Spirulina – From growth to nutritional product: A review

Abstract

Background Spirulina is multicellular and filamentous cyanobacteria that have achieved a considerable popularity in the health sector, food industry and aquacultures. It develops and grows in water, can be harvested and processed easily. It has very high content of macro and micronutrients, essential amino acids, proteins, lipids, vitamins, minerals and anti-oxidants. Spirulina is considered as a complete food supplement to fight against malnutritional deficiencies in developing countries. Spirulina is deemed safe for human consumption as evident by its long history of food use and latest scientific findings. In recent years, Spirulina has gathered enormous attention from research fraternity as well as industries as a flourishing source of nutraceutical and pharmaceuticals. Scope and approach The primary objective of this paper is to review the utilization of Spirulina as a dietary supplement in the food industry. In the present work, the three main area of Spirulina research: growth, harvesting and potential application are presented. Key findings and conclusion The important growth parameters have been studied to enhance Spirulina biomass productivity qualitatively and quantitatively. This review provides useful information on commercially viable technology for Spirulina cultivation. Mass cultivation and Innovative formulations are further needed to fortify conventional foods with Spirulina based protein system.

Full text

Review
Spirulina eFrom growth to nutritional product: A review
Ruma Arora Soni
a
, K. Sudhakar
a
,
c
,
*
, R.S. Rana
b
a
Energy Centre, Maulana Azad National Institute of Technology, Bhopal, M.P, India
b
Department of Mechanical Engineering, Maulana Azad National Institute of Technology, Bhopal, M.P, India
c
Faculty of Mechanical Engineering, Universiti Malaysia Pahang, 26600 Pahang, Malaysia
article info
Article history:
Received 12 April 2017
Received in revised form
18 June 2017
Accepted 25 September 2017
Available online 28 September 2017
Keywords:
Spirulina
Pharmaceutical
Nutritional use
Dietary supplement
Open pond
PBR
abstract
Background: Spirulina is multicellular and filamentous cyanobacteria that have achieved a considerable
popularity in the health sector, food industry and aquacultures. It develops and grows in water, can be
harvested and processed easily. It has very high content of macro and micronutrients, essential amino
acids, proteins, lipids, vitamins, minerals and anti-oxidants. Spirulina is considered as a complete food
supplement to fight against malnutritional deficiencies in developing countries. Spirulina is deemed safe
for human consumption as evident by its long history of food use and latest scientificfindings. In recent
years, Spirulina has gathered enormous attention from research fraternity as well as industries as a
flourishing source of nutraceutical and pharmaceuticals.
Scope and approach: The primary objective of this paper is to review the utilization of Spirulina as a
dietary supplement in the food industry. In the present work, the three main area of Spirulina research:
growth, harvesting and potential application are presented.
Key findings and conclusion: The important growth parameters have been studied to enhance Spirulina
biomass productivity qualitatively and quantitatively. This review provides useful information on
commercially viable technology for Spirulina cultivation. Mass cultivation and Innovative formulations
are further needed to fortify conventional foods with Spirulina based protein system.
©2017 Elsevier Ltd. All rights reserved.
1. Introduction
Algae are photosynthetic organisms that convert light energy
from the sun into the chemical energy by the process of photo-
synthesis. Algae possess simple reproductive structure. The
biomass of algae contains various compounds with diversified
structures and functions. Algal biotechnology is divided into
microalgae, macroalgae and cyanobacteria with its unique speci-
ficity (Becker, 2007). Sometimes cyanobacteria are also included in
microalgae. Microalgae classification includes prokaryotic and
eukaryotic unicellular and multicellular. Microscopic are micro-
algae, Cyanobacteria, are prokaryotic. The Spirulina is Earth's oldest
living plant approximately 3.6 billion years ago and a first photo-
synthetic life form that has created our oxygen atmosphere so all
life could evolve. Blue-green algae are the evolutionary bridge be-
tween green plants and bacteria. At present the main directions in
microalgal biotechnology are biofuels, agricultural biostimulants
for crop plants, waste water treatment etc. Microalgal bio-
technologies refer to the production of different products as
phycocyanin, carotenoids, fatty acids and lipids for application in
health food, cosmetics, food supplements, pharmaceuticals and
fuel production. Microalgal groups of major importance are chlor-
ophyte, bacillariophytes, while macroalgae are harvested from
natural habitats. Algae that is currently cultivated for its maximum
protein content is the cyanobacterium species Athrospira, which is
commonly known as Spirulina.
Spirulina was first discovered by Spanish Scientist Hernando
Cortez and Conquistadors in 1519. Cortez observed that Spirulina
was eaten at the tables of the Aztecs during his visit in Lake Texcoco
in the Valley of Mexico. Pierre Dangeard discovered the health
benefits of Spirulina who observed that flamingos were surviving
by consuming blue-green algae. Botanist Jean Leonard supported
the findings of Dangeard and people soon started to commercialize
Spirulina to reap its benefits (Ugwu, Aoyagi, &Uchiyama, 2008).
The first Spirulina processing plant, Sosa Texcoco, was set up in
1969 by the French.
Spirulina is the most nutritious, concentrated food that is known
*Corresponding author. Energy Centre, Maulana Azad National Institute of
Technology, Bhopal, M.P, India.
E-mail addresses: rumaarora14@gmail.com (R.A. Soni), sudhakar.i@manit.ac.in
(K. Sudhakar).
Contents lists available at ScienceDirect
Trends in Food Science &Technology
journal homepage: http://www.journals.elsevier.com/trends-in-food-science-
and-technology
https://doi.org/10.1016/j.tifs.2017.09.010
0924-2244/©2017 Elsevier Ltd. All rights reserved.
Trends in Food Science &Technology 69 (2017) 157e171

to mankind containing antioxidants, phytonutrients, probiotics,
and nutraceuticals. Spirulina is fast emerging as a complete answer
to the varied demands due to its imposing nutrient composition
which can be used for therapeutic uses. The United Nations world
at food conference declared that Spirulina as the best food for
future, and it is gaining popularity nowadays (Pulz &Gross, 2004).
World Health Organization has described spirulina as Mankind's
best health product. According to UNESCO, spirulina is most ideal
food for tomorrow. According to NASA and European Space Agency,
it is one of the primary foods that can be cultivated in long-term
space missions in space. FDA validated it as “One of the best pro-
tein source”. Intergovernmental institution permitted for the use of
Micro-algae Spirulina against Malnutrition (IIMSAM).
The two most important species of Spirulina are Spirulina max-
ima and Spirulina platensis. It has a considerable high content of
micro and macronutrients. Its dry weight chemical composition
includes 60e70% proteins, carbohydrates, vitamins like provitamin
A, vitamin C, vitamin E, minerals such as iron, calcium, chromium,
copper, magnesium, manganese, phosphorus, potassium, sodium
and zinc. Essential fatty acids
g
-linolenic acid (GLA), pigments like
chlorophyll a, phycocyanin and carotenes are also present. Spirulina
is also used in cosmetics, medicines and waste water treatment. Its
cell wall consists of polysaccharides that have a digestibility of 86%,
and can be easily absorbed by the human body (Sjors &Alessandro,
2010). These microalgae contain chlorophyll a, like higher plants;
therefore it is classified as microalgae according to botanists
belonging to Cyanophyceae class; and bacterium due to its pro-
karyotic structure according to bacteriologists (Koru, 2009;
Sudhakar &Premalatha, 2015).
Spirulina is a planktonic photosynthetic cyanobacterium that
forms huge populations in tropical as well as subtropical bodies of
water which contain a high amount of salts such as carbonate and
bicarbonate with alkaline pH 9.5(Sjors &Alessandro, 2010; Habib,
Parvin, Huntington, &Hasan, 2008, pp. 1e41). Generally, micro-
algae have higher growth rates, higher CO
2
fixation efficiency and
larger quantities of high-value products, such as dietary supple-
ments for human along with animals (Anupama, 2000; Zeng,
Danquah, Chen, &Lu, 2011). Cost effectiveness and composition
of cultivation media along with growth rate needs to be managed
properly for commercially viable production. From ancient times
different media have been used for cultivation of Spirulina and
monitoring its growth rate i.e. Zarrouk's media (Zarrouk, 1966),
Rao's media, CFTIR media, OFERR media, revised media (Raoof,
Kaushika, &&Prasanna, 2006).
Past few decades have seen considerable progress in spirulina
cultivation for nutritional use however there is no substantial
argument on the nutritional productivities, best cultivation
method, and ideal growth conditions. This review addresses these
issues based on prior publications and the author's prior work in
the large scale cultivation of spirulina for nutritional products. The
article starts with the illustration of spirulina growth chain from
identifying suitable strain to the final product.
The present study focuses on growth rate, productivity, growth
parameters, different cultivation systems (outdoor and indoor
systems), harvesting and drying techniques of Spirulina. This re-
view focuses on following aspects:
Strain selection and cultivation of Spirulina.
Optimum parameters for growth of Spirulina.
Harvesting and drying techniques of Spirulina.
Commercial applications of Spirulina as pharmaceutical and
nutraceuticals product.
2. Review of growth system
Cultivation of algae can be done in open systems like ponds,
lakes or lagoons or in a closed system (Singh and Sharma 2012).
Presently, two major technologies are being considered for the
cultivation of Spirulina: closed photobioreactors (PBR) and open
ponds. Both approaches are used commercially to produce high-
value products.
2.1. Open pond system
Cultivation of algae in open ponds has been extensively studied
(Vardaka, Kormas, Katsiapi, Genitsaris, &Moustaka-Gouni, 2016;
Zhang et al., 2015; Madhu, Satyanarayana, Kalpana, &Bindiya,
2015;Vega-Estrada, Montes-Horcasitas., Dominígues-Bocanegra, &
Ca~
nizares-Villanueva, 2005). Open ponds can be categorized into
natural waters as lakes, lagoons, ponds and artificial ponds or
containers. The most commonly used systems are shallow big
ponds, circular ponds, tanks and raceway ponds. Open systems are
easier in construction and operation, results in low production and
operating cost (Ugwu et al., 2008). The major drawback in open
ponds includes poor light utilization by the cells, evaporative losses,
diffusion of carbon dioxide to the atmosphere, and requirement of
large acres of land. Also, due to inefficient aeration in open culti-
vation systems, their mass transfer rates are very poor resulting in
less biomass productivity. The growth also depends on location,
season, temperature, pH level, nutrient and carbon - dioxide supply
(Cuaresma, Janseen, &VilchezWijffels, 2011). The other major
drawback of open pond system is the contamination by fauna and
other fast growing heterotrophs. To expel the problems associated
with an open system, researchers have tried for closed systems
(Singh and Sharma 2012).
Table 1 summarizes the advantages and limitations of open
ponds, photobioreactors and hybrid system. Large quantities of
algae can be grown but they are difficult to grow outdoor as they
easily get contaminated. This can be rectified by growing algae in
greenhouses, which protect them from foreign particles in the air.
The optimally designed algae greenhouse and controlled environ-
ment systems can increase productivity 10 fold compared to out-
door growth. Construction of greenhouse includes design and
optimizing for improved biomass yield. Controlled environment
algae facilities are gaining momentum due to improved yields and
reduced contamination. The internal systems to control the internal
humidity, temperature, and carbon dioxide through the use of fans,
vents, evaporative cooling, and climate zoning is done (Sierra,
Acien, Fernandez, Garcıa, &GonzalezMolina, 2008). pH, nutrients,
and bacteria are regulated in the water system through fertigation,
oxygenation and also sterilization. Integrating the climatic condi-
tions, water, and nutrient systems with simulation allows us to
Nomenclature
(P
X
) Cell productivity
(T
C
) Cultivation time
G
Productivity of the system
m
Specific growth rate
x Biomass concentration
(X
m
-X
i
) Cell concentration
N
0
Initial population size
t Amount of time that has past
N
t
Population size at time
G Generation time
N.S Not Specified
R.A. Soni et al. / Trends in Food Science &Technology 69 (2017) 157e171158

provide exactly what that algae facility needs, resulting in opti-
mized yields. The open roof greenhouses design provides complete
protection against undesirable weather conditions, while the full
vertical vent promotes optimum light and air movement.
Fig. 1 illustrates the flowchart for Spirulina cultivation phases
(from Phase a ePhase e) from strain selection to pellets formation.
2.2. Photobioreactors
A photobioreactor can be an enclosed, illuminated culture vessel
designed for controlled biomass production. Photobioreactor refers
to closed systems that are closed to the environment having no
direct exchange of gases and contaminants with the environment.
The closed system commonly called as photobioreactors, is closed
equipment which provides a controlled environment and also re-
sults in high productivity of algae. Photobioreactors facilitate better
control of culture environments such as carbon dioxide supply,
water supply, optimal temperature, efficient light intensity, culture
density, pH levels, gas exchange, aeration and culture density. Algal
culture systems can be illuminated by artificial or natural light or by
both. Naturally illuminated algal culture systems with large illu-
mination surface areas include open ponds (Hase, Oikawa, Sasao,
Morita &Watanabe, 2000), flat-plate (Hu, Guterman, &
Richmond, 1996), horizontal/serpentine tubular airlift (Camacho
Rubio, Aci
enFern
andez, S
anchezP
erez, García Camacho, &Molina
Grima, 1999), and inclined tubular photobioreactors (Ugwu,
Ogbonna, &Tanaka, 2002). In order to overcome the problems
with open ponds, much attention is now focused on the develop-
ment of suitable closed systems such as flat-plate, tubular, vertical
column and internally-illuminated photobioreactor. Generally,
laboratory-scale photobioreactors are illuminated artificially
internally or externally using fluorescent lamps or other light
providers. Some of these photobioreactors include bubble column
(Degen, Uebele, Retze, Schmidt-Staigar, &Trosch, 2001; Ogbonna,
Ichige, &Tanaka, 2002; Ugwu et al., 2002), airlift column
(ChiniZittelli, Rodolfi,&Tredici, 2003; Harker, Tsavalos, &Young,
1996), stirred-tank (Kaewpintong, Shotipruk, Powtongsook, &
Pavasant, 2007), helical tubular (Ogbonna, Soejima, &Tanaka,
1999) conical (Hall, Fernandez, Guerrero, Rao, &Grima, 2003),
torus (Watanabe &Saiki, 1997), and seaweed type (Pruvost, Pottier,
&Legrand, 2006) photobioreactors. Some photobioreactors can be
easily tempered. Large scale outdoor systems mainly tubular
photobioreactors cannot be easily tempered without high technical
efforts. Efforts have been taken in designing temperature-
controlled photobioreactors, such as double-walled internally-
lighted photobioreactor with both heating as well as cooling water
circuit (Chetsumon et al., 1998). Photobioreactors, despite their
costs, have several major advantages over open systems (Tsoglin,
Gabel, Fal’kovich, &Semenenko, 1996).
Photobioreactors minimize the contamination and allow hyge-
nicalgal cultivation of monocultures.
Photobioreactors offer better control over conditions such as pH,
temperature, light intensity, carbon dioxide concentration etc.
Photobioreactors reduce carbon dioxide loss.
Photobioreactors prevent water evaporation.
Photobioreactors permit higher cell concentrations.
Photobioreactors enhance the production of complex
biopharmaceuticals.
PBR permits the cultivation of various microalgal species.
PBR design provides the uniform illumination of the culture
surface and the fast mass transfer of carbon dioxide and oxygen.
PBR has a minimum non-illuminated part.
2.2.1. Vertical-column PBR
Vertical-column photobioreactors are easy to operate compact
and low-cost (Mir
on, Garcıa, Camacho, Grima &Chisti, 2002).
Various designs and scales of vertical column photobioreactors
have been reported for the cultivation of algae (Vega-Estrada et al.,
2005; Kaewpingtong et al., 2007) which are very promising for
large-scale cultivation. It was reported that bubble-column and
airlift photobioreactors (up to 0.19 m in diameter) can attain a final
biomass concentration and a specific growth rate that are compa-
rable to tubular photobioreactors (Gallardo-Rodríguez et al., 2012).
Some bubble column photobioreactors are equipped with either
draft tubes or constructed as split cylinders.
2.2.2. Flat plate PBR
For cultivation of photosynthetic microorganisms flat-plate
photobioreactors have received much consideration due to their
large illumination surface area. The work reported paved a way to
use flat culture vessels for the cultivation of algae (Samson &Leduy,
1985). A flat reactor was developed and equipped with fluorescence
Table 1
Comparison between Spirulina production in open, closed and hybrid system (Roberto, 2015).
Factor Open systems (raceway ponds) Closed systems (photobioreactors) Hybrid system
(Open Pond þPBR)
Space required High Low High
Area/volume ratio Low (5e10 m
1
) High (20e200 m
1
) Variable
Evaporation High No evaporation Minimized
Water loss Very high Low Less
CO
2
-loss High Low Minimizes
Temperature Highly variable Required cooling Controlled
Weather dependence High Low Low
Process control Difficult Easy Difficult
Cleaning Easy Required Difficult
Biomass quality Variable Reproducible Better
Population density Medium High Medium
Harvesting efficiency Medium High High
Harvesting cost High Lower High
Light utilization efficiency Poor Good Better
Most costly parameters Mixing Oxygen and temperature control Temp control
Contamination control Difficult Easy Easy
Capital investments Low High Low
Productivity Low 3e5 times more productive 5-7 times more productive
Hydrodynamic stress on Spirulina Very low Lowehigh Low
R.A. Soni et al. / Trends in Food Science &Technology 69 (2017) 157e171 159

lamps (Ramos de Ortega and Roux 1986). After this, an outdoor flat
panel reactor was developed using thick transparent PVC materials
(Tredici &Materassi,1992). Later extensive works were reported on
various designs of flat plate reactors and vertical panels for mass
cultivation of different algae (Hu et al., 1996; Zhang, Kurano, &
Miyachi, 2002; Hoekema, Bijmans, Janssen, Tramper, &Wijffels,
2002; Olguín, Galicia, Mercado, P
erez, 2003). Flat plate photo-
bioreactors are constructed using transparent materials for
maximum utilization of solar light. Accumulation of dissolved ox-
ygen concentrations in horizontal tubular photobioreactors is
relatively high as compared to flat-plate photobioreactors. It has
been reported that high photosynthetic efficiencies can be achieved
with flat-plate photobioreactors (Hoekema et al., 2002; Olguín
et al., 2003). Overview of spirulina productivities reported in the
literature for various growth systems is presented in Table 2.
Among all culture systems productivity of Spirulina platensis is
highest in raceway ponds. The areal productivity is generally based
on one-hectare ground surface area.
2.2.3. Tubular PBR
A tubular photobioreactor is the most suitable types of bio-
reactors for outdoor mass cultivation (Kaewpington et al., 2007).
Mostly outdoor tubular photobioreactors are constructed either
with glass or plastic tube. They can be horizontal/serpentine
Fig. 1. Different phases of Spirulina cultivation system (a) strain selection (b) Growth systems (c) growth parameters (d) Harvesting system (e) Final product as capsules or pellets.
R.A. Soni et al. / Trends in Food Science &Technology 69 (2017) 157e171160

(Chaumont, Thepenier, &Gudin, 1988; Molina, Fern
andez, Aci
en, &
Chisti, 2001; Pirt et al., 1983; Watanabe &Saiki, 1997), vertical
(Tredici &ChiniZittelli, 1998)conical(Lee &Low, 1991) inclined
(Torzillo et al., 1986; Ugwu et al., 2002). Mixing and aeration of the
cultures in tubular photobioreactors are usually done by air-pump or
airlift systems. Mass transfer becomes a problem when tubular
photobioreactors are scaled up. Many have reported that very high
dissolved oxygen (DO) levels are easily reached in tubular photo-
bioreactors (Gallardo-Rodríguez et al., 2012;Pirt et al., 1983;
Richmond, Boussiba, Vonshak, &Kopel, 1993; Ugwu, Ogbonna, &
Tanaka, 2003, 2005a). It is difficult to control culture temperatures
in most tubular photobioreactors. They can be equipped with a
thermostat to maintain the desired culture temperature and it could
be very expensive and there will be difficulties in implementing.
2.2.4. Internally-illuminated PBR
These photobioreactors can be internally illuminated with
fluorescent lamps. Air and CO
2
are supplied to the cultures through
the spargers with continuous agitation by impellers. This photo-
bioreactor can also be modified in such a way that it can utilize both
solar and artificial light system (Ogbonna et al., 1999). The artificial
light source is used whenever the solar light intensity decreases
below a set value as during cloudy weather or at night. It has been
reported, on the use of optic fibers to collect and distribute solar
light in cylindrical PBR (Matsunaga et al., 1991; Mori, 1985). A major
advantage of internally-illuminated photobioreactor is that it can
be heat-sterilized under pressure and by this contamination can be
minimized. A continuous supply of light to the photobioreactor can
be maintained both day and night by integrating artificial and solar
light devices. Outdoor mass cultivation of algae in this type of
photobioreactor would have some technical difficulties. Flat plate
photobioreactors are generally more efficient in sunlight utilization
than tubular photobioreactors because they have a wider surface
area. Most early tubular PBRs used tubes 10e30 cm in diameter, but
almost all tubular reactors used now have a tube diameter of 4 cm.
The narrower tube diameter not only improves the light utilization
efficiency, but also provides more mixing, which enhances growth
(Tredici, 2004). In photobioreactors (PBRs), the microalgae get ad-
heres to the transparent surfaces which lead to biofouling and
along with it reduces the solar radiation penetration the PBR. Light
intensity reduction within the PBR reduces the biomass produc-
tivity which also reduces the photosynthetic efficiency of the
Spirulina cultivation system. Adherence of the cells to wall tubes is
very common in tubular photobioreactors. Designing of photo-
bioreactor surfaces with proper materials, functional groups or
surface coatings, to prevent microalgal adhesion is essential for
solving the biofouling problem. Such a significant advance in
microalgal biotechnology would enable extended operational pe-
riods at high biomass productivity and depreciate the maintenance
costs (Zeriouh et al., 2017).
2.3. Hybrid system
A hybrid type of photobioreactor is most widely used to exploit
the advantages of the two different types of reactor and overcome
the disadvantage of other. Integrated airlift system and external
tubular loop placed horizontally in a thermostatic pond of water
have been reported (Zittelli, Biondi, Rodolfi,&Tredici, 2013). The
reactor had a total volume of 200 L. The external loop acts like the
light-harvesting unit and gives high surface area to volume ratio
and controls the temperature of the culture. The airlift system acts
as a degassing system where probes can also be integrated in order
to regulate the other culture variables. It has the advantage of better
control over culture variables, enabling higher productivities and
reducing power consumption (Cuaresma et al., 2011; Pohl,
Kohlhase, &Martin, 1988; Singh and Sharma 2012; Ugwu et al.,
2008). Hybrid systems have the features of open ponds and PBRs
(Hoekema et al., 2002). First can be covered open pond this concept
reduces the possibility of contamination, evaporative losses, and
CO
2
desorption. The other type is a partially filled tubular design
widened and inflated to approximate an open pond; this design is
mainly aimed at reducing costs (Hoekema et al., 2002; Olguín et al.,
2003; Tredici &Materassi, 1992). Some of the advantages and
limitations of various cultivation systems are listed in Table 3.
2.3.1. Polybags
The cultivation of algae using natural ponds is easy, but turning
it into a viable feedstock is very difficult. So to enable higher pro-
duction levels, least investments and operating costs, greater
biomass density, better climatic controlled conditions, and indus-
trial scalability, this technique can be implemented. Thin, floating,
flexible, multi-compartment photobioreactors (PBR) can be
deployed either on land, in salt water ponds or ditches, or in any
water body. The bag floats because its water is relatively less dense
than what it is floating in. Density can be controlled in different
ways, allowing the bags to be vertical to facilitate harvesting. The
productivity results have indicated that growing algae in floating
bags can be much more efficient than other cultivation methods.
Poly Bags achieve optimal light exposure with good productivity
results as they float in a cushion of water. Compared to other closed
algae systems, this PBR technology has many advantages, including
site selection, optimum temperature, low-cost materials, scalabil-
ity, optimal light intensity, high biomass concentration, low energy
consumption and effective environmental condition (Licamele and
White 2011).
The diameter of the culture vessel is inversely related to cell
density with a fixed level of light penetration. However, these bags
are superior in productivity to similar rectangular volume fiber-
glass reactors or plastic tanks. They are, nevertheless, inefficient
when compared with internally illuminated cultures. Polyethylene
bag cultures have a relatively short life because the internal surface
attracts culture trash and bacteria, which collectively reduces light
penetration and also increases contamination. At the end of a cul-
ture run it is necessary to renew the bag. Large diameter bags are
inefficient but bags less than 30 cm diameter can be effective
because the surface area to volume relationship for light penetra-
tion is improved (Algae Industry Magazine, 2012).
Table 2
Spirulina productivity and Photosynthetic efficiency.
Reactor system Location Light path Photosynthetic Efficiency Productivity (ton ha
1
yr
1
) Reference
Raceway pond La Mancha, Mexico 0.1e0.25 1.5% 43.1 (Olguín et al., 2003)
Raceway pond Florence, Italy 0.035 1.5% 20.0 (Tredici &Materassi, 1992)
Raceway pond Malaga, Spain 0.30 1.5% 23.6e30.0 (Jim
enez, Cossío, &Niell, 2003)
Raceway pond Australia 0.30 1.5% 91.0 (Borowitzka, 1999)
Horizontal Tubular Florence, Italy 0.06 1.8e3% 30.0 (Tredici &Materassi, 1992)
Flat Panel US 0.10 3.8% 22.1 (Richmond &Zhang, 2001)
R.A. Soni et al. / Trends in Food Science &Technology 69 (2017) 157e171 161

Table 3
Prospects and limitations of various cultivation systems (Chojnacka &Noworyta, 2004; Vymazal, 1990; Ugwu et al., 2008; Vree, Bosma, Janssen, Barbosa, &Wijffels, 2015; Newsted, 2004).
Culture systems Dimensions Specific growth rate Prospects Limitations Images
Open systems Variable 0.30day
1
Relatively economical, easy
to clean up after cultivation,
good for mass cultivation of algae
Little control of culture conditions, difficulty in growing
algal cultures for long periods,
poor productivity,
occupy large land mass,
limited to few strains of algae,
cultures are easily contaminated
Vertical Column
PBR
0.2 m diameter and
4 m column height
0.015 ±0.002 h
1
High mass transfer,
good mixing with low shear stress,
low energy consumption,
high potentials for scalability,
easy to sterilize,
good for immobilization of algae,
reduced photoinhibition and
photo-oxidation
Small illumination surface area,
construction require sophisticated materials,
shear stress to algal cultures,
the decrease of illumination surface area upon scale-up
Flat plate PBR 0.07 m wide,
1.5 m height, 2.5 m length
Volume 250lts
Productivity - 1.0 g/L day
Large illumination surface area,
suitable for outdoor cultures,
good for immobilization of algae,
good light path, good biomass productivities,
relatively cheap,
easy to clean up,
readily tempered,
low oxygen buildup
Scale-up require many compartments and support materials,
difficulty in controlling culture temperature,
some degree of wall growth,
the possibility of hydrodynamic stress to some algal strains
Tubular PBR D ¼3e10 cm 0.055 h
1
Large illumination surface area,
suitable for outdoor cultures,
fairly good biomass productivities,
relatively cheap
Gradients of pH,
dissolved oxygen and CO2 along the tubes, fouling,
some degree of wall growth,
requires large land space
Internally
Illuminated PBR
Not Specified Large illumination surface area,
can utilize both solar and artificial light system,
contamination can be minimized in this system
Outdoor mass cultivation of algae require some
technical efforts.
Hybrid System Not Specified Minimize microbial contamination,
maximize biomass and product yield,
Maximize CO
2
supply
Requires large areas of land and some technical efforts
Poly Bags D <30 cm 0.20day
1
site flexibility,
Low-cost materials,
easy scalability,
optimal light exposure,
isolation of the crop from predators,
very high biomass concentration,
low energy consumption
effective weather protection
Polyethylene bag cultures have a relatively short life
because the internal surface attracts culture debris and
bacteria, which collectively reduce light penetration and
are a source of contamination
R.A. Soni et al. / Trends in Food Science &Technology 69 (2017) 157e171162

3. Review of growth parameters
Spirulina growth requirements are similar to terrestrial plants but
they use these resources very efficiently to increase biomass pro-
ductivity with comparatively less water use (Sudhakar, Premalatha,
&Rajesh, 2014).
3.1. Climatic factors
Temperature is an important climatic factor influencing the rate
of growth of Spirulina. Below 17

C, growth is practically nil, but
Spirulina does not die. The optimum temperature for growth is
35

C, but above 38

CSpirulina growth is inhibited. Light is an
important factor but direct sunlight is not recommended, 30% of
full sunlight is actually better, except that more may be required to
quickly heat up the culture in the morning (Saeid &Chojnacka,
2015). Growth takes place only in the light, but illumination 24 h
a day is also not recommended. During dark periods, chemical re-
actions take place within Spirulina, like a synthesis of proteins and
respiration.
3.2. Media
Different culture media are used to start new cultures according
to the water source. The water used should be clean or filtered to
avoid growth of other algae. Water often contains enough calcium,
but if it is too hard it will cause muds. Portable water is convenient
whereas RO treated water is the best to grow Spirulina. The make-
up media mainly consist of urea. Carbonate is replaced by bicar-
bonate. Urea, certain ions may be present as sulphate, chloride,
nitrate, and sodium which is more efficient to supply nitrogen but is
highly toxic with large concentration. Spirulina can grow on either
nitrate or urea alone, but using both at the same time is
advantageous. Phosphate, magnesium and calcium cannot be
increased much. Potassium concentration can be increased
accordingly, provided it does not become more than five times the
sodium concentration. If fertilizer grade chemicals are used for cost
reduction, they should be of the soluble or crystallized type, not of
the slow release, granulated type. There are different media prep-
arations according to the local growing conditions. Most commonly
used is zarrouks media (Pragya, Pandey, &Sahoo, 2013; Zarrouk,
196 6). Chemical compositions of different growth media are
compared in Table 4.
3.3. Mother culture
For Inoculums preparation and culture maintenance fully grown
concentrated Spirulina culture is required. The chosen Spirulina
strain must have a high proportion of coiled filaments (<25%
straight filaments, or none), and at least 1% of gamma-linolenic acid
(GLA) based on dry weight. Concentrated Spirulina seed culture can
be obtained either from the floating layer of a composed culture, or
by diluting a freshly filtered biomass. Colour of the culture should
be clearly green. The growth rate is about 30%/day when the tem-
perature and other climatic conditions are adequate (Pal, Gupta, &
Tripathi, 2011). As the growth is proportional to the area of the
culture exposed to light, it is recommended to maximize this area
at all times. It is reported that minimum cell population is neces-
sary to initiate and sustain Spirulina cultures.
3.4. Mixing and aeration
Agitation of the culture is necessary to homogenize and ensure
a good distribution of lighting among all the filaments of Spirulina.
Mixing plays an important role in the productivity of ultrahigh
density cultures. Aeration is very necessary for getting good
Table 4
Chemical composition of different growth media (Madkour, Kamil, &Nasr, 2012; Atlas &Parks, 1997; Venkataraman, Bhagyalakshmi, &Ravishankar, 2005; Pandey, Tiwari, &
Mishra, 2010).
Ingredient Zarrouk's Media
(gms/l)
Rao's Media
(gms/l)
CFTRI Media
(gms/l)
OFERR Media
(gms/l)
George's Media
(gms/l)
Conventional growth
Media (gms/l)
Reduced Cost
Media (gms/l)
NaHCO
3
16.80 15 4.5 8.0 e16 16.8
K
2
HPO
4
0.50 0.50 0.5 - 0.02 e0.235
NaNO3 2.50 2.50 1.5 - ee e
K
2
SO
4
1.00 0.60 1.0 0.5 e0.5 0.353
NaCl 1.00 0.20 1.0 5.0 e1.00 0.471
MgSO
4
$7H
2
O 0.20 0.04 1.2 0.16 0.02 0.1 e
EDTA 0.08 - - - ee 0.353
CaCl
2
$2H
2
O 0.04 0.008 0.04 - e0.1 0.176
FeSO
4
$2H
2
O 0.01 - 0.01 0.05 ee 0.265
H
3
BO
3
2.86 - - 0.052 ml ee 2.86
MnCl
2
$4H
2
O 1.180 - - - ee 1.81
ZnSO
4
$7H
2
O 0.222 - - - ee 0.222
Na
2
MoO
3
$0.015 - - - ee 0.0177
CuSO
4
$5H
2
O 0.074 - - - ee 0.079
NH
4
VO
3
22.9 - - - ee e
NiSO
4
$7H
2
O 47.8 - - - ee e
NaWO
2
17.9 - - - ee e
Ti
2
(SO
4
)
3
$6H
2
O 4.4 - - - ee e
Co(NO
3
)
2
$6H
2
O 4.4 - - - ee e
Ferric citrate e- - - 0.035 ee
Peptone e- - - 1.00 ee
KNO
3
e-- - e2.00 e
(NH
4
)
2
HPO
4
e-- - e0.1 e
Chelated Iron e-- - e2 squeezes (¼teaspoon) e
Lime e-- - e0.1 e
NH4NO3 e-- - ee 0.118
CO (NH
2
)
2
e- - 0.2 ee 0.088
Fe EDTA e0.20 - - ee e
A
5
solution e1ml - - ee e
R.A. Soni et al. / Trends in Food Science &Technology 69 (2017) 157e171 163

quality and better yields of Spirulina species. It can be achieved by
rotators, which maintain the cells in suspension by gentle agitation
of growing cells. The Spirulina species produces high biomass yield
when the growth medium is aerated (bubbling with air). Aeration
gives a homogenous distribution of the Spirulina filaments
throughout the growth system for adequate exposure to illumi-
nation. It also helps to distribute carbon dioxide concentration
uniformly and removes inhibitory substances as oxygen (Dubey,
2006; Richmond &Vonshak, 1978). Aeration is, therefore, essen-
tial for the cultivation of the Spirulina filaments such as Spirulina
platensis (Famelart, Kobilinsky, Bouillamnne, &Desmazeaud, 1987;
Powls, 1985). Adequate and turbulent mixing is essential for higher
biomass productivity (Chisti, 2016,pp.21e40). Mixing of raceway
pond is effected by means of a paddle wheel. Mixing velocity of
5e60 cm/s has been used by many researchers. Low velocities
result in dead zones around corners while high velocities incur
high energy cost, and may result in shear stress that damages the
algae. It also noted that continuous mixing of the culture medium
is required to prevent cell sinking and thermal stratification. It is
also required to maintain even nutrient distribution, and to
remove excess oxygen. When aeration is not adequate, the effi-
ciency of energy utilization and biomass production will be low.
Similarly, if growth medium is not aerated, the cell on the surface
of the medium float to the surface due to the presence of air-filled
vacuoles. These cells suffer photoinhibition, resulting in low
growth or low biomass production. The optimal conditions for
spirulina were found to be at a light intensity lower than
200
m
mol m
2
s
1
,CO
2
enriched air flow (0.5%), superficial aeration
rate of 0.0056 m s
1
in a NaHCO
3
-free Zarrouk medium (Zhang
et al., 2015).
3.5. Temperature and pH
Spirulina can grow at 20

C- 37

C. The best temperature for
Spirulina growth is between 29

C-35

C. During night growth of
Spirulina is least or almost zero. It is reported that the effect of pH
on the algal growth, pigment production and protein content of
Spirulina species has the direct effect on the antioxidant system
(Ogbonda, Aminigo, &Abu, 2007; Vonshak &Guy, 1987). The
growth may be affected in two ways.
Available carbon alteration, which may interfere with
photosynthesis.
Through the disruption of cell membrane processes.
This may have a direct impact on the accumulation of antioxi-
dants (Matsunaga et al., 1991). Moreover, factors such as nutrient
availability, ionization and heavy metal toxicity have large impacts
on algal metabolism (Newsted, 2004). The fluctuation in atmo-
spheric temperature is the main factor affecting the biomass pro-
duction rates in outdoor Spirulina cultivation. In the rainy season
the culture may become contaminated due to raindrops resulting in
lowest dried mass. The physical factors which are not favorable in
monsoon can be controlled by using the locally available tech-
niques (Pandey &Tiwari, 2010). The warm humid environment
causes the bacterial contamination. The main contaminants of the
Spirulina culture were protozoan like amoeba and paramecium
which ultimately spoils the cultures. During the monsoon season
insects also appears in the culture and make it unfit for human
consumption. To reduce the effect of the low-temperature Spirulina
cultures can be kept in the house made of a plastic sheet. When pH
is between 9 and 11, it indicates a healthy culture. It also assures
that other strains are prevented from contaminating the tank as
they simply can't live in the alkaline environment that Spirulina
grows in.
3.6. Light intensity
All photoautotrophic organisms including photosynthetic bac-
teria, cyanobacteria and higher plants, convert light energy into
chemical energy through photosynthesis. It is reported that light
quality, intensity and duration are important factors of algal pro-
duction (Sudhakar &Premalatha, 2012; Lucie et al., 2016). In an
outdoor cultivation system, natural light or solar radiation is the
whole sole source of light. Light availability is totally dependent on
geographical area, climatic conditions, seasonality and local at-
mosphere. Spirulina makes its own food in the presence of optimal
light. The requirement of light intensity for growth varies from
organism to organism. Spirulina also requires a specific range of
intensity for its growth (Sudhakar, Rajesh, &Premalatha, 2012).
Zarrouks did the first detailed study on the response of Spirulina
maxima to light (Zarrouk, 1966). The optical density of the culture is
directly proportional to the light intensity. Higher the optical
density higher is the requirement of light and lower is the optical
density, lower is the requirement of light (Samuel, Sofi,&Masih,
2010). The light intensity is an important variable in cyanobac-
teria cultivation. High values of light intensity promote growth
parameters such as maximum specific growth rate, whereas low
values result in a biomass that is rich in pigments and proteins.
Outdoor algal cultures are exposed to two rhythms of the dark and
light regime. These cycles impose a unique physiological regime on
the adjustment or acclimatization of outdoor algal cells to light.
Increasing the cell concentration of culture, increases the self-
shading and results in a decrease of the growth rate of Spirulina.
The attenuation coefficient was observed to scale linearly with
microorganism density.
The irradiance attenuation coefficient at wavelength
l
,
a
l
,is
calculated according to
G
l
(z)/G
l
(0) ¼e

al
z
(1)
The Spectral Irradiances at different depths z is calculated ac-
cording to above equation knowing the value of
a
l
, The spectral
attenuation cross section, A
l
,isdefined as,
A
l
¼
al
/X (2)
Using the irradiance attenuation coefficients for each culture,
al
,
G
l
(z) ¼G
l
(0)e

al
z
(3)
Where G
l
(z) ¼spectral irradiance at depth z.
G
l
(0) ¼Incident spectral irradiance just below the culture
surface.
X¼microorganism density in grams of dry biomass per liter (g/l).
It has been observed that decreasing the depth of a pond from
20 cm to 10 cm achieve the targeted biomass density of 0.19 g dry
biomass per liter (g/l). The shallower ponds achieve greater
biomass densities with a decrease in monetary costs of dewatering
and harvesting the resultant biomass.
Bezerra et al. (2011) reported that the maximum cell concen-
tration (Xm) increased from 5200 to 5800 mg L
1
when the light
intensity was increased from 36 to 72
m
mol photons m
2
s
1
,
highlighting growth limitation by light intensity within this irra-
diance level. On the other hand, an additional increase in light in-
tensity up to 108
m
mol photons m
2
s
1
led only to a reduction in
the cultivation time from 8 to 6 days. Similar results were obtained
by Danesi, Rangel-Yagui, Carvalho, and Sato. (2004) using urea as a
R.A. Soni et al. / Trends in Food Science &Technology 69 (2017) 157e17 1164

nitrogen source in the light intensity range of 2e5 klux. This
behavior suggests that, at a relatively high light intensity (108
m
mol
photons m
2
s
1
), cell growth was accelerated by the faster
photosynthetic production of ATP and NADPH; but, when cell
concentration reached 5800 mg L
1
, the growth stopped likely due
to photo saturation or shadowing.
3.7. Growth rate &productivity
Salinity or nutrient concentration affects the growth rate of
algae. Specific growth rates of Spirulina were reported to be lower
in increased salinity concentrations. The highest growth was ach-
ieved at the lowest salinity ratio for studies performed with various
concentrations of NaHCO
3
and NaCl salts. The growth rate of Spir-
ulina undergoes simple cell division. Thus, under normal growth
conditions the specific growth rate is described by the following
equation:
m
¼t
x
dx
dt (4)
Calculation of specific growth rate has been described in many
ways. Most commonly used formula is
m
¼ln x
2
ln x
1
t
2
t
1
(5)
Where x
1
and x
2
are biomass concentration at time interval t
1
and
t
2
The simple equation that combines the specific growth are (
m
)
and the doubling time or the generation time (g) of the culture is:
g¼ln 2
m
¼¼ 0:633
m
¼d:t(6)
Cell productivity (P
X
) is a function of the independent variable,
which is described as the lowest difference in the cultivation time
(T
C
).
According to Grobbelaar (Mir
on et al., 1999), one of the most
important factors to obtain high biomass productivity is the
nutritional content of the culture medium. The use of certain nu-
trients can alter production costs and affect growth or biomass
composition (Grobbelaar, 2007; Sassano, Gioielli, Almeida, Sato,
Perego, &.ConvertiCarvalho, 2007). Annual biomass production
of Spirulina in PBRs is 3000 tonnes which are maximum when
compared to other microalgae species (Bharathiraja et al., 2015;
Jayati et al., 2015) Productivity is a measure of how much algal
biomass is produced per area per unit of time. Production up to
127,00 0 kg ha
1
yr
1
can be achieved in high-rate raceway ponds.
Productivity rates between 20 and 30 gm
2
day
1
(73e109,000 kg
ha
1
yr
1
) are in the range of usual open raceway performance
(Bharathiraja et al., 2015).
The productivity of the system
g
is defined as
g
¼
m
x (7)
Where
m
is the specific growth rate in units of reciprocal of time and
x is the biomass concentration.
The cell productivity (P
X
) is calculated as the ratio of the varia-
tion in cell concentration (X
m
-X
i
) to the cultivation time (T
C
)
P
X
¼(X
m
eX
i
)/T
C
(8)
As demonstrated in the earlier work (Mir
on et al., 1999), there is
an optimal biomass concentration which corresponds to the high-
est productivity.
Masojídek et al. (2003) applied a peristaltic pump as circulation
apparatus to cultivate Spirulina platensis and obtained a cell pro-
ductivity of 0.5 g/L/day, which was considered a relatively high
value in open pond cultivation system.
Toyoshima, Aikawa, Yamagishi, Kondo, &Kawai, 2015 reported
the maximum biomass productivities of Spirulina platensis in the
warm temperature habitat. 9 g dry biomass m
2
day
1
in summer
and in the subtropical habitat 10 g dry biomass m
2
day
1
in
autumn and. 6 g dry biomass m
2
day
1
in winter in the closed
bioreactor. The maximum specific growth rate of 0.141 was found at
32

C for Spirulina platensis and that of 0.144 was found at 37

C for
Spirulina fusiformis. Maximum biomass production of 2.4 g l
1
and
chlorophyll aproduction of 16.6 mg l
1
were observed at 32

C for
Spirulina platensis. Maximum biomass production of 2.3 g l
1
and
chlorophyll - a production of 14.2 mg l
1
were observed at 37

C for
Spirulina fusiformis (Allen, 2016; Rafiqul Islam, Hassan, Sulebele,
Orosco, &Roustaian, 2003). Spirulina, (Arthrospira platensis) is
normally cultivated in high salinity (>100 g/L) media or in high
bicarbonate (16 g/L alkalinity) waters to allow stable growth and
reduce the harmful bacteria and fungi invasions. The maximum
productivity of biomass Spirulina is in the range of 21e13.2 g m
2
/
d(Vonshak, 1997). Maximum biomass yield of Spirulina reported in
the large open pond is lower than other species. Spirulina biomass
yield of 35 tonnes/hectare/yr has been reported in a commercial
open mass cultivation pond at Siam Algae, Bangkok (Habib et al.,
2008, pp. 1e41).
4. Review of harvesting system
The best time for harvesting is early morning for following
reasons.
Percentage of proteins in the Spirulina is highest in the morning.
Cool temperature makes the work easier.
More sunshine hours will be available to dry the product.
Harvesting is carried out in two steps:
Filtration - to obtain a biomass containing about 10% dry matter
and 50% residual culture medium,
Removals of the residual culture medium to obtain the fresh
Spirulina biomass, containing about 20% dry matter.
Different harvesting techniques used are
filtration,
flotation,
centrifugation,
precipitation,
ion exchange,
Electrolytic and
Ultrasonic vibration.
Harvesting of microalgae Spirulina is done using a filter or mesh
cloth of at least 50 microns to efficiently collect Spirulina from its
medium.
4.1. Centrifugation
Centrifugation is a method to separate Spirulina algae from the
media. Centrifugation and chemical precipitation are economically
feasible, where centrifugation being in appreciably better A
centrifuge is an equipment, driven by a motor, that puts an object in
rotation around a fixed axis, applying a force perpendicular to the
axis. This method is reasonably efficient, but sensitive algal cells
may be damaged by pelleting against the rotor wall. Centrifugation
R.A. Soni et al. / Trends in Food Science &Technology 69 (2017) 157e17 1 165

and drying are currently considered too expensive for personal use,
though viable on a commercial and industrial scale. The centrifuge
works using the sedimentation principle, where the centripetal
acceleration is used to evenly distribute substances of greater and
lesser density.
4.2. Filtration
During commercial production processes filtration devices are
used for harvesting. These are of two types, i.e. inclined or vibrating
screens. Inclined Screens are 380e500 mesh with a filtration area
of 2e4m
2
per unit and are capable of harvesting nearly about
10e18 m
3
of Spirulina culture per hour (Ogbonna et al., 1999). Ef-
ficiencies of biomass harvesting are very high which nearly 95%.
Inclined, stationary screen is considered as a better solution for
harvesting Spirulina. Vibrating screens filter the same volume per
unit time as the inclined screens, but require one-third of the area.
Their harvesting efficiencies are often very high. The combination
of both inclined filter and a vibrating screen is used. In the process
of pumping the algal culture, the Spirulina filaments may be
damaged physically. Repeated harvesting leads to the increasing
enrichment of the culture with unicellular microalgae or short fil-
aments of Spirulina, which can pass through the screen easily. Ac-
cording to the work reported in large-scale production of Spirulina
the vibrating screen may not be the optimum device for harvesting.
Next step is the washing of excess salts from the biomass. The
washed cake is frequently homogenized before being dried.
4.3. Drying
Though Spirulina can be consumed fresh, it has to be used after
slight drying (Ankita, Michael Ceballos, &GantiS, 2013). Spirulina
should be consumed within 6 h of its harvest although it can be
preserved for later consumption for a period of up to one or more
year by sun drying or in greenhouses or in a solar drier.
Spirulina is relatively easily digestible in its fresh form
(Richmond &Vonshak, 1978). Health and nutritioncompanies have
tried to minimize the nutrients lost during drying and maximizing
the pure microalgae biomass recovered, while still keeping cost
effective (Sierra et al., 2008). Different drying methods include sun
drying, freeze drying, spray drying, drum drying and cooking. Since
Spirulina has a thin, fragile cell wall so, sun drying is sufficient to
sterilize the algae and make it consumable. Sun drying is the most
popular drying method, but requires a few precautions. Direct sun
drying must be very quick, otherwise the chlorophyll will be
destroyed and the dry product will appear blue. In industries spray
drier is used for Spirulina which flash dries fine droplets at very
high temperature and yields an extremely fine powder of low
apparent density. Although freeze drying considered as the best
way of drying but far too expensive and complicated. The biomass
to be dried must be thin enough to dry before it starts fermenting.
Fundamentally two types of shapes are used, thin layers of rather
fluid biomass laid on a plastic film, and rods as spaghetti laid on a
perforated tray. In the former case the air flows horizontally over
the film, while in the later case it flows vertically through the tray.
The rod shape is theoretically better as evaporation can take place
all around; rods are obtained by extrusion to a diameter of 1e2 mm.
But rods must be sturdy enough to maintain their shape, so this
type of drying is restricted to biomass that can be dewatered by
pressing. The total duration of the drying should not be less than
2 h. Drying temperature should be limited to 68

C and drying time
is limited to 7 h. For better preservation under storage, moisture
should not exceed 3e4%. During the drying process as well as af-
terward the product must be protected against contaminations
from dust and insects and should not be touched by hands.
Incipient fermentation during drying can be detected by smelling
during the drying process as well as afterward. For long time
storage of Spirulina, it is vacuum dried and packed air-tight where it
sustains its nutritional qualities for at least five years. The best
storage is in heat sealed, aluminized plastic bags.
As far as drying treatment is concerned, significant amounts of
energy are needed to evaporate water from the high moisture
containing biomass. The evaporation energy for 1 kg of water is
2.257 kJ, while depending on the drying equipment the efficiency of
the process varies. In the case of solar drying the efficiency is
considered to be around 50% since the material is exposed to open
air, while for vacuum drying the efficiency can rise up to 80%.
Taking into consideration the final moisture content that can be
achieved, specifically 4% and 2.5% for solar and vacuum drying,
respectively, the amount of cultivated and harvested biomass that it
is needed to acquire 1 kg of dried material differs (Papadaki,
Kyriakopoulou, Stramarkou, Tzovenis, &Krokida, 2017).
4.4. Grinding/powdering
The dry chips or rods are usually converted to powder by
grinding to increase their apparent density. Spirulina is used as a
whole food/dietary supplement which is available in tablet, flake
and powder form (Fig. 2). Spirulina can be directly ground to ultra
fine powder form. It is also used as a feed supplement in the
aquaculture, aquarium and poultry industries. Commercial Spir-
ulina is most often sold as a deep green-coloured powder or a
tablet. It is used as an ingredient in packaged health food snacks
and drinks. The strained Spirulina algae paste is laid out and triple-
washed with potable water for salt removal before it goes into a
drying vessel that converts it into powder form. The dried Spirulina
flakes are crushed using high impact ultrafine grinding mill.
Grinding is continued for about 6e10 h, till the average powder size
reaches 200e800 nm. The two most common forms of commer-
cially available Spirulina are powder and tablets. It is also an
ingredient in some protein and energy-boosting powder mixes.
4.5. Pellets/capsules
Spirulina powder is pressed together into a tablet or granule
shape (Ogbonda et al., 2007) for improved acceptance and perfor-
mance. It is formulated as a completely balanced diet which pro-
vides optimum growth and health (Slade, &Bauen, 2013). It
contains proteinated trace minerals for higher stability, biological
availability and overall human health.
Advantages of Spirulina pellets are as follows.
Excellent water stability
Easily consumable
Contains extra levels of preservative and antioxidants
Longer shelf life.
4.6. Spirulina products
Spirulina fights against aging, oxidative stress, diabetes, cardio-
vascular diseases, hypertension, arthritis, infertility and cancer.
Spirulina is considered as a superfood as it is the best food sup-
plement. Different healthcare industries make Spirulina products.
Major companies which are involved in cultivating spirulina glob-
ally are:
Earthrise Nutritionals (USA California) (earthrise.com)
DIC Lifetec Spirulina (Japan) (dlt-spl.co.jp/business/en/spirulina/)
Cyanotech Spirulina (USA Hawaii) (cyanotech.com)
Boonsom Spirulina Farm (Thailand) (boonsomfarm.com)
R.A. Soni et al. / Trends in Food Science &Technology 69 (2017) 157e17 1166

FEBICO (Far East Bio-Tec Co.) (Taiwan) (febico.com)
Spirulinea (France/Laos) (spirulinea.com)
Spiruline de Burkina (Burkina Faso) (spirulineburkina.org)
Green Valley (Germany) (greenvalley.de)
Natesis Spirulina (France) (natesis.com)
Spirulina.PL (Poland) (spirulina.pl)
All Seasons Health (United Kingdom) (allseasonshealth.com)
NaturKraftWerke Spirulina (Switzerland) (naturkraftwerke.com)
Sanatur Spirulina (Germany) (sanatur.de)
Marcus Rohrer Spirulina (Netherlands) (spirulina.nl)
Taiwan Chlorella (Taiwan) (taiwanchlorella.com)
RBC Life Sciences (USA) (rbclifesciences.com)
Gerophyta Nutraceuticals Company in Tamil Nadu, India offers a
wide range of products, as Spirulina Powder, Spirulina Capsules,
Spirulina tablets, Spiruvita-C, Dr. Spirulina Diavita-C, Spirulina
herbal face pack. Other companies also offers a wide range of
products as spirulina bar, spirulina green tea, Spirulina personal
care products, Spirulina chocolates, spirulina drinks, spirulina
honey etc.
5. Spirulina benefits
5.1. Nutritional composition of Spirulina
Spirulina is a microalga that has been consumed for decades due
to its high nutritional value and reported health benefits. Today
Spirulina is endorsed as a secret, potent superfood, also considered
as the miracle that grows naturally in oceans and salty lakes in
subtropical climates. Spirulina contains practically all the compo-
nents found in the ideal complete food. A considerable proportion
of proteins, vitamins, mineral salts, carbohydrates, pigments, trace
elements, and essential fatty acids are present. Unlike other algae,
Spirulina is easier to consume.
5.1.1. Protein
Spirulina is the richest source of proteins. Spirulina is abundant
in plant protein, which makes up 60%e70% of its weight
(Balasubramani et al., 2016). Soya flour, contains about 35% protein.
Qualitatively, Spirulina provides complete proteins as it contains
the full range of essential amino acids which is 47% of total protein
weight.
5.1.2. Vitamins
The vitamins naturally found in Spirulina are
b
-carotene, B
1
,B
2
,
B
12
, E. Its
b
-carotene content is unusually high which is about 30
times higher than found in a carrot. Spirulina is also exceptionally
rich in vitamin B
12
cobalamin. This vitamin is, most difficult to get
from a vegetarian diet because no fruit, vegetable, grain, or legume
contains it. Spirulina has four times as much vitamin B
12
than raw
liver, which was considered to be the best source of this nutrient.
Spirulina is also recognized as an excellent source of vitamin E
comparable to those found in wheat gram (Yin, Daoust, Young,
Tebbs, &Harper, 2017). The primary antioxidant vitamins con-
tained in Spirulina are
b
-carotene, carotenoids, and vitamin E.
5.1.3. Minerals
Spirulina contains mineral such as iron, magnesium, calcium,
and phosphorus. Spirulina is a splendid source of iron which con-
tains 20 times more iron than wheat gram. Iron is a mineral that is
mainly present in foods from animals, such as meat, and fish
(Balasubramani et al., 2016; Roberto, 2015). Spirulina is very ad-
vantageous for athletes, vegetarians, pregnant women, and teen-
agers. Average nutritional analysis of Spirulina per 100 gm is shown
in Table 5.
5.2. Pharmaceuticals and nutraceutical applications
Spirulina is the best complete nutritional food source of protein,
beta carotene, GLA, B Vitamins, minerals, chlorophyll, sulfolipids,
glycolipids, superoxide dismutase, phycocyanin, enzymes, RNA,
DNA, and supplies many nutrients that are lacking in most of the
people's diets. Nutraceutical food products supplement the diet as
well as facilitate the prevention or treatment of a disease or dis-
order. There are many Nutraceutical and Functional food products
which are commercially available with researched and approved
health benefits. The current estimated global market size for
nutraceuticals products is approximately 30e60 billion dollars,
which is primarily in the United States, Japan, and Europe. Spirulina
products have a potential short-term growth market demand of
over 197 billion dollars. As the demand for nutraceuticals and food
supplements is increasing, organisms that can rapidly produce
nutritional compounds are in demand. The ability of Spirulina as a
potent for anti-viral, antiecancer, hypocholesterolemic and health
improvement agent is getting attention as a nutraceutical and
pharmaceutical.
Spirulina has the following health benefits.
Helps athletes with long lasting energy and vitality
Nourishes people with digestion, assimilation &elimination
Prevents diabetes
Aids in reducing stress
Prevents depression
Concentrated impressive nutrients to weight loss
Improves memory and mental clarity
Fig. 2. Dried Spirulina (a) Spirulina flakes (b) Powdered form of Spirulina.
R.A. Soni et al. / Trends in Food Science &Technology 69 (2017) 157e17 1 167

Stimulates immune system to destroy invading disease organ-
isms and carcinogens
Enhance the immune system with its antiviral, anti-tumor and
interferon inducing effects
Promotes tissue repair in wounds and burns and also has the
anti-infectious properties
Decreases cholesterol levels and helps to lower the risk of car-
diovascular disease
Functions as an anti-inflammatory agent
Reduce the inflammation characteristic of arthritis
Govern the appetite and helps to stimulate the metabolism
Hailed by health professional as the superfood to conquer vi-
ruses, prevent aging and even ward off cancer, Spirulina may be
able to play another, much more significant role as a way to combat
malnutrition in developing countries. In light of Spirulina's nutri-
tional goodness, a number of individuals and organizations are
developing Spirulina programmes to address malnutrition. Aloni,
Lukusa, Matondo, Nkuadiolandu, &Takaisi, 2016 reported that
the administration of Spirulina at a dose of 10 g per day seemed to
significantly and quickly improve the nutritional status of under-
nourished children in the intervention group when compared to
the control group. Indeed, the rate of global acute malnutrition
decreased from 30% before the Spirulina supplements to 20% at day
30. According to The Hindu Survey Spirulina powder ranges from
1000 to 4500INR/Kg. Spirulina capsules range from 250 to 900INR/
60 capsules. Spirulina face packs vary from 360 to 900INR/100 gm.
6. Future outlook
Spirulina is a promising food source with protein content about
65e70%.However the maximum protein content reported in liter-
ature till date is 59%. Proper designing of cultivation system, growth
efficient techniques and use of organic fertilizer may be adopted to
maximize the protein content of Spirulina.
The food processing technique including drying of Spirulina
biomass is an important step to retain the nutrition and active
compound.
Further efforts should be made to increase protein content and
biomass yield.
Open raceway pond is economical but the annual production of
only 0.8 gms liter
1
day
1
has been reported.
Open pond cultivation system has many drawbacks such as
improper light intensity, contamination and requires large acres
of land.
Aeration is very necessary for getting good quality and better
yields of Spirulina species. Aeration should be done every 3e4h,
to avoid clump formation.
It has been reported on a dry weight basis for Spirulina, pro-
ductivity and total biomass production at the end of a produc-
tion cycle in PBR were 30 mg L
1
day
1
and 0.9 g.L
1
.
Highest productivity with Spirulina plantesis was reported in
raceway pond at Australia with a photosynthetic efficiency of
1.5% and areal productivity of 91 ton ha
1
yr
1
.
The daily production system according to the work reported is
greater with PBR and lesser with the open raceway ponds, So,
qualitatively as well as quantitatively when measured, PBR
systems are more efficient.
Hybrid reactors are fortunate outcomes of groundbreaking
strategies and technology advancements of Spirulina cultivation.
Productivity is expected to increase in the case of the hybrid
system. The hybrid system proves to be a better solution to
overcome the drawbacks of open pond and PBR. Poly bags can
be a good option if economically tested.
Climatic factors play an important role in Spirulina cultivation
where the optimum temperature is very important. So, in very
hot or cold or less humid conditions greenhouse can be used for
Spirulina cultivation. Different greenhouse designs have been
studied to design for Spirulina.
Various harvesting system has been reported among them
centrifugation may not be suggested for Spirulina as it is
expensive and it may also break Spirulina cells on separation.
Normal filter or mesh cloth of 30
m
- 450
m
is highly used and it
may separate Spirulina very easily and efficiently.
Greenhouse-based solar drying is preferred over open drying in
order to maintain the nutritional quality. Microwave or oven
drying method can also be used as an alternate method.
Dried powder may be transformed to easy and consumable form
than pellets, powder and capsules which are already available in
the market.
7. Summary
The main purpose of this review is to call attention for different
cultivation systems, growth parameters, and productivity of Spir-
ulina in various climatic conditions. The present review had
revealed that significant studies have been carried out on various
growth techniques to increase the protein productivity of Spirulina.
The following conclusions are drawn from the study.
Spirulina is mainly reported to be grown in open raceway ponds
for commercial or industrial purposes. New hybrid techniques
such as poly bags and greenhouse can also be implemented to
increase cost economics and the annual spirulina biomass
productivity.
Commercial Industrial scale cultivation of spirulina uses inor-
ganic chemicals which are expensive and requires optimization
Table 5
Average nutritional analysis of Spirulina per 100 g (Roberto, 2015).
Components Nutritional Value (in mgs) Components Nutritional Value (in mgs)
Plant Protein 63000 Calcium 1000
Carbohydrates 22000 Phosphorus 800
Fat 2200 Magnesium 400
Minerals 8000 Iron 58
Dietary Fibre 7000 Zinc 3
Vitamin A 212 Copper 1.2
Chlorophyll 600 Manganese 0.5
Vitamin E 10 Chromium 0.03
Vitamin B1 3.5 Potassium 1.4
Vitamin B2 0.4 Gamma-linoleic acid 1
Vitamin B3 1.3 Vitamin B8 0.005
Vitamin B5 0.2 Vitamin B9 0.05
Vitamin B6 6 Vitamin B12 0.35
R.A. Soni et al. / Trends in Food Science &Technology 69 (2017) 157e17 1168

of media concentration to avoid intrusion of prevention of
facultative pathogens.
Climatic factors, light intensity and aeration are very important
in Spirulina growth system. The culture conditions also influence
the growth phases of Spirulina platensis, causing changes in its
composition. Growth rate and doubling time can be increased
by bringing variations in used growth media.
There has been a significant change in functional properties of
Spirulina under stressed conditions. Environmental stresses like
high pH, light, salinity and temperature affect growth and
nutrient productivity.
Spirulina is contended to have several health benefits as it
contains essential proteins, carbohydrates, essential fatty acids,
vitamins, minerals, carotenes, chlorophyll aand phycocyanin to
fight against malnutrition. So it can be used in nutraceuticals
and pharmaceuticals applications.
Innovative formulations are required to fortify conventional
foods with Spirulina and more scientific, clinical and toxicolog-
ical research has to be carried out for extensive usage of Spir-
ulina in food and pharma industry.
Development of various Spirulina fortified foods is required to
create nutritional awareness and increase the acceptance level
in developing countries.
Despite their evident use as a nutritional product, Industrial
production of Spirulina are still more or less confined to the
limited natural areas. Mass cultivation of spirulina has to be
encouraged globally to avoid food shortages in near future.
Acknowledgement
We are very thankful to the Honourable Ex-Director, Dr.
K.K.Appukuttan, Maulana Azad National Institute of Technology
Bhopal, India for his continued support and guidance to complete
this research work. This research did not receive any specific grant
from funding agencies in the public, commercial, or not-for-profit
sectors.
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