inhibit cell-to-cell and virus-to-cell fusion.14 Other studies using a water-soluble extract of blue-green algae have found a novel sulfated polysaccharide, calcium spirulan (Ca-SP), to be an antiviral agent. This compound appears to selectively inhibit the penetration of enveloped viruses (Herpes simplex, human cytomegalovirus, measles virus, mumps virus, inﬂuenza A virus, and HIV-1) into host cells, thereby preventing replica-tion.15-17 A review of anti-HIV activity of extracts from blue-green algae has been recently published.18
An early study on bluegreen algae’s cancer-preventive properties in humans was performed on tobacco-induced oral leukoplakia.19 Mathew et al found that oral supplementation with Spirulina fusiformis resulted in complete regression of 57% of subjects with homogenous leukoplakia. After discontinuation of Spirulina supplementation, almost half of the complete responders developed recurrent lesions.
In other studies, extracts of bluegreen algae have been used to treat cancer in animal models. In one model, ingestion of an extract of Spirulina and Dunaliella was shown to inhibit chemically-induced carcinogenesis in hamster buccal pouches.20,21 Earlier studies often attributed the anticancer effect of algae to its content in carotenoids since beta-carotene has been shown to have an effect similar to that of algae extract. A more recent study, however, showed that the sulfated polysaccharide mentioned above, Ca-SP, appears to inhibit tumor invasion and metastasis.22 Both the in vitro and in vivo effects of Ca-SP suggest that the intravenous administration of Ca-SP reduces the lung metastasis of melanoma cells by inhibiting the tumor invasion of the basement membrane. A water-based extract of Aphanizomenon ﬂos aquae containing high concentrations of phycocyanin inhibited the in vitro growth of one out of four tumor cell lines tested, indicating that at least some tumor cell types may be directly sensitive to killing by phycocyanin (Jensen et al, manuscript in preparation). Another fresh-water blue-green algae, Phormidium tenue, contains several diacylglycerol compounds which effectively inhibited chemical-ly-induced skin tumors in mice.23 In addition, Spirulina was shown to have a modulatory effect on hepatic carcinogen metabolizing enzymes.24
Of major interest to ongoing research in inﬂammation as well as breast cancer is the ﬁnding that C-phycocyanin selectively inhibits COX-2, but has no effect on COX-1.25 The COX enzymes are involved in prostaglandin synthesis. Since COX-2 is over-expressed in many breast cancer cells, and inhibition of COX-2 leads to a markedly reduced tumor growth and blocks angiogenesis, the ﬁnding that phycocyanin specifically interferes with this pathway holds promise.
BLUE-GREEN ALGAE AS A BIOMODULATOR
Besides their effects on the immune system, blue-green algae have also been reported to modulate other systems and improve metabolism. In the past few years increasing attention has been given to the study of the therapeutic effects of blue-green algae. The anecdotal claims for such effects are numerous. Although there is limited data from controlled animal or clinical studies, such claims include improvement in condition of Alzheimer’s patients, overall enhancement of immune response, improvement in ﬁbromyalgia, control of hypertension, alleviation of depression and chronic fatigue, increased stamina, healing of internal and external lesions, increased mental acuity, and general improvement in overall well-being. This last section will review the scientiﬁc evidence supporting the therapeutic effects of blue-green algae.
EFFECTS ON METABOLISM
Several reports from different labs have shown that certain species of blue-green algae have cholesterol-lowering effects in animal and human models. In feeding experiments in rats, two studies have reported that the elevation in total cholesterol, LDL, and VLDL cholesterol in serum caused by cholesterol feeding was reduced when the high cholesterol diet was supplemented with 16% and 5% blue-green algae, respectively.31,32 In addition, Kato found that adipohepatosis induced by a high fat and high cholesterol diet was cured rapidly when the diet was supplemented with algae.31 Investigations into the mechanism of this phenomenon led to the ﬁnding that the algae-fed group showed a statistically signiﬁcant increase in the activity of lipoprotein lipase, a key enzyme in the metabolism of triglyceride-rich lipoproteins.33
The hypocholesterolemic effect of blue green algae was also observed in humans in a study conducted on 30 patients with mild hyperlipidemia and mild hypertension.34 Patients took 4.2 grams of algae or placebo per day, and were observed for two months. At the end of the study, patients taking the algae showed a signiﬁcant reduction of LDL-cho-lesterol (p<0.05) compared to the control group. LDL cholesterol increased back to baseline levels after administration of the algae was discontinued. In addition to lowering LDL cholesterol levels, the atherogenic index (a measure of fat deposition in arteries) declined signiﬁcantly after four weeks of algae consumption.
In a recent study by Kushak et al, rats were fed the blue-green alga Aphanizomenon ﬂos-aquae and total cholesterol level was monitored. After 43 days, cholesterol levels were significantly decreased when compared to the control group.30 Although Aphanizomenon ﬂos-aquae contains a signiﬁcant amount of the omega-3 polyunsaturated linolenic
Table 4. Biomodulatory Effects of Whole Blue-Green Algae on Metabolism
|Algae Species||Introduced as||
|Aphanizomenon||Food||Rat||Reduction of cholesterol||Kushak et al, 2000||Reduction of cholesterol|
|Food||Rat||Reduction of blood glucose levels||Drapeau et al, 2001||Reduction of blood glucose levels|
|Food||Human||Modulation of brain activity (EEG)||Walker & Valencia, 1999||Modulation of brain activity (EEG)|
|Spirulina||Food||Human||Reduced body weight||Becker et al, 1986||Reduced body weight|
|Food||Rat||Reduction of cholesterol||Kato et al, 1984||Reduction of cholesterol|
|Food||Rat||Increased activity of lipase||Iwata et al, 1990||Increased activity of lipase|
|Food||Rat||Reduced glucose levels||Takai et al, 1991||Reduced glucose levels|
|Food||Rat||Inhibition of maltase and sucrase||Kushak et al, 1999||Inhibition of maltase and sucrase|
|Food||Mouse||Modulation of carcinogen metabolic enzymes||Mittal et al, 1999||Modulation of carcinogen metabolic enzymes|
|Food||Mouse||Modulation of lead toxicity||Shastri et al, 1999||Modulation of lead toxicity|
Increased iron status during pregnancy and lactation
|Kapoor & Mehta, 1998||
Increased iron status during pregnancy and lactation
|Nostoc||Food||Rat||Reduction of cholesterol||Hori et al, 1994||Reduction of cholesterol|
acid, the effect on cholesterol levels seemed unrelated to the lipid content of the diets. Kushak et al30 proposed that the hypocholesterolemic effect of Aphanizomenon ﬂos-aquae may be due to its chlorophyll content which was shown to stimulate liver function and decrease blood cholesterol.35
In a double-blind crossover study involving human patients, supplementing the diets of obese outpatients with 2.8 grams of bluegreen algae three times daily over a four week period resulted in a statistically signiﬁcant reduction of body weight.36 In a study measuring the effect of bluegreen algae on glucose levels in diabetic rats, the water-soluble fraction was found to be effective in lowering the serum glucose level at fasting, while the water insoluble fraction suppressed glucose levels at glucose loading.37 In another study investigating the effect of the blue-green alga Aphanizomenon ﬂos-aquae on rat intestinal mucosal digestive enzymes, it was observed that this alga speciﬁcally inhibited the activity of maltase and sucrase in a dose-dependent manner.38 Furthermore, this decrease in enzymatic activity was accompanied by a dose-dependent decrease in blood glucose.
The overall conclusion is that blue-green algae may have beneﬁts on lipid and sugar metabolism, as well as liver function. Further human studies are needed to address the feasibility of using blue-green algae in conjunction with cholesterol-lowering medication.
OTHER EFFECTS OF BLUE GREEN ALGAE
Other research studies on blue green algae consumption deserve mention. Many reports exist in the literature on its antimicrobial effects. The secretion of anti-microbial substances is an important part of the competition for ecological niches in the natural environment. However, an interesting caveat exists. In one study, Spirulina was cultured in vitro, and the extracellular medium was shown to stimulate the growth of lactic acid bacteria.39 If the growth-promoting sub-stance(s) exist in sufficient amounts intracellularly, blue green algae may play a role in vivo by supporting friendly gut bacteria. This leads to other facets of health including gut health and nutrient absorption. On that note, consumption of Spirulina was shown to support the iron status and hemoglobin of rats during pregnancy and lactation.40 Spirulina fusiformis had a signiﬁcant protective effect against lead-induced toxicity in rats.41 Finally, a report by Valencia et al has presented evidence that Aphanizomenon ﬂos-aquae accelerates recovery from mild traumatic brain injury.42
CONCLUSION AND SUMMARY
Research results based on the numerous isolated compounds from blue green algae warrant the exploration of using whole algae as conjunctive therapy due to the possible synergistic effects of many phytochemicals within the whole algae. The emergence of composite algae supplements in contrast to single algae supplements may also yield further anti-inﬂammatory, immune-boosting, and metabolic beneﬁts. A signiﬁcant body of data suggests that blue green algae immunoenhancing properties could be useful in the adjunct treatment of various diseases involving 1) suppressed or exhausted immune system, and 2) inappropriate immune response including allergies, autoimmune diseases, and chronic inﬂammatory conditions. The data presented also suggests that blue green algae could be useful as an adjunct in the treatment of cancer and AIDS, and calls for the design of controlled human clinical studies.
- Eisenberg D, Davis R, et al. Trends in alternative medicine use in the United States. 1990-1997.” JAMA. 1998:280(18):1569-1575.
- Astin J. Why patients use alternative medicine. JAMA. 1998;279(19):1548-1553.
- Sobel D. Rethinking medicine: improving health outcomes with cost-effective psychosocial interventions. Psychosomatic Medicine. 1995;57:234-244.
- Furnham A. Forey J. The attitudes, behaviors, and beliefs of patients of conventional vs complementary (alternative) medicine. J Clini Psych. 1994;50:458-469.
- Jensen GS, Ginsberg DI, et al. Consumption of Aphanizomenon ﬂos aquae has rapid effects on the circulation and function of immune cells in humans. JANA. 2000;2(3):50-58.
- Qureshi M, Ali R. Spirulina platensis exposure enhances macrophage phagocytic function in cats. Immunopharmacol Immunotoxicol. 1996;18(3):457-463.
- Hayashi O, Katoh T, et al. Enhancement of antibody production in mice by dietary Spirulina platensis. J Nutr Sci Vitaminol. 1994;40:431-441.
- Qureshi M, Garlich J, et al. Dietary Spirulina platensis enhances humoral and cell-mediated immune function in chickens. Immunopharmacol Immunotoxicol. 1996;18(3):465-476.
- Pugh N, Ross SA, ElSohly HN, ElLohly MA, Pasco DS.Isolation of three high molecular weight polysaccharides with potent immunostimulatory activity from Spirulina platensis, Aphanizomenon ﬂos-aquae and Chlorella pyrenoidosa. Planta Medica. In Press.
- Hayashi O, Hirahashi T, et al. Class-speciﬁc inﬂuence of dietary Spirulina platensis on antibody production in mice. J Nutr Sci Vitaminol. 1998;44(6):841-851.
- Kim H, Lee E, et al. Inhibitory effect of mast cell-mediated immediate-type allergic reactions in rats by Spirulina. Biochem Pharmacol. 1998;55(7):1071-1076.
- Yang H, Lee E, et al. Spirulina platensis inhibits anaphylactic reaction. Life Sci. 1997;61(13):1237-1244.
- Gustafson K, Cardellina II J, et al. AIDS-antiviral sulfolipids from cyanobacteria (blue-green algae). J National Cancer Institute.1989;81:1254-1258.
- Boyd M. Protein isolated from blue-green algae inactivatesHIV. Antimicrob Agents Chemother. 1997;41:1521-1530.
- Hayashi K, Hayashi T, et al. A natural sulfated polysaccharide, calcium spirulan, isolated from Spirulina platensis: in vitro and ex vivo evaluation of anti-herpes simplex virus and antihuman immunodeﬁciency virus activities. AIDS Res Hum Retrovir. 1996;12(15):1463-1471.
- Hayashi T, Hayashi K. Calcium spirulan, an inhibitor of enveloped virus replication, from a Blue-Green Alga Spirulina platensis. J Natural Products. 1996;59:83-87.
- Ayehunie S, Belay A, et al. Inhibition of HIV-1 replication by an aqueous extract of Spirulina platensis. J Aquir Immun Deﬁc Syndr Hum Retrovirol. 1998;18(1):7-12.
- Schaeffer DJ, Krylov VS. Anti-HIV activity of extracts and compounds from algae and cyanobacteria. Ecotoxicology and Environmental Safety. 2000;45:208-227.
- Mathew B, Sankaranarayanan R, et al. Evaluation of chemo-prevention of oral cancer with Spirulina fusiformis. Nutr Cancer. 1995;24(2):197-202.
- Schwartz J. Shklar G. Regression of experimental hamstercancer by beta carotene and algae extracts. J Oral Maxillofac Surg. 1987;45:510-515.
- Schwartz J, Shklar G, et al. Prevention of experimental oralcancer by extracts of Spirulina-Dunaliella algae. Nutr Cancer. 1988;11:127-134.
- Mishima T, Murata J, et al. Inhibition of tumor invasion and metastasis by calcium spirulan (Ca-SP), a novel sulfated polysaccharide derived from a blue-green algae, Spirulina platen-sis. Clin Exp Metastasis. 1998;16(6):541-550.
- Tokuda H, Nishino H, et al. Inhibition of 12-O-tetrade-canoylphorbol-13-acetate promoted mouse skin papilloma by digalactosyl diacylglycerols from the fresh water cyanobacterium Phormidium tenue. Cancer Lett. 1996;104(1):91-95.
- Mittal A, Kumar PV, et al. Modulatory potential of Spirulina fusiformis on carcinogen metabolizing enzymes in Swiss albino mice. Phytother Res. 1999;13(2):111-114.
- Reddy CM, Bhat VB, et al. Selective inhibition of cyclooxyge-nase-2 by C-phycocyanin, a biliprotein from Spirulina platen-sis. Biochem Biophys Res Commun. 2000;277(3):599-603.
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- Romay C, Ledon N, Gonzalez R. Phycocyanin extract reducesleukotriene B4 levels in arachidonic acid-induced mouse-ear inﬂammation test. J Pharm Pharmacol. 1999;51(5):641-642.
- Gonzalez R, Rodriguez S, et al. Anti-inﬂammatory activity of phycocyanin extract in acetic acid-induced colitis in rats. Pharmacol Res. 1999;39(1):55-59.
- Kushak RI, Drapeau C, Van Cott EM. Favorable effects of blue-green algae Aphanizomenon ﬂos-aquae on rat plasma lipids. JANA. 2000;2(3):59-65.
- Kato T, Takemoto K, et al. Effects of Spirulina on dietary hypercholesterolemia in rats. J Jap Soc Nutr Food Science. 1984;37:323-332.
- Hori KG, Ishibashi G, et al. Hypocholesterolemic effect of blue-green alga, ishikurage (Nostoc commune) in rats fed atherogenic diet. Plant Foods Hum Nutr. 1994;45:63-70.
- Iwata K, Inayama T, et al. Effects of Spirulina platensis on plasma lipoprotein lipase activity in fructose-induced hyperlipidemic rats. J Nutr Sci and Vitaminology. 1999;36:165-171.
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Winter 2001 Vol. 3, No. 4 JANA 28