Trends in Food Science & Technology 69 (2017) 157e171

Contents lists available at ScienceDirect

Trends in Food Science & Technology

jo ur na l h o me p a ge : h t tp :/ / w w w. j o ur n a l s .e ls ev ie r .c om / t r e n d s - i n -f o o d - s c i en ce -
a n d - tec h no l og y

Review

Spirulina e From growth to nutritional product: A review

a, c, *
Ruma Arora Soni a, K. Sudhakar , 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

A R T I C L E I N F O
A B S T R A C T
Article history:
Received 12 April 2017 Background: Spirulina is multicellular and filamentous cyanobacteria that have achieved a considerable
Received in revised form popularity in the health sector, food industry and aquacultures. It develops and grows in water, can be
18 June 2017 harvested and processed easily. It has very high content of macro and micronutrients, essential amino
Accepted 25 September 2017 acids, proteins, lipids, vitamins, minerals and anti-oxidants. Spirulina is considered as a complete food
Available online 28 September 2017 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 scienti fic findings. In
Keywords: recent years, Spirulina has gathered enormous attention from research fraternity as well as industries
Spirulina as a flourishing source of nutraceutical and pharmaceuticals.
Pharmaceutical Scope and approach: The primary objective of this paper is to review the utilization of Spirulina as a
Nutritional use
dietary supplement in the food industry. In the present work, the three main area of Spirulina research:
Dietary supplement
growth, harvesting and potential application are presented.
Open pond
PBR 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
microalgal biotechnology are biofuels, agricultural biostimulants
for crop plants, waste water treatment etc. Microalgal bio-
Algae are photosynthetic organisms that convert light energy
technologies refer to the production of different products as
from the sun into the chemical energy by the process of photo-
phycocyanin, carotenoids, fatty acids and lipids for application in
synthesis. Algae possess simple reproductive structure. The
health food, cosmetics, food supplements, pharmaceuticals and
biomass of algae contains various compounds with diversified
fuel production. Microalgal groups of major importance are chlor-
structures and functions. Algal biotechnology is divided into
ophyte, bacillariophytes, while macroalgae are harvested from
microalgae, macroalgae and cyanobacteria with its unique speci-
natural habitats. Algae that is currently cultivated for its maximum
ficity (Becker, 2007). Sometimes cyanobacteria are also included
protein content is the cyanobacterium species Athrospira, which is
in microalgae. Microalgae classification includes prokaryotic and
commonly known as Spirulina.
eukaryotic unicellular and multicellular. Microscopic are micro-
Spirulina was first discovered by Spanish Scientist Hernando
algae, Cyanobacteria, are prokaryotic. The Spirulina is Earth's
Cortez and Conquistadors in 1519. Cortez observed that Spirulina
oldest living plant approximately 3.6 billion years ago and a first
was eaten at the tables of the Aztecs during his visit in Lake
photo- synthetic life form that has created our oxygen atmosphere
Texcoco in the Valley of Mexico. Pierre Dangeard discovered the
so all life could evolve. Blue-green algae are the evolutionary
health benefits of Spirulina who observed that flamingos were
bridge be- tween green plants and bacteria. At present the main
surviving by consuming blue-green algae. Botanist Jean Leonard
directions in
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
* Corresponding author. Energy Centre, Maulana Azad National Institute of Texcoco, was set up in 1969 by the French.
Technology, Bhopal, M.P, India.
Spirulina is the most nutritious, concentrated food that is known
E-mail addresses: rumaarora14@gmail.com (R.A. Soni), sudhakar.i@manit.ac.in
(K. Sudhakar).

https://doi.org/10.1016/j.tifs.2017.09.010
0924-2244/© 2017 Elsevier Ltd. All rights reserved.
 158 R.A. Soni et al. / Trends in Food Science & Technology 69 (2017) 157e171

issues based on prior publications and the author's prior work in

the large scale cultivation of spirulina for nutritional products. The
Nomenclature
article starts with the illustration of spirulina growth chain from
identifying suitable strain to the final product.
tivity Cultivation
(PX)
time Productivity of the system Specific growth rate Biomass concentration
(TC) The present study focuses on growth rate, productivity, growth
G parameters, different cultivation systems (outdoor and indoor
m systems), harvesting and drying techniques of Spirulina. This re-
x view focuses on following aspects:
(Xm- Xi) Cell concentration
N0Initial population size ● Strain selection and cultivation of Spirulina.
tAmount of time that has past ● Optimum parameters for growth of Spirulina.
NtPopulation size at time ● Harvesting and drying techniques of Spirulina.
GGeneration time ● Commercial applications of Spirulina as pharmaceutical and
N.SNot Specified nutraceuticals product.

2. Review of growth system

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
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,
&
Can~ izares-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
 R.A. Soni et al. / Trends in Food Science & Technology 69 (2017) 157e171 159

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 þ PBR)

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
CO2-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

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 e Phase 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, Acie´nFern´andez, Sa´nchezPe´rez, 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 (Miro´n, 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
160 R.A. Soni et al. / Trends in Food Science & Technology 69 (2017) 157e171

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.

lamps (Ramos de Ortega and Roux 1986). After this, an outdoor

with flat-plate photobioreactors (Hoekema et al., 2002; Olguín
flat panel reactor was developed using thick transparent PVC
et al., 2003). Overview of spirulina productivities reported in the
materials (Tredici & Materassi, 1992). Later extensive works were
literature for various growth systems is presented in Table 2.
reported on various designs of flat plate reactors and vertical
Among all culture systems productivity of Spirulina platensis is
panels for mass cultivation of different algae (Hu et al., 1996;
highest in raceway ponds. The areal productivity is generally
Zhang, Kurano, & Miyachi, 2002; Hoekema, Bijmans, Janssen,
based on one-hectare ground surface area.
Tramper, & Wijffels,
2002; Olguín, Galicia, Mercado, Pe´rez, 2003). Flat plate
photo- 2.2.3. Tubular PBR
bioreactors are constructed using transparent materials for A tubular photobioreactor is the most suitable types of bio-
maximum utilization of solar light. Accumulation of dissolved ox- reactors for outdoor mass cultivation (Kaewpington et al., 2007).
ygen concentrations in horizontal tubular photobioreactors is Mostly outdoor tubular photobioreactors are constructed either
relatively high as compared to flat-plate photobioreactors. It has with glass or plastic tube. They can be horizontal/serpentine
been reported that high photosynthetic efficiencies can be
achieved
 R.A. Soni et al. / Trends in Food Science & Technology 69 (2017) 157e171
Table 2
Spirulina productivity and Photosynthetic efficiency.
Reactor system Location Light path Photosynthetic Efficiency
Raceway pond La Mancha, Mexico 0.1e0.25 1.5%
Raceway pond Florence, Italy 0.035 1.5%
Raceway pond Malaga, Spain 0.30 1.5%
Raceway pond Australia 0.30 1.5%
Horizontal Tubular Florence, Italy 0.06 1.8e3%
Flat Panel US 0.10 3.8%
(Chaumont, Thepenier, & Gudin, 1988; Molina, Fern´andez, Acie
´n, & 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 CO2 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
161
Productivity (ton ha—1yr—1) Reference
43.1 (Olguín et al., 2003)
20.0 (Tredici & Materassi, 1992)
23.6e30.0 (Jime´nez, Cossío, & Niell, 2003)
91.0 (Borowitzka, 1999)
30.0 (Tredici & Materassi, 1992)
22.1 (Richmond & Zhang, 2001)
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 CO2 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 3 16
Prospects and limitations of various cultivation systems (Chojnacka & Noworyta, 2004; Vymazal, 1990; Ugwu et al., 2008; Vree, Bosma, Janssen, Barbosa, & Wijffels, 2015; Newsted, 2004). 2

Culture systems Dimensions Specific growth rate Prospects Limitations Images

Open systems Variable 0.30day—1 Relatively economical, easy

Little control of culture conditions, difficulty in growing
to clean up after cultivation,
algal cultures for long periods,
good for mass cultivation of algae
poor productivity,
occupy large land mass,
limited to few strains of algae,
cultures are easily contaminated

Vertical Column
PBR 0.2 m diameter and 0.015 ± 0.002 h—1 High mass transfer, Small illumination surface area,
4 m column height good mixing with low shear stress, construction require sophisticated materials,
low energy consumption, shear stress to algal cultures,
high potentials for scalability, the decrease of illumination surface area upon scale-up
easy to sterilize,
good for immobilization of
R.
algae, reduced photoinhibition
A.
and photo-oxidation So
Flat plate PBR 0.07 m wide, Large illumination surface area, Scale-up require many compartments and support ni
1.5 m height, 2.5 m length et
suitable for outdoor cultures, materials, difficulty in controlling culture temperature,
al.
Volume 250lts good for immobilization of algae, some degree of wall growth, /
Productivity - 1.0 g/L day good light path, good biomass the possibility of hydrodynamic stress to some algal strains Tr
productivities, relatively cheap, en
easy to clean up, ds
in
readily tempered,
Fo
low oxygen buildup od
Sci
Tubular PBR D ¼ 3e10 cm 0.055 h—1 Large illumination surface area,
Gradients of pH, en
suitable for outdoor cultures, ce
dissolved oxygen and CO2 along the tubes, fouling,
fairly good biomass productivities, &
some degree of wall growth,
relatively cheap Te
requires large land space ch
no
lo
gy
69
Internally (2
Illuminated PBR Not Specified Large illumination surface area, Outdoor mass cultivation of algae require some 01
can utilize both solar and artificial light system, technical efforts. 7)
contamination can be minimized in this system 15
7e
17
1

Hybrid System Not Specified Minimize microbial contamination,

maximize biomass and product Requires large areas of land and some technical efforts
yield, Maximize CO2 supply

Poly Bags D < 30 cm 0.20day—1 site flexibility,

Low-cost materials, Polyethylene bag cultures have a relatively short life
easy scalability, because the internal surface attracts culture debris and
optimal light exposure, bacteria, which collectively reduce light penetration and
isolation of the crop from predators, are a source of contamination
very high biomass concentration,
low energy consumption
effective weather protection
 R.A. Soni et al. / Trends in Food Science & Technology 69 (2017) 157e171 163

3. Review of growth parameters advantageous. Phosphate, magnesium and calcium cannot be

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 C Spirulina 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
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, 1966). 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 Rao's Media CFTRI Media OFERR Media George's Media Conventional growth Reduced Cost
(gms/l) (gms/l) (gms/l) (gms/l) (gms/l) Media (gms/l) Media (gms/l)

NaHCO3 16.80 15 4.5 8.0 e 16 16.8

K2HPO4 0.50 0.50 0.5 - 0.02 e 0.235
NaNO3 2.50 2.50 1.5 - e e e
K2SO4 1.00 0.60 1.0 0.5 e 0.5 0.353
NaCl 1.00 0.20 1.0 5.0 e 1.00 0.471
MgSO4$7H2O 0.20 0.04 1.2 0.16 0.02 0.1 e
EDTA 0.08 - - - e e 0.353
CaCl2$2H2O 0.04 0.008 0.04 - e 0.1 0.176
FeSO4$2H2O 0.01 - 0.01 0.05 e e 0.265
H3BO3 2.86 - - 0.052 ml e e 2.86
MnCl2$4H2O 1.180 - - - e e 1.81
ZnSO4$7H2O 0.222 - - - e e 0.222
Na2MoO3$ 0.015 - - - e e 0.0177
CuSO4$5H2O 0.074 - - - e e 0.079
NH4VO3 22.9 - - - e e e
NiSO4$7H2O 47.8 - - - e e e
NaWO2 17.9 - - - e e e
Ti2(SO4)3$6H2O 4.4 - - - e e e
Co(NO3)2$6H2O 4.4 - - - e e e
Ferric citrate e - - - 0.035 e e
Peptone e - - - 1.00 e e
KNO3 e - - - e 2.00 e
(NH4)2HPO4 e - - - e 0.1 e
Chelated Iron e - - - e 2 squeezes (¼ teaspoon) e
Lime e - - - e 0.1 e
NH4NO3 e - - - e e 0.118
CO (NH2)2 e - - 0.2 e e 0.088
Fe EDTA e 0.20 - - e e e
A5 solution e 1 ml - - e e e
164 R.A. Soni et al. / Trends in Food Science & Technology 69 (2017) 157e171
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 mmol m—2 s—1, CO2 enriched air flow (0.5%), superficial aeration
rate of 0.0056 m s—1 in a NaHCO3-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
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, al, is
calculated according to
—a z
Gl(z)/Gl(0) ¼ e l (1)
The Spectral Irradiances at different depths z is calculated ac-
cording to above equation knowing the value of al, The spectral
attenuation cross section, Al, is defined as,
Al ¼ al/X (2)
Using the irradiance attenuation coefficients for each culture,
with al,
Gl(z) ¼ Gl(0)e —alz (3)
Where Gl(z) ¼ spectral irradiance at depth z.
Gl(0) ¼ Incident spectral irradiance just below the culture
surface.
X ¼ microorganism 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 mmol 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 mmol 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) 157e171
nitrogen source in the light intensity range of 2e5 klux. This
behavior suggests that, at a relatively high light intensity (108
mmol 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 NaHCO3 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:
t dx
m¼
x dt
Calculation of specific growth rate has been described in many
ways. Most commonly used formula is
ln x — ln x
m¼ 2 1
t2 — t1
Where x1 and x2 are biomass concentration at time interval t1 and
t2 The simple equation that combines the specific growth are (m)
and the doubling time or the generation time (g) of the culture is:
ln 2 0:633
g¼ ¼¼ ¼ d:t
m ● Percentage of proteins in the Spirulina is highest in the morning.
Cell productivity (PX) is a function of the independent variable,
which is described as the lowest difference in the cultivation time
(TC).
According to Grobbelaar (Miro´n 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
127,000 kg ha—1 yr—1 can be achieved in high-rate raceway ponds.
Productivity rates between 20 and 30 gm —2day—1 (73e109,000 kg
ha—1yr—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 mx
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 (Xm- Xi) to the cultivation time (TC)
PX ¼ (Xm e Xi) / TC
As demonstrated in the earlier work (Miro´n 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
165
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 a production 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
(4) 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 m2/
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.,
(5) 2008, pp. 1e41).
4. Review of harvesting system
The best time for harvesting is early morning for following
reasons.
(6)
● 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
(7) 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
(8) 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
166 R.A. Soni et al. / Trends in Food Science & Technology 69 (2017) 157e171

and drying are currently considered too expensive for personal

Incipient fermentation during drying can be detected by smelling
use, though viable on a commercial and industrial scale. The
during the drying process as well as afterward. For long time
centrifuge works using the sedimentation principle, where the
storage of Spirulina, it is vacuum dried and packed air-tight where
centripetal acceleration is used to evenly distribute substances of
it sustains its nutritional qualities for at least five years. The best
greater and lesser density.
storage is in heat sealed, aluminized plastic bags.
As far as drying treatment is concerned, significant amounts of
4.2. Filtration
energy are needed to evaporate water from the high moisture
containing biomass. The evaporation energy for 1 kg of water is
During commercial production processes filtration devices are
2.257 kJ, while depending on the drying equipment the efficiency
used for harvesting. These are of two types, i.e. inclined or
of the process varies. In the case of solar drying the efficiency is
vibrating screens. Inclined Screens are 380e500 mesh with a
considered to be around 50% since the material is exposed to
filtration area of 2e4 m2 per unit and are capable of harvesting
open air, while for vacuum drying the efficiency can rise up to
nearly about 10e18 m3 of Spirulina culture per hour (Ogbonna et
80%. Taking into consideration the final moisture content that can
al., 1999). Ef- ficiencies of biomass harvesting are very high which
be achieved, specifically 4% and 2.5% for solar and vacuum
nearly 95%. Inclined, stationary screen is considered as a better
drying, respectively, the amount of cultivated and harvested
solution for harvesting Spirulina. Vibrating screens filter the same
biomass that it is needed to acquire 1 kg of dried material differs
volume per unit time as the inclined screens, but require one-third
(Papadaki, Kyriakopoulou, Stramarkou, Tzovenis, & Krokida,
of the area. Their harvesting efficiencies are often very high. The
2017).
combination of both inclined filter and a vibrating screen is used.
In the process of pumping the algal culture, the Spirulina filaments
4.4. Grinding/powdering
may be damaged physically. Repeated harvesting leads to the
increasing enrichment of the culture with unicellular microalgae
The dry chips or rods are usually converted to powder by
or short fil- aments of Spirulina, which can pass through the screen
grinding to increase their apparent density. Spirulina is used as a
easily. Ac- cording to the work reported in large-scale production
whole food/dietary supplement which is available in tablet, flake
of Spirulina the vibrating screen may not be the optimum device
and powder form (Fig. 2). Spirulina can be directly ground to ultra
for harvesting. Next step is the washing of excess salts from the
fine powder form. It is also used as a feed supplement in the
biomass. The washed cake is frequently homogenized before
aquaculture, aquarium and poultry industries. Commercial Spir-
being dried.
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
4.3. Drying
and drinks. The strained Spirulina algae paste is laid out and triple-
washed with potable water for salt removal before it goes into a
Though Spirulina can be consumed fresh, it has to be used after
drying vessel that converts it into powder form. The dried
slight drying (Ankita, Michael Ceballos, & GantiS, 2013). Spirulina
Spirulina flakes are crushed using high impact ultrafine grinding
should be consumed within 6 h of its harvest although it can be
mill. Grinding is continued for about 6e10 h, till the average
preserved for later consumption for a period of up to one or more
powder size reaches 200e800 nm. The two most common forms of
year by sun drying or in greenhouses or in a solar drier.
commer- cially available Spirulina are powder and tablets. It is also
Spirulina is relatively easily digestible in its fresh form
an ingredient in some protein and energy-boosting powder
(Richmond & Vonshak, 1978). Health and nutrition companies have
mixes.
tried to minimize the nutrients lost during drying and maximizing
the pure microalgae biomass recovered, while still keeping cost
4.5. Pellets/capsules
effective (Sierra et al., 2008). Different drying methods include sun
drying, freeze drying, spray drying, drum drying and cooking.
Spirulina powder is pressed together into a tablet or granule
Since Spirulina has a thin, fragile cell wall so, sun drying is
shape (Ogbonda et al., 2007) for improved acceptance and perfor-
sufficient to sterilize the algae and make it consumable. Sun drying
mance. It is formulated as a completely balanced diet which pro-
is the most popular drying method, but requires a few precautions.
vides optimum growth and health (Slade, & Bauen, 2013). It
Direct sun drying must be very quick, otherwise the chlorophyll
will be destroyed and the dry product will appear blue. In contains proteinated trace minerals for higher stability, biological
industries spray drier is used for Spirulina which flash dries fine availability and overall human health.
Advantages of Spirulina pellets are as follows.
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 ● Excellent water stability
complicated. The biomass to be dried must be thin enough to dry ● Easily consumable
before it starts fermenting. Fundamentally two types of shapes are ● Contains extra levels of preservative and antioxidants
used, thin layers of rather fluid biomass laid on a plastic film, and ● Longer shelf life.
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 4.6. Spirulina products
vertically through the tray. The rod shape is theoretically better as
evaporation can take place all around; rods are obtained by Spirulina fights against aging, oxidative stress, diabetes, cardio-
extrusion to a diameter of 1e2 mm. But rods must be sturdy vascular diseases, hypertension, arthritis, infertility and cancer.
enough to maintain their shape, so this type of drying is restricted Spirulina is considered as a superfood as it is the best food sup-
to biomass that can be dewatered by pressing. The total duration plement. Different healthcare industries make Spirulina products.
of the drying should not be less than Major companies which are involved in cultivating spirulina glob-
◦ ally are:
2 h. Drying temperature should be limited to 68 C and drying time
is limited to 7 h. For better preservation under storage, moisture
Earthrise Nutritionals (USA California) (earthrise.com)
should not exceed 3e4%. During the drying process as well as af-
terward the product must be protected against contaminations DIC Lifetec Spirulina (Japan) (dlt-
from dust and insects and should not be touched by hands. 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) 157e171
Fig. 2. Dried Spirulina (a) Spirulina flakes (b) Powdered form of Spirulina.
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, B1, B2,
B12, 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 B12 cobalamin. This vitamin is, most difficult to get
167
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
168 R.A. Soni et al. / Trends in Food Science & Technology 69 (2017) 157e171

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

Stimulates immune system to destroy invading disease organ-

● isms and carcinogens ● It has been reported on a dry weight basis for Spirulina, pro-
ductivity and total biomass production at the end of a produc-
● Enhance the immune system with its antiviral, anti-tumor and tion cycle in PBR were 30 mg L—1 day —1 and 0.9 g.L—1.
interferon inducing effects
● Highest productivity with Spirulina plantesis was reported in
● Promotes tissue repair in wounds and burns and also has the
raceway pond at Australia with a photosynthetic efficiency of
anti-infectious properties
1.5% and areal productivity of 91 ton ha—1yr—1.
● Decreases cholesterol levels and helps to lower the risk of car-
diovascular disease ● The daily production system according to the work reported is
greater with PBR and lesser with the open raceway ponds, So,
● Functions as an anti-inflammatory agent
qualitatively as well as quantitatively when measured, PBR
● Reduce the inflammation characteristic of arthritis
systems are more efficient.
● Govern the appetite and helps to stimulate the metabolism
● Hybrid reactors are fortunate outcomes of groundbreaking
strategies and technology advancements of Spirulina cultivation.
Hailed by health professional as the superfood to conquer vi-
Productivity is expected to increase in the case of the hybrid
ruses, prevent aging and even ward off cancer, Spirulina may be
system. The hybrid system proves to be a better solution to
able to play another, much more significant role as a way to
overcome the drawbacks of open pond and PBR. Poly bags can
combat malnutrition in developing countries. In light of Spirulina's
be a good option if economically tested.
nutri- tional goodness, a number of individuals and organizations
are developing Spirulina programmes to address malnutrition. ● Climatic factors play an important role in Spirulina cultivation
where the optimum temperature is very important. So, in very
Aloni, Lukusa, Matondo, Nkuadiolandu, & Takaisi, 2016 reported
hot or cold or less humid conditions greenhouse can be used for
that the administration of Spirulina at a dose of 10 g per day
Spirulina cultivation. Different greenhouse designs have been
seemed to significantly and quickly improve the nutritional status
studied to design for Spirulina.
of under- nourished children in the intervention group when
compared to the control group. Indeed, the rate of global acute ● Various harvesting system has been reported among them
centrifugation may not be suggested for Spirulina as it is
malnutrition decreased from 30% before the Spirulina supplements
expensive and it may also break Spirulina cells on separation.
to 20% at day
30. According to The Hindu Survey Spirulina powder ranges from ● Normal filter or mesh cloth of 30m - 450m is highly used and it
may separate Spirulina very easily and efficiently.
1000 to 4500INR/Kg. Spirulina capsules range from 250 to 900INR/
60 capsules. Spirulina face packs vary from 360 to 900INR/100 ● Greenhouse-based solar drying is preferred over open drying in
order to maintain the nutritional quality. Microwave or oven
gm.
drying method can also be used as an alternate method.
● Dried powder may be transformed to easy and consumable
6. Future outlook form than pellets, powder and capsules which are already
available in the market.
Spirulina is a promising food source with protein content about
65e70%.However the maximum protein content reported in liter-
7. Summary
ature till date is 59%. Proper designing of cultivation system, growth
efficient techniques and use of organic fertilizer may be adopted to
The main purpose of this review is to call attention for different
maximize the protein content of Spirulina.
cultivation systems, growth parameters, and productivity of Spir-
ulina in various climatic conditions. The present review had
● The food processing technique including drying of Spirulina
revealed that significant studies have been carried out on various
biomass is an important step to retain the nutrition and active
growth techniques to increase the protein productivity of
compound.
Spirulina.
● Further efforts should be made to increase protein content and The following conclusions are drawn from the study.
biomass yield.
● Open raceway pond is economical but the annual production of
only 0.8 gms liter —1 day—1 has been reported. ● Spirulina is mainly reported to be grown in open raceway
ponds for commercial or industrial purposes. New hybrid
● Open pond cultivation system has many drawbacks such as
techniques such as poly bags and greenhouse can also be
improper light intensity, contamination and requires large
implemented to increase cost economics and the annual
acres of land.
spirulina biomass productivity.
● Aeration is very necessary for getting good quality and better
yields of Spirulina species. Aeration should be done every 3e4 ● Commercial Industrial scale cultivation of spirulina uses inor-
ganic chemicals which are expensive and requires optimization
h, to avoid clump formation.
 R.A. Soni et al. / Trends in Food Science & Technology 69 (2017) 157e171
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 a and 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 speci fic grant
from funding agencies in the public, commercial, or not-for-profit
sectors.
References
Allen, K. (2016). Evaluating Spirulina as a protein source in Nile Tilapia (Oreochromis
niloticus) grow-out diets (Doctoral dissertation).
Aloni, M. N., Lukusa, A. K., Matondo, F. K., Nkuadiolandu, A. B., & Takaisi, K. (2016).
Spirulina supplements improved the nutritional status of undernourished
children quickly and Significantly: Experience from Kisantu, the democratic
Republic of the Congo. International Journal of Pediatrics, 2016. https://doi.org/
10.1155/2016/1296414. Article ID 1296414, 5 pages.
Ankita, Juneja, Michael Ceballos, Ruben, & GantiS, Murthy (2013). Effects of envi-
ronmental factors and nutrient availability on the biochemical composition of
algae for biofuels production: A review. Energies, 19961073(6), 9.
Anupama, P. R. (2000). Value-added food: Single cell protein. Biotechnology Ad-
vances, 18, 459e479.
Atlas, R. M., & Parks, L. C. (1997). Handbook of microbiological media (2nd ed.). Boca
Raton, Fla, USA: CRC. Press.
Balasubramani, R., Gupta, S. K., Cho, W., Kim, J., Lee, S., Jeong, K., … Choi, H.
(2016).
Microalgae potential and multiple roles-current progress and future prospects-
an overview. Sustainability, 8(12).
Becker, E. W. (2007). Micro-algae as a source of protein. Biotechnology Advances,
2(2), 207e210.
Bezerra, R. P., Montoya, E. Y. O., Sato, S., Perego, P., de Carvalho, J. C. M., & Converti, A.
(2011). Effects of light intensity and dilution rate on the semicontinuous
cultivation of Arthrospira (Spirulina) platensis. A kinetic Monod-type approach.
Bioresource Technology, 102(3), 3215e3219.
Bharathiraja, B., Chakravarthy, M., Ranjith Kumar, R., Yogendran, D., Yuvaraj, D.,
Jayamuthunagai, J., et al. (2015). Aquatic biomass(algae) as a future feedstock
for bio-refineries:Areviewoncultivation, processingandproducts. Renewable and
Sustainable Energy Reviews, 47, 634e653.
Borowitzka, M. A. (1999). Commercial production of microalgae: Ponds, tanks,
tubes and fermenters. Journal of Biotechnology, 70(1), 313e321.
Camacho Rubio, F., Acie´nFern´andez, F. G., S´anchezPe´rez, J. A., García
Camacho, F., &
Molina Grima, E. (1999). Prediction of dissolved oxygen and carbon dioxide
concentration profiles in tubular photobioreactors for microalgal culture.
Biotechnology and Bioengineering, 62, 71e86.
Chaumont, D., Thepenier, C., & Gudin, C. (1988). Scaling up a tubular
169
photobioreactor for continuous culture of Porphyridiumcruentum e from lab-
oratory to pilot plant. In T. Stadler, J. Morillon, M. S. Verdus, W. Karamanos,
H. Morvan, & D. Christiaen (Eds.), Algal biotechnology (pp. 199e208). London:
Elsevier Applied Science.
Chetsumon, A., Umeda, F., Maeda, I., Yagi, K., Mizoguchi, T., & Miura, Y. (1998). Broad
spectrum and mode of action of an antibiotic produced by Scytonema sp. TISTR
8208 in a seaweed-type bioreactor. Applied Biochemistry and Biotechnology,
70e72, 249e256.
ChiniZittelli, G., Rodolfi, L., & Tredici, M. R. (2003). Mass cultivation of Nanno-
chloropsis sp. in annular reactors. Journal of Applied Phycology, 15, 107e114.
Chisti, Y. (2016). "Large-scale production of algal biomass: Raceway ponds." algae
biotechnology. Springer International Publishing.
Chojnacka, K., & Noworyta, A. (2004). Evaluation of Spirulina sp. growth in
photoautotrophic, heterotrophic and mixotrophic cultures. Enzyme and Micro-
bial Technology, 34(5), 461e465.
Cuaresma, M., Janseen, M., Vilchez, & Wijffels, R. H. (2011). Horizontal or Vertical
photobioreactrs?How to improve microalgae photosynthetic efficiency. Bio-
resource Technology, 102, 5129e5137.
Danesi, E. D. G., Rangel-Yagui, C. O., Carvalho, J. C. M., & Sato, S. (2004). Effect of
reducing the light intensity on the growth and production of chlorophyll by
Spirulina platensis. Biomass and Bioenergy, 26(4), 329e335.
Degen, J., Uebele, A., Retze, A., Schmidt-Staigar, U., & Trosch, W. A. (2001). A novel
airlift photobioreactor with baffles fro improved light utilization through
flashing light effect. Journal of Biotechnology, 92, 89e94.
Dubey, R. C. (2006). A textbook of Biotechnology. Fourth revised and enlarged edition
(pp. 419e421). S. hand and Company Limited.
Famelart, M., Kobilinsky, A., Bouillamnne, C., & Desmazeaud, M. J. (1987). Influence
of temperature, pH and dissolved oxygen on growth of Brevibacterium linen in
a fermentor. Applied Microbiology Biotechnology, 25, 442e448.
Gallardo-Rodríguez, J., Sa´nchez-Miro´n, A., García-Camacho, F., Lo´pez-Rosales,
L.,
Chisti, Y., & Molina-Grima, E. (2012). Bioactives from microalgal dinoflagellates.
Biotechnology Advances, 30(6), 1673e1684. https://doi.org/10.1016/j.biotechadv.
2012.07.005.
Grobbelaar, J. U. (2007). Photosynthetic characteristics of Spirulinaplatensis grown
in commercial-scale open outdoor raceway ponds: What do the organisms tell
us? Journal of Applied Phycology, 19, 591e598.
Habib, M. A. B., Parvin, M., Huntington, T. C., & Hasan, R. M. (2008). A review on
culture, production and use of Spirulina as food for humans and feeds for domestic
animals and fish. No. 1034, Rome-Italy: FAO Fisheries and Aquaculture Circular,
ISBN 978-92-5-1061060.
Hall, D. O., Fernandez, F. G. A., Guerrero, E. C., Rao, K. K., & Grima, E. M. (2003).
Outdoor helical tubular photobioreactors for microalgalproduction:modeling of
fluid-dynamics and mass transfer and assessmentof biomass productivity.
Biotechnology and Bioengineering, 82, 62e73.
Harker, M., Tsavalos, A. J., & Young, A. J. (1996). Autotrophic growth and carotenoid
production of Haematococcuspluvialis in a 30 liter airlift photobioreactor.
Journal of Fermation and Bioengineering, 82, 113e118.
Hase, Ryouetsu, Oikawa, Hiroyoshi, Sasao, Chiyo, Morita, Masahiko, &
Watanabe, Yoshitomo (2000). Photosynthetic production of microalgal biomass
in a raceway system under greenhouse conditions in Sendai city. Journal of
Bioscience and Bioengineering, 89(2), 157e163.
Hoekema, S., Bijmans, M., Janssen, M., Tramper, J., & Wijffels, R. H. (2002).
A pneumatically agitated flat-panel photobioreactor with gas recirculation:
anaerobic photoheterotrophic cultivation of a purple nonsulfur bacterium.
Intenational Journal of Hydrogen Energy, 27, 1331e1338.
Hu, Q., Guterman, H., & Richmond, A. (1996). A flat inclined modular photo-
bioreactor for outdoor mass cultivation of phototrophs. Biotechnology and
Bioengineering, 51, 51e60.
Jayati, Trivedi, Aila, Mounika, Bangwal, D. P., Kaul, Savita, & Garg, M. O. (2015). Algae
based biorefinery-How to make sense? Renewable and Sustainable Energy Re-
views, 47, 295e307.
Jime´nez, C., Cossío, B. R., & Niell, F. X. (2003). Relationship between physicochemical
variables and productivity in open ponds for the production of spirulina: A
predictive model of algal yield. Aquaculture, 221, 331e345.
Kaewpintong, K., Shotipruk, A., Powtongsook, S., & Pavasant, P. (2007). Photoau-
totrophic high-density cultivation of vegetative cells of Haematococcuspluvialis
in airlift bioreactor. Bioresource Technology, 98, 288e295.
Koru, E. (2009). Earth food spirulina(Arthrospira): Production and quality
standards. Turkey Journal of Agriculture, - May-June 2008, (11), 133e134.
Year:3.
Lee, Y. K., & Low, C. S. (1991). Effect of photobioreactor inclination on the biomass
productivity of an outdoor algal culture. Biotechnology and Bioengineering, 38,
995e1000.
Licamele, J. D., White, C. L. (2011). V-trough photobioreactor system and method of
use. U.S. Patent Application US2011/0258920 A1 (27 October 2011).
Low-Cost Algae ProductiondIs It Finally With Us? May 13, 2012 http://www.
algaeindustrymagazine.com/low-cost-algae-production-is-it-finally-with-us/.
Lucie, Novovesk´aa, Zapataa, Anastasia K. M., Zabolotneya, Jeffrey B.,
Atwood, Matthew C., & Sundstrom, Eric R. (2016). Optimizing microalgae
cultivation and wastewater treatment in large-scale offshore photobioreactors.
Algal Research, 18, 86e94.
Madhu, G. M., Satyanarayana, S. V., Kalpana, P., & Bindiya, P. (2015). Equilibrium and
kinetic studies of lead biosorption by three Spirulina (Arthrospira) species in
open raceway ponds. Journal of Biochemical Technology, 6(1), 894e909.
Madkour, FedekarFadel, Kamil, Abd El-Wahab, & Nasr, HodaShafik (2012).
170 R.A. Soni et al. / Trends in Food Science & Technology 69 (2017) 157e171
Production and nutritive value of Spirulina platensis in reduced cost media.
Egyptian Journal of Aquatic Research, 38, 51e57.
Masojídek, J., Pap´aˇcek, Sˇ, Sergejevova´, M., Jirka, V., Cˇ ervený , J., Kunc, J., …
Torzillo, G.
(2003). A closed solar photobioreactor for cultivation of microalgae under supra-
high irradiance: Basic design and performance. Journal of Applied Phycology,
15(2), 239e248.
Matsunaga, T., Takeyama, H., Sudo, H., Oyama, N., Ariura, S., Takano, H., et al. (1991).
Glutamate production from CO2 by marine cyanobacterium Synechococcus sp.
using a novel biosolar reactor employing light diffusing optical fibers. Applied
Biochemistry and Biotechnology, (28/29), 157e167.
Miro´n, Asterio S´anchez, Garcıa, Marie-Carmen Cero´n, Camacho, Francisco
Garcıa,
Grima, Emilio Molina, & Chisti, Yusuf (2002). Growth and biochemical charac-
terization of microalgal biomass produced in bubble column and airlift pho-
tobioreactors: Studies in fed-batch culture. Enzyme and Microbial Technology,
31(7), 1015e1023.
Miro´n, AsterioSa´nchez, Go´mez, Antonio Czontreras, Camacho, Francisco
García,
Grima, Emilio Molina, & Chisti, Yusuf (1999). Comparative evaluation of
compact photobioreactors for large-scale monoculture of microalgae. Journal of
Biotechnology, 70, 249e270.
Molina, E., Ferna´ndez, J., Acie´n, F. G., & Chisti, Y. (2001). Tubular
photobioreactor
design for algal cultures. Journal of Biotechnology, 92, 113e131.
Mori, K. (1985). Photoautotrophic bioreactor using visible solar rays condensed by
fresnel lenses and transmitted through optical fibers. Biotechnology and
Bioengineering Symposium Journal., 15, 331e345.
Newsted, J. L. (2004). Effect of light, temperature, and pH on the accumulation of
phenol by Selenastrumcapricornutum, a green alga. Ecotoxicology and Envi-
ronmental Safety, 59, 237e243 [PubMed].
Ogbonda, K. H., Aminigo, R. E., & Abu, G. O. (2007). Influence of temperature and pH
on biomass production and protein biosynthesis in a putative Spirulina sp.
Bioresource Technology, 98, 2207e2211 [PubMed].
Ogbonna, J. C., Ichige, E., & Tanaka, H. (2002). Interactions between photoautotro-
phic and heterotrophic metabolism in photoheterotrophic cultures of Euglena
gracilis. Applied Microbiology Biotechnology, 58, 532e538.
Ogbonna, J. C., Soejima, T., & Tanaka, H. (1999). An integrated solar and artificial
light system for internal illumination of photobioreactors. Journal of Biotech-
nology, 70, 289e297.
Olguín, E., Galicia, S., Mercado, G., & Pe´rez, T. (2003). Annual productivity of
Spir-
ulina (Arthrospira) and nutrient removal in a pig wastewater recycling process
under tropical conditions. 15, 249e257.
Pal, R., Gupta, A., & Tripathi, A. (2011). Impact of environmental factors on the
biomass production of Spirulina in different conditions. Vegetos-An International
Journal of Plant Research, 24(2), 142e148.
Pandey, J. P., & Tiwari, A. (2010). Optimization of biomass production of Spirulina
maxima. Journal of Algal Biomass Utilization, 1, 20e32.
Pandey, J. P., Tiwari, A., & Mishra, R. M. (2010). Evaluation of biomass production of
Spirulina maxima on different reported media. Journal of Algal Biomass Utili-
zation, 1(3), 70e81.
Papadaki, S., Kyriakopoulou, K., Stramarkou, M., Tzovenis, I., & Krokida, M. (2017).
Environmental assessment of industrially applied drying technologies for the
treatment of spirulina platensis. IOSR Journal of Environmental Science, Toxi-
cology and Food Technology, 11(1), 41e46.
Pirt, S. J., Lee, Y. K., Walach, M. R., Pirt, M. W., Balyuzi, H. H. M., & Bazin, M. J. (1983).
A tubular photobioreactor for photosynthetic production of biomass from car-
bon dioxide: Design and performance. Journal of Chemical Technology and
Biotechnology, 33B, 35e38.
Pohl, P., Kohlhase, M., & Martin, M. (1988). Photobioreactors for the axenic mass
cultivation of microalgae. In T. Stadler, J. Mollion, M. C. Verdus, Y. Karamanos,
H. Morvan, & D. Christiaen (Eds.), Algal biotechnology (pp. 209e217). London
and New York: Elsevier Applied Science.
Powls, S. B. (1985). Photo-inhibition of photosynthesis induced by visible light. Ann.
Rev. Plant Physiology, 35, 15e44.
Pragya, Namita, Pandey, Krishan K., & Sahoo, P. K. (2013). A review on harvesting, oil
extraction and biofuels production technologies from microalgae. Renewable &
Sustainable Energy Reviews, 24, 159e171. Academic Search Premier. Web. 10 Dec.
2015.
Pruvost, J., Pottier, L., & Legrand, J. (2006). Numerical investigation of hydrodynamic
and mixing conditions in a torus photobioreactor. Chemical Engineering Science,
61, 4476e4489.
Pulz, M. O., & Gross, W. (2004). Valuable products from biotechnology of micro-
algae. Applied Microbiology Biotechnology, 6, 635e648.
Rafiqul Islam, M., Hassan, A., Sulebele, G., Orosco, C., & Roustaian, P. (2003). In flu-
ence of temperature on growth and biochemical composition of Spirulina
platensis and Spirulina fusiformis. Iranian International Journal of Sciences, 4(2),
97e106.
Ramos de Ortega, A., & Roux, J. C. (1986). Production of Chlorella biomass in
different types of flat bioreactors in temperate zones. Biomass, 10, 141e156.
Raoof, B., Kaushika, B. D., & Prasanna, R. (2006). Formulation of a low-cost medium
for mass production of Spirulina. Biomass and Bioenergy, 30(6) , 537e542.
Richmond, A., Boussiba, S., Vonshak, A., & Kopel, R. (1993). A new tubular reactor for
mass production of microalgae outdoors. Journal of Applied Phycology, 5,
327e332.
Richmond, A., & Vonshak, A. (1978). Spirulina culture in Israel. Arch. Hydrobiol. Bein.
Ergebn. Limnology, 11, 274e280.
Richmond, A., & Zhang, C.-W. (2001). Optimization of a flat plate glass reactor for
mass production of Nannochloropsis sp. outdoors. Journal of Biotechnology, 85,
259e269.
Roberto, Parra-Saldivar (2015). Photosynthetic bioenergy utilizing CO2: An
approach on flue gases utilization for third generation biofuels. Journal of
Cleaner Production, 98, 53e65.
Saeid, A., & Chojnacka, K. (2015). Toward production of microalgae in photo-
bioreactors under temperate climate. Chemical Engineering Research and Design,
93, 377e391.
Samson, R., & Leduy, A. (1985). Multistage continuous cultivation of bluegreen alga
Spirulina maxima in the flat tank photobioreactors. Chemical Engineering Jour-
nal, 63, 105e112.
Samuel, G. S., Sofi, M. Y., & Masih, S. (2010). Potential of different light intensities on
the productivity of Spirulinaplatensis under agra conditions. Research Journal of
Agriculture Science, 1(4), 468e469.
Sassano, C. E. N., Gioielli, L. A., Almeida, K. A., Sato, S., Perego, P., Converti, A., et al.
(2007). Cultivation of Spirulinaplatensis by continuous process using ammo-
nium chloride as nitrogen source. Biomass and Bioenergy, 31, 593e598.
Sierra, E., Acien, F. G., Fernandez, J. M., Garcıa, C. J., Gonzalez, L., & Molina, E. (2008).
Characterization of a flat plate photobioreactor for the production of micro-
algae. Chemical Engineering Journal, 138, 136e147.
Singh, R. N., & Sharma, Shaishav (2012). Development of suitable photobioreactor
for algae production e a review. Renewable and Sustainable Energy Reviews, 16,
2347e2353.
Sjors, V. I., & Alessandro, F. (2010). Algae based biofuels, Applications and coproducts.
Environment and natural resources management working paper. Environment
climatechange. Bioenergy monitoring and assessment.
Slade, Raphael, & Bauen, Ausilio (2013). Micro-algae cultivation for Biofuels: Cost,
energy balance, environmental impacts and future prospects. Biomass & Bio-
energy, 53, 29e38.
Sudhakar, K., & Premalatha, M. (2012). Theoretical assessment of algal biomass
potential for carbon mitigation and biofuel production. Iranica Journal of Energy
& Environment, 3(3), 232e240. ISSN 2079e2115.
Sudhakar, K., & Premalatha, M. (2015). Characterization of micro algal biomass
through FTIR/TGA/CHN Analysis: Application to Scenedesmus sp. Energy Sour-
ces, Part A: Recovery, Utilization, and Environmental Effects, 37(21), 2330e2337.
Sudhakar, K., Premalatha, M., & Rajesh, M. (2014). Large-scale open pond algae
biomass yield analysis in India: A case study. International Journal of Sustainable
Energy, 33(2), 304e315.
Sudhakar, K., Rajesh, M., & Premalatha, M. A. (2012). Mathematical model to assess
the potential of algal bio-fuels in India. Energy Sources, Part A: Recovery, Utili-
zation, and Environmental Effects, 34(12), 1114e1120.
Torzillo, G., Pushparaj, B., Bocci, F., Balloni, W., Materassi, R., & Florenzano, G. (1986).
Production of Spirulina biomass in closed photobioreactors. Biomass, 11, 61e74.
Toyoshima, M., Aikawa, S., Yamagishi, T., Kondo, A., & Kawai, H. (2015). A pilot-scale
floating closed culture system for the multicellular cyanobacterium Arthrospira
platensis NIES-39. Journal of Applied Phycology, 27(6), 2191e2202. http://doi.
org/10.1007/s10811-014-0484-2.
Tredici, Mario R. (2004). Mass production of microalgae: Photobioreactors. Hand-
book of Microalgal Culture: Biotechnology and Applied Phycology, 1, 178e214.
Tredici, M. R., & ChiniZittelli, G. (1998). Efficiency of sunlight utilization: Tubular
versus flat photobioreactors. Biotechnology and Bioengineering, 57, 187e197.
Tredici, M. R., & Materassi, R. (1992). From open ponds to vertical alveolar panels:
The Italian experience in the development of reactors for the mass cultivation
of photoautotrophic microorganisms. Journal of Applied Phycology, 4, 221e231.
Tsoglin, L. N., Gabel, B. V., Fal’kovich, T. N., & Semenenko, V. E. (1996). Closed
photobioreactors for microalgal production. Russ, Journal of Plant Physi-
ology1996, 43(1), 131e136.
Ugwu, C. U., Aoyagi, H., & Uchiyama, H. (2008). Photobiorectors for mass cultivation
of algae. Bioresource Technology, 99, 4021e4028.
Ugwu, C. U., Ogbonna, J. C., & Tanaka, H. (2002). Improvement of mass transfer
characteristics and productivities of inclined tubular photobioreactors by
installation of internal static mixers. Applied Microbiology Biotechnology, 58,
600e607.
Ugwu, C. U., Ogbonna, J. C., & Tanaka, H. (2003). Design of static mixers for inclined
tubular photobioreactors. Journal of Applied Phycology, 15, 217e223.
Ugwu, C. U., Ogbonna, J. C., & Tanaka, H. (2005a). Light/dark cyclic movement of
algal cells in inclined tubular photobioreactors withwith internal static mixers
for efficient production of biomass. Biotechnology Letters, 27, 75e78.
Vardaka, E., Kormas, K. A., Katsiapi, M., Genitsaris, S., & Moustaka-Gouni, M.
(2016). Molecular diversity of bacteria in commercially available “Spirulina”
food supplements. PeerJ, 4, e1610.
Vega-Estrada, J., Montes-Horcasitas, M. C., Dominígues-Bocanegra, A. R., &
Can~izares-Villanueva, R. O. (2005). Haematococcuspluvialis cultivation in
split- cylinder internal-loop airlift photobioreactor under aeration conditions
avoid- ing cell damage. Applied Microbiology and Biotechnology, 68, 31e35.
Venkataraman, L. V., Bhagyalakshmi, N., & Ravishankar, G. A. (1995). Commercial
production of micro and macro algae problems and potentials. Indian Journal of
Microbiology, 35, 1e19.
Vonshak, A. (1997). Spirulina: Growth, physiology and biochemistry Spirulina pla-
tensis (Arthrospira). In A. Vonhask (Ed.), Physiology cell-biology and biotech-
nology (pp. 43e65). London: Taylor and Francis.
Vonshak, A., & Guy, R. (1987). Photo-inhibition as a limiting factor in outdoor
cultivation of Spirulinaplatensis. In T. Stadler (Ed.), Algal biotechnology (pp.
365e370). Elsevier Applied Science Publishers.
Vree, J. H., Bosma, R., Janssen, M., Barbosa, M. J., & Wijffels, R. H. (2015). Comparison
of four outdoor pilot-scale photobioreactors. Biotechnology for Biofuels, 8(1), 215.
 R.A. Soni et al. / Trends in Food Science & Technology 69 (2017) 157e171
Vymazal, J. (1990). Uptake of heavy metals by Cladophoraglomerata. Acta Hydro-
chimica et Hydrobiologica , 18, 657e665.
Watanabe, Y., & Saiki, H. (1997). Development of photobioreactor incorporating
Chlorella sp. for removal of CO2 in stack gas. Energy Conversion Management, 38,
499e503.
Yin, C., Daoust, K., Young, A., Tebbs, E. J., & Harper, D. M. (2017). Tackling community
undernutrition at Lake Bogoria, Kenya: The potential of spirulina (Arthrospira
fusiformis) as a food supplement. African Journal of Food, Agriculture, Nutrition
and Development, 17(1), 11603e11615.
Zarrouk, C. (1966). Contribution a` l'´etuded'unecyanophyc´eeinfluenc´ee de divers fac-
teurs physiques etchimiquessur la croissanceet la photosynth`ese de
Spirulina maxima (Setch. et Gardner) Geitler. Paris, France: University of Paris. PhD
Thesis. Zeng, X.-H., Danquah, M. K., Chen, X. D., & Lu, Y.-H. (2011). Microalgae
bioengi- neering: Autotrophic cultivation from CO2 fixation to biofuel production.
171
Renewable and Sustainable Energy Reviews, 15(6), 3252e3260.
Zeriouh, O., Reinoso-Moreno, J. V., Lo´pez-Rosales, L., Cero´n-García, M. D.
C., Sa´nchez-Miro´n, A., García-Camacho, F., & Molina-Grima, E. (2017). Biofouling
in photobioreactors for marine microalgae. Critical Reviews in Biotechnology, 1e18.
Zhang, L., Chen, L., Wang, J., Chen, Y., Gao, X., Zhang, Z., et al. (2015). Attached
cultivation for improving the biomass productivity of Spirulina platensis. Bio-
resource Technology, 181, 136e142.
Zhang, K., Kurano, N., & Miyachi, S. (2002). Optimized aeration by carbon dioxide
gas for microalgal production and mass transfer characterization in a vertical
flat-plate photobioreactor. Bioprocess and Biosystem Engineering, 25, 97e101.
Zittelli, G. C., Biondi, N., Rodolfi, L., & Tredici, M. R. (2013). Photobioreactors for mass
production of microalgae. In A. Richmond, & Q. Hu (Eds.), Handbook of micro-
algal culture: Applied phycology and biotechnology (pp. 225e266). Oxford:
Blackwell Publishing.