The Open Plant Science Journal




(Discontinued)

ISSN: 1874-2947 ― Volume 11, 2019
LETTER

Chlorella vulgaris as a Source of Essential Fatty Acids and Micronutrients: A Brief Commentary



Hércules Rezende Freitas*
Laboratory of Neurochemistry, Institute of Biophysics Carlos Chagas Filho, Federal University of Rio de Janeiro. Av. Carlos Chagas Filho, 373 - Cidade Universitária, Rio de Janeiro/RJ, 21941-902, Brazil

Abstract

Polyunsaturated fatty acids (PUFAs) comprise about 35-40% of the total lipid content from green algae Chlorella, reaching up to 24% linoleic acid and 27% α-linolenic acid in C. vulgaris. Also, microalgae nutrient composition may be modulated by changes in the culture medium, increasing fatty acid and microelement concentrations in the algae biomass. PUFAs, such as α-linolenic (n-3) and linoleic (n-6) acids, as well as its derivatives, are considered essential for dietary consumption, and their ability to regulate body chemistry has been recently explored in depth. A balanced fatty acid consumption is shown to counteract the negative effects of western diets, such as chronic inflammation and glucose intolerance. In this brief commentary, technological and practical uses of C. vulgaris are explored as means to improve dietary quality and, ultimately, human health.

Keywords: Chlorella, C. vulgaris, Polyunsaturated fatty acids, Food disorders, Obesity, Oxidative stress.


Article Information


Identifiers and Pagination:

Year: 2017
Volume: 10
First Page: 92
Last Page: 99
Publisher Id: TOPSJ-10-92
DOI: 10.2174/1874294701710010092

Article History:

Received Date: 17/01/2017
Revision Received Date: 24/02/2017
Acceptance Date: 20/06/2017
Electronic publication date: 25/08/2017
Collection year: 2017

© 2017 Hércules Rezende Freitas.

open-access license: This is an open access article distributed under the terms of the Creative Commons Attribution 4.0 International Public License (CC-BY 4.0), a copy of which is available at: https://creativecommons.org/licenses/by/4.0/legalcode. This license permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.


* Address correspondence to this author at the Laboratory of Neurochemistry, Institute of Biophysics Carlos Chagas Filho, Federal University of Rio de Janeiro. Av. Carlos Chagas Filho, 373 - Cidade Universitária, Rio de Janeiro/RJ, 21941-902, Brazil; Tel: +55(21)9.8612-2194; E-mail: freitasprof@biof.ufrj.br




1. INTRODUCTION

1.1. Data Collection and Review Design

Data collection was carried out using indexed electronic databases (e.g. PubMed, LILACS and PubMed Central) and archives from the following university libraries: Central Library of the Federal University of the State of Rio de Janeiro (UNIRIO) and Central Library of the Federal University of Rio de Janeiro (UFRJ). Search for printed and electronic periodic articles was carried out using the following keywords: “polyunsaturated fatty acids”, “Chlorella”, “Chlorella vulgaris”, “obesity” and “nutritional disorders”, including the terms of lexical proximity and articles written in the English or Portuguese languages.

Due to the large number of initial documents (n > 5498), a software (Zotero Standalone 4.0) was used to organize and select references. Considering the methodological limitations of this commentary, we have adapted our search procedures from Freitas et al. (2015) and from the PRISMA (i.e. Preferring Reporting Items for Systematic Reviews and Meta-Analyses) norms and standards, allowing systematic search, optimization of analysis and discussion of the data obtained [1Freitas HR, Pereira AS, Ramos TS. The effects of acute/chronic glutamine and glutamine peptide supplementation on the performance and immune function in young active adult athletes. Curr Nutr Food Sci 2015; 11(4): 315-22.
[http://dx.doi.org/10.2174/1573401311666150729225554]
]. Table 1 compiles the selected works to provide an overview of data on Chlorella microalgae and its effects on health.

1.2. Obesity and Fatty Acids

Human struggle for gathering food on early social formations resulted in reproductive success, complex societies and the subsequent development of culture, mythology, gender specialization of work and other socially hereditary traits. In the last 10.000 years, our species has dominated virtually all habitable land on earth, and two centuries of intense scientific/technologic development ensured the control of food production, storage and transport, in a way that most individuals from developed and developing countries have access to their daily essential nutrient needs.

Despite the benefits of social integration, urban conglomerates now regularly exceed the consumption of basic nutrient needs through a process known as overfeeding, as a consequence of both cultural and behavioral adaptations to modern life and high viability of processed food. More than 1.1 billion people worldwide are overweight, and approximately 1/3 of them have reached obesity [2Haslam DW, James WP. Obesity. Lancet 2005; 366(9492): 1197-209.
[http://dx.doi.org/10.1016/S0140-6736(05)67483-1] [PMID: 16198769]
]. Western countries have the highest obesity indexes, with ~ 36% adults and ~ 17% children/adolescent classified as overweight/obese in the USA [3Flegal KM, Carroll MD, Kit BK, Ogden CL. Prevalence of obesity and trends in the distribution of body mass index among US adults, 1999-2010. JAMA 2012; 307(5): 491-7.
[http://dx.doi.org/10.1001/jama.2012.39] [PMID: 22253363]
-5Ogden CL, Carroll MD, Kit BK, Flegal KM, et al. Prevalence of obesity among adults: United States, 2011–2012. JAMA 2014; 311(8): 806-14.
[http://dx.doi.org/10.1001/jama.2014.732] [PMID: 24570244]
]. Also, ~ 20% of adult population from Americas and Caribe are, at least, overweight [2Haslam DW, James WP. Obesity. Lancet 2005; 366(9492): 1197-209.
[http://dx.doi.org/10.1016/S0140-6736(05)67483-1] [PMID: 16198769]
]. In 2014, an estimative from the World Health Organization pointed out that 39% of adults (aged 18 y.o. or older, 38% of men and 40% of women) were overweight, which is nearly two-fold the value estimated in 1980 [6 World Health Organization (WHO). Global status report on noncommunicable diseases 2014. WHO Library Cataloguing-in-Publication Data.].

Table 1
Experimental works evaluating Chlorella vulgaris as a potential dietary resource.


An acknowledged component of chronic obesity is inflammation, with recent evidence suggesting that perturbations in gut microbiota and permeability are the main triggers for the development of obesity-associated inflammation [7Cox AJ, West NP, Cripps AW. Obesity, inflammation, and the gut microbiota. Lancet Diabetes Endocrinol 2015; 3(3): 207-15.
[http://dx.doi.org/10.1016/S2213-8587(14)70134-2] [PMID: 25066177]
]. In this context, the balance between n-3/n-6 polyunsaturated fatty acids (PUFAs) is a key control mechanism in the production of inflammatory/anti-inflammatory mediators. While arachidonic acid (n-6 derivative) gives rise to pro-inflammatory eicosanoids, eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA), which are n-3 derivatives, function as substrates for the synthesis of resolvins, autacoids with high anti-inflammatory and tissue-protective properties [8Calder PC. Fatty acids and inflammation: the cutting edge between food and pharma. Eur J Pharmacol 2011; 668(September)(Suppl.1): S50-8.
[http://dx.doi.org/10.1016/j.ejphar.2011.05.085] [PMID: 21816146]
-9Hsiao HM, Sapinoro RE, Thatcher TH, et al. A novel anti-inflammatory and pro-resolving role for resolvin D1 in acute cigarette smoke-induced lung inflammation. PLoS One 2013; 8(3): e58258.
[http://dx.doi.org/10.1371/journal.pone.0058258] [PMID: 23484005]
]. Dietary n-3/n-6 ratios of 1:6 to 1:4 have been proposed to ensure lifelong health and cardiovascular safety, and experimental studies even suggest the benefits of 1:1 ratios to improve obesity-linked inflammation and insulin resistance in rats [10Liu HQ, Qiu Y, Mu Y, et al. A high ratio of dietary n-3/n-6 polyunsaturated fatty acids improves obesity-linked inflammation and insulin resistance through suppressing activation of TLR4 in SD rats. Nutr Res 2013; 33(10): 849-58.
[http://dx.doi.org/10.1016/j.nutres.2013.07.004] [PMID: 24074743]
].

Equilibrium between the dietary amounts of PUFAs is not easily achieved in urban societies, mainly due to the low availability of in natura animal or vegetable sources of n-3 fatty acids. Consumption of fish is highly associated with long-term cardiovascular health, and can optimize the availability of long-chain fatty acids in the blood of human subjects. Also, authors suggest that supplementation with fish oil may improve gestational health status (reviewed in [11Williams CM, Burdge G. Long-chain n-3 PUFA: plant v. marine sources. Proc Nutr Soc 2006; 65(1): 42-50.
[http://dx.doi.org/10.1079/PNS2005473] [PMID: 16441943]
]. While supplementation with fish oil is a good source for replenishing n-3 needs, there is still a demand for non-expensive, cultivable food to be included in western diets.

Chlorella unicellular green algae species, mainly C. vulgaris, are easy to be cultivated and behave metabolically according to the nutrients provided in the medium. Biomass obtained from Chlorella can be used in the industry, in food preparations, or in nutritional supplements, and data show promising results from the use of each of it [12Xu H, Miao X, Wu Q. High quality biodiesel production from a microalga Chlorella protothecoides by heterotrophic growth in fermenters. J Biotechnol 2006; 126(4): 499-507.
[http://dx.doi.org/10.1016/j.jbiotec.2006.05.002] [PMID: 16772097]
-14Vecina JF, Oliveira AG, Araujo TG, et al. Chlorella modulates insulin signaling pathway and prevents high-fat diet-induced insulin resistance in mice. Life Sci 2014; 95(1): 45-52.
[http://dx.doi.org/10.1016/j.lfs.2013.11.020] [PMID: 24333277]
].

One cannot, however, infer that only microalgae consumption is enough to provide sufficient dietetic PUFA levels. Known plant sources, for example, may be capable of supporting membrane turnover and renewal in health adults with modest DHA/EPA demands, but no long-term prevention of affections, such as cardiovascular events, should be claimed [11Williams CM, Burdge G. Long-chain n-3 PUFA: plant v. marine sources. Proc Nutr Soc 2006; 65(1): 42-50.
[http://dx.doi.org/10.1079/PNS2005473] [PMID: 16441943]
]. Fish is still the main and ideal source of PUFAs in the human diet, and the results indicating otherwise have been shown as misleading and/or inconclusive [15Nichols PD, Kitessa SM, Abeywardena M. Commentary on a trial comparing krill oil versus fish oil. Lipids Health Dis 2014; 13: 2.
[http://dx.doi.org/10.1186/1476-511X-13-2] [PMID: 24383554]
]. Here, C. vulgaris is presented as a possible complementary PUFAs source to optimize n-3/n-6 composition of the diet.

1.3. Chlorella is Rich in Polyunsaturated Fatty Acids

George and Mildred Burr (1929) were the first to demonstrate the essentiality of unsaturated fatty acids, specially PUFAs, when the signs of deficiency were prevented or cured by providing dietetic linoleic acid (n-6), even if compared to butter or coconut oil [16Smith W, Mukhopadhyay R. Essential fatty acids: the work of George and Mildred Burr. J Biol Chem 2012; 287(42): 35439-41.
[http://dx.doi.org/10.1074/jbc.O112.000005] [PMID: 23066112]
]. As previously pointed, besides being essential, PUFAs must be provided in an adequate proportion (i.e. n-3/n-6 ~1:6) to ensure life-long health status [10Liu HQ, Qiu Y, Mu Y, et al. A high ratio of dietary n-3/n-6 polyunsaturated fatty acids improves obesity-linked inflammation and insulin resistance through suppressing activation of TLR4 in SD rats. Nutr Res 2013; 33(10): 849-58.
[http://dx.doi.org/10.1016/j.nutres.2013.07.004] [PMID: 24074743]
]. Unfortunately, current western fatty acid intake follows a trend towards higher n-6 to n-3 proportion, and epidemiologic studies indicate a consumption of ~1:16 (n-3/n-6) by these populations. While ratios of up to 1:6 or lower suggest beneficial long-term effects, 1:10 or greater proportions are indicative of future adverse consequences [17Alarcón G, Roco J, Medina A, Van Nieuwenhove C, Medina M, Jerez S. Stearoyl-CoA desaturase indexes and n-6/n-3 fatty acids ratio as biomarkers of cardiometabolic risk factors in normal-weight rabbits fed high fat diets. J Biomed Sci 2016; 23: 13.
[http://dx.doi.org/10.1186/s12929-016-0235-6] [PMID: 26792598]
].

Chlorella have high concentrations of polyunsaturated fatty acids, and almost 1:1 proportion of n-3/n-6 PUFAs [18Petkov G, Garcia G. Which are fatty acids of the green alga Chlorella? Biochem Syst Ecol 2007; 35: 281-5.
[http://dx.doi.org/10.1016/j.bse.2006.10.017]
]. Also, analysis of fatty acid composition obtained from C. vulgaris indicates that, among the 19 different fatty acids found, 5 were saturated and 14 were C14 to C24 unsaturated fatty acids [19Sibi G. Inhibition of lipase and inflammatory mediators by Chlorella lipid extracts for antiacne treatment. J Adv Pharm Technol Res 2015; 6(1): 7-12.
[http://dx.doi.org/10.4103/2231-4040.150364] [PMID: 25709963]
]. Bewicke and Potter (1993), in a book entitled “Chlorella: The Emerald Food”, highlight the beneficial possibilities of including Chlorella in the western diets, these are: high growth rate, high protein content, resistance to climatic variations, high nutritive value and digestibility, palatability, economical production and others[20]. Recent authors, for instance, suggest the use of Chlorella species as biofactories for n-3 fatty acids [21Adarme-Vega TC, Lim DK, Timmins M, Vernen F, Li Y, Schenk PM. Microalgal biofactories: a promising approach towards sustainable omega-3 fatty acid production. Microb Cell Fact 2012; 11: 96.
[http://dx.doi.org/10.1186/1475-2859-11-96] [PMID: 22830315]
, 22Ferreira SP, Holz JC, Lisboa CR, Costa JA. Fatty acid profile of Chlorella biomass obtained by fed batch heterotrophic cultivation. Int Food Res J 2017; 24(1): 284-91.].

Long-chain n-3 and n-6 fatty acids comprise 35-40% of the total lipid content in algae from Chlorella genus, reaching up to 24% linoleic acid and 27% α-linolenic acid in C. vulgaris [18Petkov G, Garcia G. Which are fatty acids of the green alga Chlorella? Biochem Syst Ecol 2007; 35: 281-5.
[http://dx.doi.org/10.1016/j.bse.2006.10.017]
], which are an accessible source for these essential fatty acids. The possibility of modulation in lipid concentrations through changes in culture medium has stimulated research since the mid-twentieth century [23Harris RV, James AT. The fatty acid metabolism of Chlorella vulgaris. Biochim Biophys Acta 1965; 106(3): 465-73.
[http://dx.doi.org/10.1016/0005-2760(65)90063-9] [PMID: 5881329]
], either for the synthesis of biomass or to satisfy animal/human nutritional demand.

Several groups have explored methods for cultivation of lipid-rich microalgae, aiming mainly to increase biofuel productivity[24]. Some methods, however, may also show high potential application in food industry[25]. Liu, Wang and Zhou (2008) explored the effects of variable iron chloride (FeCl3) chelate concentrations in augmenting total C. vulgaris lipid content. Data showed that 1.2 x 10-5 mol/L-1 FeCl3 may increase fatty acid concentrations up to 56.6% of the total biomass [26Liu ZY, Wang GC, Zhou BC. Effect of iron on growth and lipid accumulation in Chlorella vulgaris. Bioresour Technol 2008; 99(11): 4717-22.
[http://dx.doi.org/10.1016/j.biortech.2007.09.073] [PMID: 17993270]
].

Lv et al. (2010) observed that sensible variations in cultivation settings could significantly raise (2.5-fold compared to previous results) lipid content in C. vulgaris[27]. A growth protocol using nutrient-rich medium, followed by sudden/acute nutrient depletion, changes in air availability and light intensity induced a final 53% lipid content in total biomass from C. vulgaris cultures [28Mujtaba G, Choi W, Lee CG, Lee K. Lipid production by Chlorella vulgaris after a shift from nutrient-rich to nitrogen starvation conditions. Bioresour Technol 2012; 123: 279-83.
[http://dx.doi.org/10.1016/j.biortech.2012.07.057] [PMID: 22940330]
]. Other groups suggest that incubation under high CO2 levels, nitrogen depletion and reduced incubation time are efficient strategies to increase total lipid mass in these cultivations [29Widjaja A, Chien C, Ju Y. Study of increasing production from fresh water microalgae Chlorella vulgaris. J Taiwan Inst Chem Eng 2009; 40: 2013-4.
[http://dx.doi.org/10.1016/j.jtice.2008.07.007]
].

Satisfactory fatty acid levels in Chlorella may be achieved through stimulus with several stressors, however, to generate a selective increase in PUFAs rather than monounsaturated (MUFAs) and saturated (SAFAs) fatty acids is a more demanding work. Limiting PO43-, for example, may result in higher SAFA, MUFA and 18:2n-6 (linoleic acid) content [30Chia MA, Lombardi AT, Melão MdaG, Parrish CC. Lipid composition of Chlorella vulgaris (Trebouxiophyceae) as a function of different cadmium and phosphate concentrations. Aquat Toxicol 2013; 128-129: 171-82.
[http://dx.doi.org/10.1016/j.aquatox.2012.12.004] [PMID: 23306106]
]; Also, in a previous review of PUFA sources, authors highlighted Chlorella (C. minutissima) to be effective for arachidonic acid (AA) and EPA production, but not DHA [31Abedi E, Sahari MA. Long-chain polyunsaturated fatty acid sources and evaluation of their nutritional and functional properties. Food Sci Nutr 2014; 2(5): 443-63.
[http://dx.doi.org/10.1002/fsn3.121] [PMID: 25473503]
].

Immobilization of C. vulgaris with the plant growth promoting bacteria (PGPB) Azospirillum brasilense resulted in a large increase of the lipid content from C. vulgaris, with approximately 95-98% of fatty acids with 16-18 carbon chains at the final Chlorella mass [32Leyva LA, Bashan Y, Mendoza A, de-Bashan LE. Accumulation of fatty acids in Chlorella vulgaris under heterotrophic conditions in relation to activity of acetyl-CoAcarboxylase, temperature, and co-immobilization with Azospirillum brasilense [corrected]. Naturwissenschaften 2014; 101(10): 819-30.
[http://dx.doi.org/10.1007/s00114-014-1223-x] [PMID: 25129521]
]; increasing CO2 concentration to 2.6% (v/v of culture environment), in turn, promoted a 6-fold positive change in lipid production, with higher intracellular acetyl-CoA content, which is pivotal for fatty acid synthesis [33Jose S, Suraishkumar GK. High carbon (CO2) supply leads to elevated intracellular acetyl CoA levels and increased lipid accumulation in Chlorella vulgaris. Algal Res 2016; 19: 307-15.
[http://dx.doi.org/10.1016/j.algal.2016.08.011]
]. Finding adequate methods for selectively increasing SAFA, MUFA or PUFA content in C. vulgaris and other Chlorella species may favor the standardization of these microalgae in the food industry.

1.4. Dietary Use and Effects of Chlorella on Health

Beside its nutritional value, C. vulgaris was also shown to modulate immune mechanisms and to counteract the growth of cancerous cells. When provided as food for senescent humans or model animals, C. vulgaris protected both from the development of age-associated diseases, specially hypertension and hyperlipidemia[25], and the general response to stress. Sprague-Dawley rats supplemented (by gavage) with C. vulgaris (50 or 200mg/Kg/b.w.), for instance, showed diminished peripheral and central responses to forced swimming stress tests, as seen through smaller corticotropin-releasing factor and c-fos expression levels [34Souza Queiroz J, Marín Blasco I, Gagliano H, et al. Chlorella vulgaris reduces the impact of stress on hypothalamic-pituitary-adrenal axis and brain c-fos expression. Psychoneuroendocrinology 2016; 65: 1-8.
[http://dx.doi.org/10.1016/j.psyneuen.2015.12.002] [PMID: 26685709]
].

Bae et al. (2013) investigated the effects of C. vulgaris aqueous extracts on in vitro immuno-allergic responses using rat peritoneal mast cells, and in vivo through evaluation of plasma markers. Data showed that the aqueous extract is capable of suppressing histamine release via modulation of T helper 1 (Th1) activity, thus attenuating allergenic responses in these animals [35Bae MJ, Shin HS, Chai OH, Han JG, Shon DH. Inhibitory effect of unicellular green algae (Chlorella vulgaris) water extract on allergic immune response. J Sci Food Agric 2013; 93(12): 3133-6.
[http://dx.doi.org/10.1002/jsfa.6114] [PMID: 23426977]
]. In addition, C. vulgaris dry extracts may modulate oxidative damage in chronically stressed individuals. A study providing 3600 mg/day (six weeks) dry C. vulgaris extract to non-comorbidity bearing smokers showed significant decrease in lipid peroxidation and optimized antioxidant status of participants[36]. Other Chlorella species (C. pyrenoidosa) were also shown to be beneficial for the treatment of signs and symptoms, specifically of fibromyalgia, hypertension, and ulcerative colitis. In this study, patients were supplemented daily with 10 g of Chlorella in tablets plus 100 mL of a liquid Chlorella extract for 2 to 3 months in a double-blind, placebo-controlled, randomized clinical trial [37Merchant RE, Andre CA. A review of recent clinical trials of the nutritional supplement Chlorella pyrenoidosa in the treatment of fibromyalgia, hypertension, and ulcerative colitis. Altern Ther Health Med 2001; 7(3): 79-91.
[PMID: 11347287]
].

When supplemented in the diet of Atlantic salmon (Salmo salar L.), C. vulgaris attenuated in vivo gut inflammatory symptoms [38Grammes F, Reveco FE, Romarheim OH, Landsverk T, Mydland LT, Øverland M. Candida utilis and Chlorella vulgaris counteract intestinal inflammation in Atlantic salmon (Salmo salar L.). PLoS One 2013; 8(12): e83213.
[http://dx.doi.org/10.1371/journal.pone.0083213] [PMID: 24386162]
], suggesting applicability in the treatment of human gastrointestinal diseases, such as Crohn’s disease and hypersensitivity to prolamins (e.g. wheat gliadin, commonly known as gluten). In a randomized, double-blind clinical trial, Kwak et al. (2012) showed that supplementation with C. vulgaris can optimize innate immune response, stimulating the activity of Natural Killer cells and raising the concentration of interleukins associated to defense against pathogens [39Kwak JH, Baek SH, Woo Y, et al. Beneficial immunostimulatory effect of short-term Chlorella supplementation: enhancement of natural killer cell activity and early inflammatory response (randomized, double-blinded, placebo-controlled trial). Nutr J 2012; 11: 53.
[http://dx.doi.org/10.1186/1475-2891-11-53] [PMID: 22849818]
]. In addition, detectable methylcobalamin (i.e. vitamin B12) [40Kumudha A, Selvakumar S, Dilshad P, Vaidyanathan G, Thakur MS, Sarada R. Methylcobalamin--a form of vitamin B12 identified and characterised in Chlorella vulgaris. Food Chem 2015; 170: 316-20.
[http://dx.doi.org/10.1016/j.foodchem.2014.08.035] [PMID: 25306351]
] and high phosphorus [41Tokusoglu O, Uunal MK. Biomass nutrient profiles of three microalgae: Spirulina platensis, Chlorella vulgaris, and Isochrisis galbana. J Food Sci 68: 4.] levels were found in C. vulgaris samples, again pointing towards the relevant nutritional value of Chlorella microalgae.

In a recent in vitro study, Sibi (2015) evaluated the antimicrobial activity of lipidic extracts from Chlorella microalgae (including C. vulgaris) against Propionibacterium acnes strains. Data showed that Chlorella promotes inhibitory effects over P. acnes through attenuation of lipase activity. Also, Chlorella extracts modulated oxidative and inflammatory responses from human peripheral blood mononuclear cells stimulated by heat-killed P. acnes [19Sibi G. Inhibition of lipase and inflammatory mediators by Chlorella lipid extracts for antiacne treatment. J Adv Pharm Technol Res 2015; 6(1): 7-12.
[http://dx.doi.org/10.4103/2231-4040.150364] [PMID: 25709963]
]. Sun et al. (2014) proposed the use of selenium-enriched C. vulgaris cultures as means to induce bioaccumulation, producing antioxidant-rich biomass with applications in agriculture and human diet. Data showed that C. vulgaris is satisfactorily tolerant to selenium accumulation in culture [42Sun X, Zhong Y, Huang Z, Yang Y. Selenium accumulation in unicellular green alga Chlorella vulgaris and its effects on antioxidant enzymes and content of photosynthetic pigments. PLoS One 2014; 9(11): e112270.
[http://dx.doi.org/10.1371/journal.pone.0112270] [PMID: 25375113]
].

As indicated by previous studies, Chlorella may be used as a dietary antioxidant [36Panahi Y, Mostafazadeh B, Abrishami A, et al. Investigation of the effects of Chlorella vulgaris supplementation on the modulation of oxidative stress in apparently healthy smokers. Clin Lab 2013; 59(5-6): 579-87.
[PMID: 23865357]
, 42Sun X, Zhong Y, Huang Z, Yang Y. Selenium accumulation in unicellular green alga Chlorella vulgaris and its effects on antioxidant enzymes and content of photosynthetic pigments. PLoS One 2014; 9(11): e112270.
[http://dx.doi.org/10.1371/journal.pone.0112270] [PMID: 25375113]
]. In a recent work, patients (n=30) with non-alcoholic liver steatosis were supplemented with 400 mg/day vitamin E and 1200 mg/day C. vulgaris extract. The combination was shown to be effective in reducing body mass, activity of liver enzymes, fasting glucose and controlling lipid profile [43Ebrahimi-Mameghani M, Aliashrafi S, Javadzadeh Y, AsghariJafarabadi M. The effect of Chlorella vulgaris supplementation on liver enzymes, serum glucose and lipid profile in patients with non-alcoholic fatty liver disease. Health Promot Perspect 2014; 4(1): 107-15.
[PMID: 25097844]
]. These data corroborate with the previous results from Vecina et al. (2014), where rodents supplemented with C. vulgaris for twelve weeks showed tolerance to high-fat diets, reduced triglyceride, cholesterol and free fatty acid levels. Authors suggest that C. vulgaris is capable of modulating signaling pathways associated to insulin [14Vecina JF, Oliveira AG, Araujo TG, et al. Chlorella modulates insulin signaling pathway and prevents high-fat diet-induced insulin resistance in mice. Life Sci 2014; 95(1): 45-52.
[http://dx.doi.org/10.1016/j.lfs.2013.11.020] [PMID: 24333277]
].

Also, data show that C. vulgaris may be incorporated to food products, such as pasta, thus enhancing both nutritional and sensorial quality without affecting processing [44Fradique M, Batista AP, Nunes MC, Gouveia L, Bandarra NM, Raymundo A. Incorporation of Chlorella vulgaris and Spirulina maxima biomass in pasta products 2010.]. Chlorella may also be added to cookies [45Bang BH, Kim KP, Jeong EJ. Quality characteristics of cookies that contain different amounts of Chlorella powder. Korean J Food Preserv 2013; 20(6): 798-804.
[http://dx.doi.org/10.11002/kjfp.2013.20.6.798]
], yellow layer cake [46Kim KJ, Chung HC. Quality characteristics of yellow layer cake containing different amounts of chlorella powder. Korean J Food Cookery Sci 2010; 26(6): 860-5.
[http://dx.doi.org/10.5851/kosfa.2010.30.5.860]
], imitation processed cheese [47Shalaby SM, Yasin NM. Quality characteristics of croissant stuffed with imitation processed cheese containing microalgae Chlorella vulgaris biomass. World J Dairy Food Sci 2013; 8(1): 58-66.], and others, without modifying sensorial/nutritional properties. Some Chlorella substitutions may significantly cheapen the food price, when compared with the original preparation. Increasing nutritional value of food with low cost is relevant, and may be decisive for permanence in the market.

1.5. Toxicity of Chlorella

No studies directly linking Chlorella ingestion to toxicity or chronic health risks were found. It suggests, however, that the risk of intake by susceptible populations was also not evaluated, implying that pregnant, immunosuppressed, infants and older individuals should avoid using any phytotherapic drug and/or supplement without previous medical prescription, as it is recommended for any other plant extract without complete evidence for safety/effectivity.

Chlorella, however, may be exposed to contamination and bioaccumulation (e.g. Zn2+ and Cd2+) like that of plant crops [48Roy M, McDonald LM. Metal uptake in plants and health risk assessments in metal-contaminated smelter soils. Land Degrad Dev 2015; 26: 785-92.
[http://dx.doi.org/10.1002/ldr.2237]
], once cultivable algae is highly susceptible to changes in nutrient composition. Alam et al. (2015) showed that C. vulgaris may accumulate 80% Zn2+ and 60% Cd2+ from culture medium, efficiently cleaning contaminated water [49Alam MA, Wan C, Zhao XQ, Chen LJ, Chang JS, Bai FW. Enhanced removal of Zn(2+) or Cd(2+) by the flocculating Chlorella vulgaris JSC-7. J Hazard Mater 2015; 289: 38-45.
[http://dx.doi.org/10.1016/j.jhazmat.2015.02.012] [PMID: 25704433]
]. C. vulgaris was also shown to accumulate arsenic when inoculated in rice crops, thus attenuating metal levels in the plant [50Upadhyay AK, Singh NK, Singh R, Rai UN. Amelioration of arsenic toxicity in rice: Comparative effect of inoculation of Chlorella vulgaris and Nannochloropsis sp. on growth, biochemical changes and arsenic uptake. Ecotoxicol Environ Saf 2016; 124: 68-73.
[http://dx.doi.org/10.1016/j.ecoenv.2015.10.002] [PMID: 26473328]
]. When cultivated for feeding purposes, however, it’s important to know not only the composition of Chlorella, but also the microorganisms potentially cohabitating in the nutritive environment.

Cultivated algae, similar to plants, are relatively permissive to the growth of microorganisms, which may be lately consumed by the human population. Data suggests that algal symbiotic bacteria, especially Pseudomonas sp., may grow and develop a mutualistic relationship with C. vulgaris (ATCC 13482) under photoautotrophic conditions, and that Chlorella may benefit from the presence of these organisms in culture medium, as suggested by the increase in algae cell and chlorophyll concentrations in culture [51Guo Z, Tong YW. The interactions between Chlorella vulgaris and algal symbiotic bacteria under photoautotrophic and photoheterotrophic conditions. J Appl Phycol 2014; 26: 1483.
[http://dx.doi.org/10.1007/s10811-013-0186-1]
].

In a previous literature review, Safi et al. (2014) pointed out that, despite numerous health benefits and rich nutrient composition, C. vulgaris and other algae are used mainly as nutraceuticals rather than as/in food products due to the lack of a common regulatory legislation capable of stablishing quality and good practice requirements for microalgae cultivation (see [52Safi C, Zebib B, Merah O, Pontalier PY, Vaca-Garcia C. Morphology, composition, production, processing and applications of Chlorella vulgaris: A review. Renew Sustain Energy Rev 2014; 35: 265-78.
[http://dx.doi.org/10.1016/j.rser.2014.04.007]
]). These procedures, when sufficiently regulated by law, may represent an important step in the introduction of safely grown microalgae in the diet of western populations.

CONCLUSION

Chlorella vulgaris is regularly used as food, nutritional supplement, soil nutrient for plants and in the synthesis of biomass. Unfortunately, western countries tend to consume lower amounts of microalgae than Asian nations. One reason for such is the low variety of Chlorella food products available in the market. The growth of soy and soy-derivative products, however, may stimulate the industry to apply processed algae into a myriad of formulations, once it has the advantage of being highly susceptible to manipulation in its centesimal composition, specially referring to lipid content.

Application of C. vulgaris in the food industry is not new, however, it is usually consumed in larger amounts by countries where western diet is uncommon. Developing palatable Chlorella-enriched food may increase total PUFA content in food and ultimately optimize the proportion of essential fatty acids in the diet, ensuring improvements in several aspects of health, such as plasma lipids, insulin sensitivity, immune response and inflammation.

CONFLICT OF INTEREST

The author declares no conflict of interest, financial or otherwise.

ACKNOWLEDGEMENTS

H. R. Freitas is the recipient of a CNPq (National Counsel of Technological and Scientific Development) fellowship.

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