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Academic Sciences

International Journal of Pharmacy and Pharmaceutical Sciences


ISSN- 0975-1491

Vol 4, Issue 3, 2012

Review Article

SPIRULINA - AN OVERVIEW
SHABANA KOUSER ALI*, ARABI MOHAMMED SALEH
School of Bio Sciences and Technology, VIT University, Vellore. India. Email: shabanakouserali03@gmail.com
Received: 28 Feb 2012, Revised and Accepted: 25 Mar 2012
ABSTRACT
Arthrospira is a photosynthetic, filamentous, spiral-shaped, multicellular and blue- green micro alga. Cell division occurs by binary fission. As it
contains chlorophyll a, like higher plants, botanists classify it as a micro alga belonging to Cyanophyceae class; but according to bacteriologists it is a
bacterium due to its prokaryotic structure. Mexicans (Aztecs) started using this microorganism as human food. Its chemical composition includes
proteins (55%-70%), carbohydrates (15%-25%), essential fatty acids (18%) vitamins, minerals and pigments like carotenes, chlorophyll a and
phycocyanin. Pigments are used in food and cosmetic industries. Spirulina is considered as an excellent food, lacking toxicity and have anticancer,
antiviral, immunological properties and it also acts as a potent antioxidant. There has been a significant change in Spirulina functions under stress
conditions.
Keywords: Arthrospira, Cyanophyceae.

INTRODUCTION

Systematics

Spirulina named as Tecuitlatl by Aztecs, this means stones


excrement during 16th century. Later, due to outbreak of contagious
disease, new customs were adopted by people such as new foods,
religious, political and social changes, and the topic of Tecuitlatl
came to an end. It was not known till when man began to use
microalgae, but at present this resources can be so called, green
tendency20.

Spirulina (Arthrospira) belongs to the oxygenic photosynthetic


bacteria that cover the groups Cyanobacteria and Prochlorales11,49.

Spirulina - Small cakes made of a mud-like algae, which has a


cheese-like flavor, and that natives took out of the lake to make
bread,...". They are dried into cakes called "Dihe" or "Die. Back in
9th century, during Kanem Empire, only Spirulina had long history
in Chad. In 1961, short story, The Voice of the Dolphins, Leo Szilard
postulated the development of algae-based food supplement and
named algae as Amruss. In early 1970s, First large scale
production plant by Sosa Texcoco, was established13.

With start of chemical analyses, the race to commercialization began13,34.

Now, Spirulina is marketed and consumed in many different


countries such as Germany, Brazil26,Chile, Spain, France, Canada,
Belgium, Egypt, United States, Ireland, Argentina, Philippines, India,
Africa, and other countries, where public administration, sanitary
organisms and associations have approved human consumption20.
Some of the best worldwide known Spirulina producing companies
are: Earthrise Farms (USA), Cyanotech (USA), Hainan DIC
Microalgae Co., Ltd (China), Marugappa Chettir Research Center
(India), Genix (Cuba) and Solarium Biotechnology (Chile)1,7.

They are filamentous, non-heterocystous cyanobacteria that are


generally found in tropical and subtropical regions in warm bodies
of water with high carbonate/bicarbonate content, elevated pH, and
salinity. Their large, gas-vacuolate filaments (3 to 12m in diameter)
are easily collected by filtration and other physical means of
separation. Spirulina was isolated from fresh water sample in 1827
by Turpin13.

Stizenbergers studies on aseptate forms of Spirulina genus, and the


septal forms of Arthrospira genus in 1892. Later, It is reunified the
members of the two genera under the designation Spirulina17. In
1989, these microorganisms were classified into two genera,
according to a suggestion by Gomont in 189211. This classification is
currently accepted 42, 48.
Stanier and Van Neil40 incorporated green-blue algae into the
prokaryote kingdom and named these microorganisms as
cyanobacteria and this was accepted and first published in 1974 in
the Bergey`s Manual of Determinative Bacteriology19.

Morphology

Arthrospira maxima are filamentous cyanobacteria recognizable by


the main morphological feature of the genus: the arrangement of the
multicellular cylindrical trichomes in an open left-hand helix along
the entire length.

Fig. 1: Light micrograph of Arthrospira maxima. B. Light micrograph of Arthrospira platensis. Bar represents 20m.

Ali et al.

Under light microscopy, the blue-green non-heterocystous filaments,


composed of vegetative cells that undergo binary fission in a single
plane, show easily-visible transverse cross-walls. Filaments are solitary
and free floating and display gliding motility. The trichomes, enveloped
by a thin sheath, show more or less slightly pronounced constrictions at
cross-walls and have apices either slightly or not at all attenuated. Apical
cells may be broadly rounded or pointed and may be capitate and
calyptrate. The width of the trichomes, composed of cylindrical shorter
than broad cells varies from about 6 to 12m (16m) in a variety of
forms. The helix pitch (h) is determined by the equation
h=2rcot

Where, r is the radius of the cylinder surface to which the helix


belongs and a is the angle formed by the helix and the cylinder
generatrices and represents the slope of the helix curve. In many
strains of these two species, the helix pitch varies from 12 to 72 m.
Also the helix diameter varies, ranging from about 30 to 70m.

Environmental factors, mainly temperature43, physical and chemical


conditions, may affect the helix geometry. One drastic alteration of

Int J Pharm Pharm Sci, Vol 4, Issue 3, 9-15


this geometry is the reversible transition from helix to spiral shape
after transferring the filaments from liquid to solid media, first
observed by46. Although the helical shape of the trichome is
considered a stable and constant property maintained in culture,
there may be considerable variation in the degree of helicity
between different strains of the same species and within the same
strain. Even in natural monospecific populations, variations in
trichome geometry may be observed. Moreover, straight or nearly
straight spontaneous culture variants have been repeatedly
reported47. Once a strain has converted to the straight form, both
naturally or after physical or chemical treatments, such as UV
radiation or chemicals, it does not revert back to the helical form.
This is due to a mutation affecting some trichomes during certain
growth conditions. The common occurrence of straight trichomes, in
the cultures of Arthrospira, may suggest that the helicity character is
carried on plasmids. However, no plasmids have been observed in
the strains checked. When, in a culture of a helically coiled strain, a
few filaments happen to become straight, they tend to become
predominant. This is probably due to competition between the two
morphones, as observed in A. fusiformis.

Fig. 2: Morphology of Spirulina. (A) Optical microscopy (X400) of axenic S. platensis. (Photo by G. Caretta) (B) Scanning electron micrograph of
a trichome of axenic S. platensis. (Photo by R. Locci) (C) Electron micrograph of Arthrospira maxima in longitudinal section showing the
division of the trichome into cells by cross-walls (s). Note the abundance of gas vacuoles (gv), the bundles of the thylakoid membranes (t),
with associated phycobilisomes, many osmiophilic granules and ribosomes (r). (D) Electron micrograph of Arthrospira platensis in crosssection showing the multilayered cell wall (cw) and the subcellular organization of the cytoplasm. Note the accumulation of polyglucan
granules (pg) close to the longitudinal cell wall (cw) and in the interthylakoidal space. In the central cytoplasmic region there are some
carboxysomes (cs) (arrows) and two cylindrical bodies (cb). Bar represents 0.5 m. (C and D were adapted from48).
10

Ali et al.

Ultra-Structure
Prokaryotic organization with fibrils of DNA region, photosynthetic
system, pluri-stratified cell wall, capsule, ribosomes and numerous
inclusions13. Cell wall is made of four numbered layers: L I, L II, L III
and L IV (Ciferri 1983). The LI layer is not digestible by human
beings as contains b-1, 2-glucan, the L II layer contains protein and
lipopolysaccharides are favorite reasons for the easy human
digestion of Spirulina5.
Life Cycle

There are three fundamental stages: Trichomes fragmentation,


hormogonia cells enlargement and maturation processes, and
trichome elongation. Then this mature trichomes get divided into
filaments or hormogonia,cells in the hormogonias gets increased by
binary fission,grows lengthwise and takes their helical form5.

Fig. 3: Life cycle of Spirulina.


Nutritional Composition
Chemical analysis of Spirulina started in the year 1970 which
showed Spirulina as an excellent source of proteins, vitamins and

Int J Pharm Pharm Sci, Vol 4, Issue 3, 9-15


minerals41. Proteins constitute about 60%-70% of its dry weight13.
Contains high provitamin A (-carotene) 7, rich source of vitamin
B12 and used in the treatment of pernicious anemia8,7. Lipids
constitute about 4-7%29. It provides adequate amounts of iron in
anemic pregnant women33. Carbohydrates are about 13.6%39. It has
2.2%-3.5% of RNA and 0.6 %-1% of DNA13. It also has few natural
pigments such as carotenes, chlorophyll a and phycocyanin and
these microorganisms are used as source of pigmentation for fish,
eggs13, 20,37. It is reported the comparative -carotene content in
seven Spirulina strains among them Sp4 accumulated 231.7g-1 dry
weight36.
Health Benefits

Spirulina: has profound antioxidant potential, Its true healthprotective merit has only recently been discovered. phycocyanobilin
(PCB), the chromophore bound to chief protein, phycocyanin, can
function as a potent inhibitor of NADPH oxidase, the enzyme
complex that is the chief source of pathological oxidant stress in a
wide range of health disorders28. It appears to mimic the
physiological activity of free bilirubin15. NADPH oxidase overactivity in disorders had suggested that ample intakes of Spirulina
may prevent and has therapeutic potential with respect to many
vascular diseases (including atherogenesis, hypertension, and
congestive heart failure), cancers, complications of diabetes, and a
range of neurodegenerative, fibrotic, or inflammatory disorder28.
Oral administration of phycocyanin or of whole Spirulina has
exerted central neuroprotective effects in rodent studies an
observation which strongly suggests that PCB can transit the blood
brain barrier16.
Spirulina is an ideal food and dietary supplement for the 21st
century by the Food and Agriculture Organization (FAO) of the
United Nations32. The authentication of food ingredients is of crucial
concern to food processors since the purity of food ingredients is
easily subject to abuse by unscrupulous suppliers13, 34. Recent
technological advances for the determination of food authenticity,
Trends in Food Science and Technology7. Spirulina powder is one
such food product that is easily subject to tampering.

Fig. 4: Phycocyanobilin of Spirulina and Bilirubin of Higher fauna can mimic their activity
Antiviral activity of Spirulina
Spirulina has all bio-chemicals in its constitution that can build a
healthy immune system, which scavenges free radicals as well.
Compounds extracted from Arthrospira have inhibitory activity
against a wide range of viruses such as HIV-1, HSV-1, HSV-2, HCMV,
influenza type A, measles, etc. Extracts from cyanobacteria have

antimutagenic and anticancer effect and can prevent development


and growth of tumors as well as inhibit metastasis or proliferation of
cancer cells14.

Spirulina platensis was shown to minimize HIV-I replication in


human T-cell lines, peripheral blood mononuclear cells (PBMC), and
Langerhans cells (LC). Extract concentrations ranging between 0.3
11

Ali et al.

and 1.2g/ml reduced viral production by approximately 50% in


PBMCs. A platensis extracts possess antiretroviral activity that may
be of potential clinical interest2.
Anti-Cancer Effects

Several studies have shown that Spirulina or its extracts can prevent
or inhibit cancers in humans and animals. In vitro studies suggest
the unique polysaccharides of Spirulina enhance cell nucleus enzyme
activity and DNA repair synthesis6.

Immunological Applications

NF-kappa B directed luciferase expression was enhanced by


Immulina from Spirulina treatment when cells were co-transfected
with vectors expressing proteins supporting TLR2 -(CD14 and
TLR2) but not TLR4 -(CD14, TLR4, MD-2) dependent activation4.
Spirulina or Arthrospira is a blue-green alga that became famous
after it was successfully used by NASA as a dietary supplement for
astronauts on space missionary, it inhibited the release of histamine
by mast cells, and this alga may improve several symptoms of antiallergic effects25. Spirulina has no effect on chronic fatigue3.

Spirulina extract (250mg) plus zinc (2mg) twice daily for 16 weeks may
be useful for the treatment of chronic arsenic poisoning with melanosis
and keratosis30. The first human feeding study that demonstrates the
protective effects of Spirulina towards allergic rhinitis27.
Spirulina helps to protect against certain nutritional deficiencies. It
plays in the prevention of cancer, cellular ageing, infectious diseases
and reduced immune system efficiency, as well as playing an
important part in the functioning of the medulla (stimulation of the
erythropoiesis)18. Aqueous extract of Spirulina, has a protective
effect against apoptotic cell death due to free radicals12.

Spirulina was a stronger inhibitor than Chlorella. Annexin-V staining


showed that aqueous extract of Spirulina induced apoptosis of HSC
after 12 h of treatment. In addition, the aqueous extract of Spirulina
triggered a cell cycle arrest of HSC (hepatic stellate cell) at the G2/M
phase50.

Cultivation of Spirulina platens under salt stress conditions

0.02M (control), 0.04 and 0.08M NaCl led to a remarkable alteration


of algal metabolism as well as an enhancement or induction of
biologically active compounds. Concerning algal growth, salt stress
caused a decrease in dry weight, chlorophyll a content as well as
certain xanthophylls (neoxanthin and violaxanthin), while carotene production was stimulated especially at higher salt
concentrations.

Biochemical analysis of salt stressed algae revealed that lipid


content was slightly increased together with certain saturated and
unsaturated fatty acids especially the polyunsaturated ones (inolenic acid, omega 3 fatty acid).

Phosphate buffer and water extracts of the algae exhibited antiviral


activities against both Hepatitis-A-virus-type-MBB (HAV-MBB strain,
RNA virus) and Herpes simplex-virus-type-1 (HSV-1, DNA virus).
Water extracts were found to be more effective than phosphate

Int J Pharm Pharm Sci, Vol 4, Issue 3, 9-15


buffer extracts in inducing antiviral activities (98%) especially
against HSV-1 virus.

The same water extract of the salt stressed algae demonstrated


higher anti-coagulating activity compared with those of heparin and
the positive control measured by clotting time assay38.

The salt-tolerant hypercarbonate strain CS-328 was grown in a


medium containing 0.24 to 1.24M sodium, resulting in increased
biosynthesis of soluble carbohydrates to up to 50% of the dry
weight at 1.24M sodium. For cells grown in 1.24M NaCl, the
fermentative yields of acetate, ethanol, and formate increase
substantially to 1.56, 0.75, and 1.54mmol/(g [dry weight] of cells /
day), respectively (36-, 121-, and 6-fold increases in rates relative to
cells grown in 0.24M NaCl).

Catabolism of endogenous carbohydrate increased by approximately


2-fold upon hypoionic stress. For cultures grown at all salt
concentrations, hydrogen was produced, but its yield did not
correlate with increased catabolism of soluble carbohydrates.
Instead, ethanol excretion becomes a preferred route for
fermentative NADH reoxidation, together with intracellular
accumulation of reduced products of acetyl coenzyme A (acetyl-CoA)
formation when cells are hypoionically stressed. In the absence of
hypoionic stress, hydrogen production is a major beneficial pathway
for NAD+ regeneration without wasting carbon intermediates such
as ethanol derived from acetyl-CoA. This switch presumably
improves the overall cellular economy by retaining carbon within
the cell until aerobic conditions return and the acetyl unit can be
used for biosynthesis or oxidized via respiration for a much greater
energy return10.

Salt stress leads to a modification of the QB niche at the acceptor


side and an increase in the stability of the S2 state at the donor side,
which is associated with a dissociation of the PsbO protein21. It
resulted in a significant decrease in photosynthetic oxygen evolution
activity and PSII electron transport activity, but a significant
increase in PSI electron transport activity. In addition, it resulted in
a decreased electron transport per PSII reaction center, but an
increased absorption per PSII reaction center. (Tao Zhang et al.,
2010). D1 protein turnover is involved in protection of Photosystem
II against UV-B induced damage in the cyanobacterium
Arthrospira22. Heat stress inhibited the maximum efficiency of PSII
photochemistry significantly and showed no effects on the stability
of the S2QA and S2QB states and that the different populations of
the active PSII reaction centers show different sensitivity to heat
stress in Spirullina platensis cells9.
Malondialdehyde (MDA), superoxide dismutase (SOD) and proline
contents increased under the heavy metal stress, corresponding to
the concentration of the metal ion in the culture medium. Increased
amount of MDA was indicative of formation of free radicals in the
test microorganism under heavy metals stress, while increased
levels of SOD and proline pointed to the occurrence of a scavenging
mechanism in the cyanobacterium Spirulina platensis-S5 31. S.
platensis might play a role in reducing the toxic effect of cadmium
and its antioxidant properties seem to mediate such a protective
effect 24.

Table 1: Quantity of Spirulina proteins and other foods20

Food Type
Spirulina powder
Whole Dried egg
Beer Yeast
Skimmed powdered milk
Whole soybean flour
Parmesan Cheese
Wheat germ
Peanuts
Chicken
Fish
Beef meat

Crude Protein %
65
47
45
37
36
36
27
26
24
22
22
12

Ali et al.

Int J Pharm Pharm Sci, Vol 4, Issue 3, 9-15

Table 2: Vitamins in Spirulina powder7


Vitamins
Provitamin A
(-carotene)
Vitamin E
Thiamin B1
Riboflavin B2
Niacin B3
Vitamin B6
Vitamin B12
Folic acid
Biotin
Phantothenic acid
Vitamin K

mg 100 g-1
2.330.000 IU kg 1
140
100 a-tocopherol eq:
3.5
4
14
0.8
0.32
0.01
0.01
0.1
2.2

Table 3: Fatty acid composition of Spirulina platensis powder29

Fatty acid
(C14) Myristic acid
(C16) Palmitic acid
(C16:1)D9 Palmitoleic acid
(C18:1)D9 Oleic acid
(C18:2)D9,12 Linoleic acid
(C18:3)D9,12,15 g-Linolenic acid
Others

Fatty acids (%)


0.23
46.07
1.26
5.26
17.43
8.87
20.88

Table 4: Minerals in Spirulina powder7

Mineral
Calcium
Chromium
Copper
Iron
Magnesium
Manganese
Phosphorus
Potassium
Sodium
Zinc

Table 5: Pigments in Spirulina powder7

Pigments
Carotenoids
Chlorophyll a
Phycocyanin

mg 100g-1
370
1000
14000

Table 6: Some commercial producers of Spirulina 48 b 32

Name of Company
Earthrise Farms

Location
Calipatria, California, USA

Myanma Microalgae
Biotechnology Project
Cyanotech Corporation

Yangon, Myanmar

Hainan DIC Microalgae Co., Ltd


Ballarpur Industries Ltd
Nao Pao Resins Chemical Co.,
Ltd

Kailua Kona, Hawaii, USA

China
Nanjangud, Mysore District,
India
Tainan, Taiwan, ROC

Neotech Food Co., Ltd

Banpong, Rajburi, Thailand

Siam Algae Co., Ltd.


Solarium Biotechnology

Thailand
La Huayca, Chile

Genix

mg 100g-1
700
0.28
1.2
100
400
5
800
1400
900
3

Cuba

Total area
Intensive ponds, total area
150.000m2

Mainly native ponds with a


total area 130.000m2
Intensive ponds, total area
100.000m2
b Total area 100.000m2
Intensive ponds, total area
54.000m2
Intensive ponds, total area
50.000m2
Intensive ponds, total area
50.000m2
b Intensive ponds, total area
45.000m2
b Total area 30.000m2
b Intensive ponds, total area
24.000m2

Production (ton)
1995: 360
1996: 400
b 2002: 450
1995: 32
1996: 40
1995: 250
1996: 300
b 2002: 330
1994 - 1995 : 25
1995 - 1996: 85
1995: 70
1996: 80
2000: 150
1995: 30
1996: 40
b 2001: 100

2002: 135
2000 (Oct-Dec): 4.5
b 2001: 28,6
b 2002 (Jan - Oct): 13
b
b

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Int J Pharm Pharm Sci, Vol 4, Issue 3, 9-15

CONCLUSION
Spirulina is claimed as a non-toxic, nutritious food, with some
corrective properties against viral attacks, anemia, and tumoral
growth and as a source of the yellow coloration of egg yolk when
consumed by hens, and growth. This contains proteins,
carbohydrates, essential fatty acids, vitamins, minerals, carotenes,
chlorophyll a and phycocyanin. There has been a significant change
in functional properties of Spirulina under stressed conditions (salt
and heat). Awareness of the better nutritional quality of sea food
proteins and lipids will soon make them a major source of protein in
the human diet.

14.
15.
16.

REFERENCES
1.
2.
3.
4.
5.

6.
7.
8.
9.
10.

11.
12.
13.

Ayala, F. Gua sobre el cultivo de Spirulina. In: Biotecnologa de


Microorganismos Fotoauttrofos. Motril, Granada, Espaa.1998,
p. 3-20.
Ayehunie, S., Belay, A., Baba, T.W., Ruprecht, R.M. Journal of
Acquired Immune Deficiency Syndromes and Human
Retrovirology Volume 18, Issue 1, 1 May 1998, Pages 7-12 .
Baicus, C., Baicus, A. Spirulina did not ameliorate idiopathic
chronic fatigue in four N-of-1 randomized controlled trials.
Phytotherapy Research Volume 21, Issue 6, June 2007, Pages
570-573
Balachandran, P., Pugh, N.D., Ma, G. and Pasco, D.S. Toll-like
receptor 2-dependent activation of monocytes by Spirulina
polysaccharide and its immune enhancing action in mice ,
International Immunopharmacology ,Volume 6, Issue 12, 5
December 2006, Pages 1808-1814.
Balloni, W., Tomaselli, L., Giovanetti, L. and Margheri, M.C.
1980. Biologia fondamentale Del genere Spirulina. In:
Cantarelli, C., Ciferri, O., Florenzano, G., Kapsiotis, G., Materassi,
R., Treccani, U., Eds. Progetto finalizzato Ricerca di nuove fonti
proteiche e di nuove formulazioni alimentari. Atti del
Convegno: Prospettive della coltura di Spirulina in Italia.
Consiglio Nazionale delle Richerche. Firenze-Academia dei
Georgofili, CNR, Tipografia Coppini; pp.49-82.
6.Baojiang G., et al. Study on Effect and Mechanism of
Polysaccharides of Spirulina platens is on Body Immune
Functions Improvement. Second Asia-Pacific Conference on
Algal Biotechnology, April 25-27, 1994, p. 24.
Belay, A. 1997. Mass culture of Spirulina outdoors The
Earthrise Farms experience. In: Vonshak, A., Ed. Spirulina
platensis (Arthrospira): Physiology, cell-biology and
biotechnology. Taylor and Francis. London. pp. 131-158.
Becker, E.W. 1984. Nutritional properties of microalgal
potentials and constraints. In: Richmond A, Ed. Handbook of
microalgal mass culture. CRC Press, Inc, Boca Ratn; pp. 339408.
Binbin Zhao, Jia Wang, Hongmei Gong, Xiaogang Wen, Haiyun
Ren and Congming Lu. Effects of heat stress on PSII
photochemistry in a cyanobacterium Spirulina platensis.
Plant Science Volume 175, Issue 4, October 2008, Pages 556564.
Carrieri, D., Momot, D., Brasg, I.A., Ananyev, G., Lenz, O., Bryant,
D.A. Dismukes, G.C. Boosting autofermentation rates and
product yields with sodium stress cycling: Application to
production of renewable fuels by cyanobacteria. Applied and
Environmental Microbiology, Volume 76, Issue 19, October
2010, Pages 6455-6462.
Castenholz, R.W., and Waterbury, J.B. Oxygenic photosynthetic
bacteria. Section 19, In: Staley, J.T., Bryant, M.P., Pfenning, N.,
Holt, J.G., Eds. Bergeys Manual of Systematic Bacteriology. Vol.
3, Williams and Wilkins Co, Baltimore, USA.1989, pp 17101806.
Chu, W.L., Lim, Y.W., Radhakrishnan, A.K., Lim, P.E. Protective
effect of aqueous extract from Spirulina platens is against cell
death induced by free radicals, BMC Complementary and
Alternative Medicine Volume 10, 21 September 2010, Article
number 53 .
Ciferri, O. 1983. Spirulina, the edible microorganism. Microbiol.
Rev. 47:551-578. Cordella, I. Moussa, A.C. Martel, N.
Sbirrazzuoli and L. Lizzani-Cuvelier, Recent developments in
food characterization and adulteration detection: Technique-

17.
18.
19.

20.
21.
22.
23.

24.
25.
26.
27.

28.
29.
30.

oriented perspectives, Journal of Agricultural and Food


Chemistry 50 (7) (2002), pp. 17511764.
Duda-Chodak, Aleksandra, Wajda, Lukasz, Kubica, Maria,
Uniwersytet Rolniczy W Krakowie, Wplyw Bakterii Rodzaju
Arthrospira Na Funkcjonowanie Ukladu Immunologicznego.
Post. Mikrobiol. 2010. 49 (1):15-23.
F. Jiang, S.J. Roberts, S. Datla and Dusting, G.J. NO modulates
NADPH oxidase function via heme oxygenase-1 in human
endothelial cells. Hypertension 48 (5) (2006), pp. 950957.
G. Chamorro, M. Perez-Albiter, N. Serrano-Garcia, J.J. MaresSamano and P. Rojas. Spirulina maxima pretreatment partially
protects
against
1-methyl-4-phenyl-1,
2,
3,
6tetrahydropyridine neurotoxicity, Nutr Neurosci 9 (56)
(2006), pp. 207212.
Geitler, L. Cyanophyceae. In R. Kolkwitz(ed.), L. Rabenhorst's
Kryptogamen-Flora von Deutschland, Osterreich und der
Schweiz, vol. 14. Akademische Verlag, Leipzig.1932,p.916-931.
Girardin-Andrani, C. Spirulina: Blood supply, immune system
and cancer. Facult Chirurgie Dentaire de Nancy. Facult de
Mdecine de Lyon, Laboratoire Phytocorsa, Route de Pinarello,
Sainte-Lucie-de-Porto-Vecchio, France. Phytotherapie ,Volume
3, Issue 4, August 2005, Pages 158-161 .
Guglielmi, G., Rippka, R., and Tandeu de Marsac, N. Main
properties that justify the different taxonomic position of
Spirulina sp. and Arthrospira sp. among cyanobacteria. In:
Doumenge, F., Durand-Chastel, H., Toulemont, A., Eds. Spiruline
algue de vie. Bulletin de lInstitut Ocanographique Monaco.
Muse Ocanographique. Numro spcial,1993, 12:13-23.
Henrikson, R. Microalga Spirulina, superalimento del futuro.
Ronore Enterprises. 2 ed. Ediciones Urano, Barcelona,
Espaa.1994, pp. 222.
Hongmei Gong, Yunlai Tang, Jia Wang, Xiaogang Wen, Lixin
Zhang and Congming Lu. Characterization of photosystem II in
salt-stressed cyanobacterial Spirulina platens is cells.
Biochimica et Biophysica acta 1777:2008, pp. 488-495.
Hongyan Wu, Leyla Abasova, Otilia Chereg, Zsuzsanna Dek,
Kunshan Gao and Imre Vass. D1 protein turnover is involved in
protection of Photosystem II against UV-B induced damage in
the cyanobacterium Arthrospira (Spirulina) platensis January
2011.
Jourdan, Journal of Photochemistry and Photobiology B:
Biology. Solarium Spirulina farm in the Atacama Desert (North
Chile). In: Doumenge, F., Durand-Chastel, H., Toulemont, A.,
Eds. Spiruline algue de vie. Bulletin de lInstitut
Ocanographique Monaco. Muse Ocanographique. Numro
spcial,1993, 2:191-194.
Karadeniz, A., Cemek, M. and Simsek, N. The effects of Panax
ginseng and Spirulina platens is on hepatotoxicity induced by
cadmium in rats. Ecotoxicology and Environmental Safety
January 2009, 72(1): pp. 231-235.
Karkos, P.D. , Leong, S.C., Karkos, C.D., Sivaji, N. and
Assimakopoulos, D.A. Spirulina in clinical practice: Evidencebased human applications, Evidence-based Complementary
and Alternative Medicine. Volume 2011: Article number
531053.
Lacaz, R., and Nascimento, E. Produo de biomassa de
Spirulina mxima para alimentao humana e animal. Rev
Microbiol,1990,21:85-97.
Mao, T.K., Van De Water, J., Gershwin, M.E. Effects of a
Spirulina-based dietary supplement on cytokine production
from allergic rhinitis patients. Division of Rheumatology,
University of California at Davis, School of Medicine, Davis, CA,
United States. Journal of Medicinal Food Volume 8, Issue 1,
March 2005, Pages 27-30.
28.M.F. McCarty, Iatrogenic Gilbert sydrome a strategy for
reducing vascular and cancer risk by increasing plasma
unconjugated bilirubin, Med Hypoth 69 (2007), pp. 974994.
29.Misbahuddin, M. , Maidul Islam, A., Khandker, S., Ifthaker-AlMahmudc, Islam, N., Anjumanara.Efficacy of Spirulina extract
plus zinc in patients of chronic arsenic poisoning: A
randomized placebo-controlled study. Clinical Toxicology,
Volume 44, Issue 2, 1 April 2006, Pages 135-141 .
Meenakshi Choudhary, Umesh Kumar Jetley, Mohammed Abash
Khana, Naina Zutshi and Tasneem Fatma. Effect of heavy metal
14

Ali et al.

31.

32.
33.
34.
35.

36.
37.
38.
39.

stress on proline, malondialdehyde, and superoxide dismutase


activity in the cyanobacterium Spirulina platensis-S5.
Ecotoxicology and Environmental Safety, Volume 66, Issue 2,
February 2007, Pages 204-209.
Othes, S., and Pire, R. Fatty acid composition of Chlorella and
Spirulina microalgae species. J. AOAC Int2001. 84: 1708-1714.
Pelizer,L.H. Pelizer, E.D.G. Danesi, C.D. Rangel, C.E.N. Sassano,
J.C.M. Carvalho, S. Sato and I.O. Moraes, Influence of inoculum
age and concentration in Spirulina platens is cultivation,
Journal of Food Engineering 56 (4), 2003,pp. 371375.
Puyfoulhoux, G., Rouanet, J.M,, Besancon, P., Baroux, B., Baccou,
J.C., and Caporiccio, B.Iron availability from iron-fortified
Spirulina by an in vitro digestion/Caco-2 cell culture model. J
Agric Food Chem.2001, 49: 1625-29.
Reid et al.,L.M. Reid, C.P. ODonnell and G. Downey, Recent
technological advances for the determination of food
authenticity, Trends in Food Science and Technology 17 (7)
(2006), pp. 344353.
Richmond, A. Mass culture of cyanobacteria. In: Mann, N., Carr,
N., Eds. Photosynthetic prokaryotes. 2nd Ed. Plenum Press,
New York and London. pp. 181-210. Romay et al. (1998)
Antioxidant and anti-inflammatory properties of Cphycocyanin from blue-green algae. Inflamm Res
1992,47(1):36-41.
Saleh, A.M, P.K. Singh and Dolly Wattal Dhar. Comparative caroten content of Spirulina strains at different days of
incubation. The Andhra Agric.2008, J 55(1): 61-62 .
Saxena, P.N., Ahmad, M.R., Shyan, R., and Amla, D.V. Cultivation
of Spirulina in sewage for poultry feed. Experientia,1983,
39:1077-1083.
Shalaby, E.A., Shanab, S.M.M. and Singh, V. Salt stress
enhancement of antioxidant and antiviral efficiency of Spirulina
platensis.
Journal
of
Medicinal
Plant
Research
Volume 4, Issue 24, 18 December 2010, Pages 2622-2632 .
Shekharam, K., Ventakaraman, L., and Salimath, P.Carbohydrate
composition and characterization of two unusual sugars from

Int J Pharm Pharm Sci, Vol 4, Issue 3, 9-15

40.
41.

42.

43.

44.
45.
46.

47.
48.
49.
50.

the blue-green algae Spirulina platens is. Phytochem,1987,


26:2267-2269.
Stanier, R.Y., and Van Niel, Y. The concept of a bacterium. Arch.
Mikrobiol. 42:17-35. Switzer, L. 1980. Spirulina, the whole food
revolution. Proteus Corporation, USA; 1962,pp. 1-69.
Switzer, L. Spirulina, the whole food revolution. Proteus
Corporation, USA;1980, pp. 1-69.
Tomaselli, L., Palandri, M. and Tredici, M.on the correct use of
Spirulina designation. Algological Studies,1996, 83:539-548.
Van Eykelenburg, C. The ultrastructure of Spirula platensis in
relation to temperature and light intensity.Antonie van
Leeuwenhoek J. Microbiol. Serol.1979,45:369-390.
Van Eykelenburg, C.Rapid reversible macromorphological
changes
in
Spirulina
platensis.
Naturwissenschaften.1980,67:200-201.
Van Eykelenburg, C. Some theoretical considerations on the in
vitro shape of the cross-walls in Spirulina spp. J. Theor.
Biol.1980, 82:271-282.
Van Eykelnburg, C., Fuchs, A. and Schmidt, G.H.Anatomie Van
Leewenbokek,1989, 45, 369.
Vonshak, A.Appendices. In: Vonshak, A., Ed. Spirulina platensis
(Arthrospira): Physiology, Cell biology and Biotechnology.
Taylor and Francis, London, Great Britain; 1997,pp. 213- 226.
Vonshak, A. and Tomaselli, L.Arthrospira (Spirulina):
Systematics and ecophysiology. In: Whitton, A., Potts, M., Eds.
The Ecology of Cyanobacteria. Kluwer Academic Publishers.
The Netherlands,2000,pp. 505-522.
Whitton, B. Diversity, ecology and taxonomy of the
cyanobacteria. In: Mann N, Carr N, Eds. Photosynthetic
prokaryotes. Plenum Press,1992, pp. 1-37.
Wu, L.C. , Ho, J.A.A., Shieh, M.C. and Lu, I.W. Department of
Applied Chemistry, National Chi-Nan University, Puli, Nantou,
Taiwan..Antioxidant and Antiproliferative activities of Spirulina
and Chlorella water extracts. Journal of Agricultural and Food
Chemistry Volume 53, Issue 10, 18 May 2005, Pages 42074212.

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