Acessibilidade / Reportar erro

Moringa oleifera potential as a functional food and a natural food additive: a biochemical approach

Abstract

Several works have shown different aspects of the use of the plant Moringa oleifera. However, few review studies bring an approach to its use in food preparation, specifying its role as a functional food and its use as a natural additive, focusing on food biochemistry and including sensory acceptance and safety. Composed by multiple bioactive substances, Moringa oleifera has the potential to be used as a food additive, mainly as a preservative with the potential to prevent lipid oxidation and other unwanted chemical reactions that lead to product deterioration. Furthermore, it can improve the physicochemical characteristics of food, increasing its quality and shelf life. It also promotes nutritional improvement, elevating protein, mineral, and vitamin levels. Despite this, the sensorial characteristics of this plant result in a low consumer acceptance of the fortified products, which is a problem for the food industry. Apart from inconclusive works, some data involving Moringa’s safety are contradictory, resulting in its commercialization prohibition in Brazil in 2019. This review focused on important data about Moringa use to contribute to the literature and to the food industry, describing information about this medicinal plant effects on food products.

Key words
bioactive compounds; food biochemistry; food fortification; medicinal plant; nutritional improvement

INTRODUCTION

With the growing interest in healthy lifestyle, functional foods have become popular and recurrent in the human diet. Consequently, this global market niche has been expanding constantly, and its innovation is being stimulated (Barauskaite et al. 2018BARAUSKAITE D, GINEIKIENE J, FENNIS BM, AURUSKEVICIENE V, YAMAGUCHI M & KONDO N. 2018. Eating healthy to impress: How conspicuous consumption, perceived self-control motivation, and descriptive normative influence determine functional food choices. Appetite 131: 59-67. https://doi.org/10.1016/j.appet.2018.08.015., Farag et al. 2020FARAG MA ET AL. 2020. Metabolomics reveals impact of seven functional foods on metabolic pathways in a gut microbiota model. J Adv Res 23: 47-59. https://doi.org/10.1016/j.jare.2020.01.001.). Functional food is defined as food products that incorporate or enhance ingredients that offer health benefits, in addition to nutritional values, modulating bodily functions, which can improve the immune response or decrease the risk of diseases and comorbidities (Farag et al. 2020FARAG MA ET AL. 2020. Metabolomics reveals impact of seven functional foods on metabolic pathways in a gut microbiota model. J Adv Res 23: 47-59. https://doi.org/10.1016/j.jare.2020.01.001., Contreras-Rodriguez et al. 2020CONTRERAS-RODRIGUEZ O, MATA F, VERDEJO-ROMÁN J, RAMÍREZ-BERNABÉ R, MORENO D, VILAR-LOPEZ R, SORIANO-MAS C & VERDEJO-GARCÍA A. 2020. Neural-based valuation of functional foods among lean and obese individuals. Nutr Res 78: 27-35. https://doi.org/10.1016/j.nutres.2020.03.006.). Each country, or trading blocs, defines and regulates the approval criteria for the use of a functional food independently (Stringheta et al. 2007STRINGHETA PC, OLIVEIRA TTD, GOMES RC, AMARAL MDPHD, CARVALHO AFD & VILELA MAP. 2007. Health policies and functional property and health claims for food in Brazil. Rev Bras Cien Farm 43(2): 181-194. https://doi.org/10.1590/S1516-93322007000200004.).

In the food industry, food shelf life and their sensory characteristics maintenance during storage are important concerns. Hence, the use of food additives is essential in most industrialized products. The regulation for its use, although strict, is still controversial, as there are a large number of studies with divergent results. Moreover, there are different interpretations by the governments (Silva & Lidon 2016SILVA MM & LIDON F. 2016. Food preservatives–An overview on applications and side effects. Emir J Food Agr 28(6): 366-373. https://doi.org/10.9755/ejfa.2016-04-351., Carocho et al. 2014CAROCHO M, BARREIRO MF, MORALES P & FERREIRA IC. 2014. Adding molecules to food, pros and cons: A review on synthetic and natural food additives. Compr Rev Food Sci F 13(4): 377-399. https://doi.org/10.1111/1541-4337.12065.). An alternative to synthetic food additives is the natural additives, obtained from plants, fungi, algae and animals, often used empirically by the population. Amongst the various beneficial effects that can be promoted by natural food additives, antimicrobial and antioxidant activity are the ones which arouse the biggest interest in the food industry (Bearth et al. 2014BEARTH A, COUSIN ME & SIEGRIST M. 2014. The consumer’s perception of artificial food additives: Influences on acceptance, risk and benefit perceptions. Food Qual Prefer 38: 14-23. https://doi.org/10.1016/j.foodqual.2014.05.008.).

Moringa oleifera is one of the various medicinal plants that can be used both as a functional food and as a natural food additive. Belonging to the Moringacea family of perennial angiosperm plants, which includes 12 other species, this plant is widely cultivated in the Middle East, Africa, and Asia (Farid & Hegazy 2019FARID AS & HEGAZY AM. 2019. Ameliorative effects of Moringa oleifera leaf extract on levofloxacin-induced hepatic toxicity in rats. Drug Chem Toxicol 43(6): 616-622. https://doi.org/10.1080/01480545.2019.1574811., Hisam et al. 2018). Moringa has been used for centuries, with reference to its use in more than 80 countries, and researches about its nutritional values have been carried out since 1970. In 1998, the World Health Organization (WHO) promoted this plant as an alternative supplement to treat malnutrition. (Mahmood et al. 2010MAHMOOD KT, MUGAL T & HAQ IU. 2010. Moringa oleifera: a natural gift-A review. J Pharm Sci Res 2(11): 775-781.).

Moringa leaves contain important bioactive compounds, including vitamins, carotenoids, phenolics, flavonoids, glucosinolates, isothiocyanates, tannins, and saponins. Thereby it is commonly known for its medicinal power (Hisam et al. 2018HISAM EEA ET AT. 2018. Combined extract of Moringa oleifera and Centella asiatica modulates oxidative stress and senescence in hydrogen peroxide-induced human dermal fibroblasts. Turk J Biol 42(1): 33-44.). Countless benefits are assigned to this plant, such as antioxidant activity, hepatoprotective, anti-inflammatory and antihypertensive properties. It is also associated with hyperglycemia decreasing, showing an antidiabetic effect (Farid & Hegazy 2019FARID AS & HEGAZY AM. 2019. Ameliorative effects of Moringa oleifera leaf extract on levofloxacin-induced hepatic toxicity in rats. Drug Chem Toxicol 43(6): 616-622. https://doi.org/10.1080/01480545.2019.1574811.). Hence, the plant is called “Miraculous Tree” and “Tree of Life” and is also recognized for the beneficial effects on water sanitation (Padayachee & Baijnath 2020PADAYACHEE B & BAIJNATH H. 2020. An updated comprehensive review of the medicinal, phytochemical and pharmacological properties of Moringa oleifera. S Afr J Bot 129: 304-316. https://doi.org/10.1016/j.sajb.2019.08.021.).

Several attributions are given to M. oleifera. However, recently in Brazil ANVISA (National Health Surveillance Agency) banned the manufacturing, import, commercialization, advertising, and distribution of all foods containing Moringa owing to lack of evaluation and proof both of the safety of its use and the therapeutic claims attributed to it (BRAZIL 2019BRAZIL. 2019. Resolução n° 1.478, de 3 de junho de 2019. Diário Oficial da União. Retrieved from https://www.in.gov.br/web/dou/-/resolucao-re-n-1.478-de-3-de-junho-de-2019-152008784.
https://www.in.gov.br/web/dou/-/resoluca...
). Cytotoxicity, moderate organ toxicity, and histopathological changes were observed in studies carried out in vivo and in vitro (Asare et al. 2012ASARE GA, GYAN B, BUGYEI K, ADJEI S, MAHAMA R, ADDO P, OTU-NYARKO L, WIREDU EK & NYARKO A. 2012. Toxicity potentials of the nutraceutical Moringa oleifera at supra-supplementation levels. J Ethnopharmacol 139: 265-272. https://doi.org/10.1016/j.jep.2011.11.009., Kasolo et al. 2012KASOLO JN, BIMENYA GS, OJOK L & OGWAL-OKENG JW. 2012. Sub-acute toxicity evaluation of Moringa oleifera leaves aqueous and ethanol extracts in Swiss Albino rats. Int J Med Plant Res 1(6): 075-081.).

Due to the contradictory data available in the literature, it is necessary to compile results about Moringa incorporation in functional foods and its use as a natural food additive. There is a gap in the literature regarding the potential of Moringa in food biochemistry, associated with its sensory acceptance and safety. Thus, this review aims to describe the Moringa oleifera utilization in food formulation, in addition to its potential to modify the biochemical properties of food products. Therefore, databases such as Google Scholar, Science Direct, and PubMed were used.

CHARACTERIZATION OF Moringa oleifera

Moringa leaves contain high levels of fiber (11.23 g/100g), ash (4.56 g/100g), carbohydrates (56.33 g/100g), total proteins (9.38 g/100g), and lipids (7.76 g/100g). The plant is an excellent source of essential minerals (such as sodium, potassium, magnesium, phosphorus, iron, zinc, copper, calcium, and manganese). 17 amino acids were quantified, both essential and non-essential. The amino acids found in higher levels were leucine and lysine (94.36 and 69.13 mg/100g, respectively). Regarding vitamins, beta-carotene (vitamin A precursor), vitamins E, C, B1, B2, and B3 were identified (El Sohaimy et al. 2015EL SOHAIMY SA, HAMAD GM, MOHAMED SE, AMAR MH & AL-HINDI RR. 2015. Biochemical and functional properties of Moringa oleifera leaves and their potential as a functional food. Global Adv Res J Agric Sci 4(4): 188-199.).

El Sohaimy et al. 2015EL SOHAIMY SA, HAMAD GM, MOHAMED SE, AMAR MH & AL-HINDI RR. 2015. Biochemical and functional properties of Moringa oleifera leaves and their potential as a functional food. Global Adv Res J Agric Sci 4(4): 188-199. and Coz-Bolaños et al. 2018COZ-BOLAÑOS X, CAMPOS-VEGA R, REYNOSO-CAMACHO R, RAMOS-GÓMEZ M, LOARCA-PIÑA GF & GUZMÁN-MALDONADO SH. 2018. Moringa infusion (Moringa oleifera) rich in phenolic compounds and high antioxidant capacity attenuate nitric oxide pro-inflammatory mediator in vitro. Ind Crop Prod 118: 95-101. https://doi.org/10.1016/j.indcrop.2018.03.028. executed extractions with different solvents (water, ethanol 70% and methanol 70%) from the previously dried leaves, and the extracts exhibited a high content of total phenolic compounds and, consequently, of antioxidant activity.

Moringa is a multifaceted plant. Most of its parts are edible, and it has therapeutics values. Its seeds, flowers, and fruits (pods) have relevant nutrients and substances for feeding, as characterized by Fernandes et al. 2021FERNANDES Â ET AL. 2021. Nutritional and phytochemical profiles and biological activities of Moringa oleifera Lam. edible parts from Guinea-Bissau (West Africa). Food Chem 341. https://doi.org/10.1016/j.foodchem.2020.128229. (Table I). Because of this, Moringa has been widely used as a supplement against malnutrition. Its leaves are the most used parts and best studied by diverse authors (Table II). They can be dried, ground, and stored for later use (Shiriki et al. 2015SHIRIKI D, IGYOR MA & GERNAH DI. 2015. Nutritional evaluation of complementary food formulations from maize, soybean and peanut fortified with Moringa oleifera leaf powder. Food Nutr Sci 6(5): 494-500. https://doi.org/10.4236/fns.2015.65051.).

Table I
Nutritional value and composition of Moringa oleifera seeds, flowers and fruitsa.
Table II
Nutritional characterization of Moringa oleifera dried leaves.

Many factors can affect the plants’ composition, such as edaphoclimatic and biotic conditions. Techniques used in agronomy can also contribute to the differences in the plant’s nutrients levels (Ziani et al. 2019ZIANI BE, RACHED W, BACHARI K, ALVES MJ, CALHELHA RC, BARROS L & FERREIRA IC. 2019. Detailed chemical composition and functional properties of Ammodaucus leucotrichus Cross. & Dur. and Moringa oleifera Lamarck. J Funct Foods 53: 237-247. https://doi.org/10.1016/j.jff.2018.12.023.). Thus, this can explain why there are variations in the composition of Moringa found in the literature.

ANTIMICROBIAL POTENTIAL AND FOOD PRESERVATION

Aqueous, ethanolic and methanolic Moringa leaves extracts revealed broad antimicrobial potential. These extracts inhibited the growth of eight pathogenic bacteria and fungi species (Streptococcus pyogenes, Streptococcus agalactiae, Staphylococcus epidermis, Staphylococcus aureus, Salmonella senftenberg, Escherichia coli, Bacillus subtilis, and Candida albicans). This inhibition suggests that pharmaceutical and food industries can use Moringa leaves extracts as a natural antimicrobial (El Sohaimy et al. 2015EL SOHAIMY SA, HAMAD GM, MOHAMED SE, AMAR MH & AL-HINDI RR. 2015. Biochemical and functional properties of Moringa oleifera leaves and their potential as a functional food. Global Adv Res J Agric Sci 4(4): 188-199.).

Moringa leaves and seeds have been reported to contain antibacterial properties, acting against Gram-positive and Gram-negative bacteria (Saadabi & Zaid 2011SAADABI AM & ZAID IA. 2011. An in vitro antimicrobial activity of Moringa oleifera L. seed extracts against different groups of microorganisms. Aust J Basic Appl Sci 5(5): 129-134., Rahman et al. 2009RAHMAN MM, SHEIKH MMI, SHARMIN SA, ISLAM MS, RAHMAN MA, RAHMAN MM & ALAM MF. 2009. Antibacterial activity of leaf juice and extracts of Moringa oleifera Lam. against some human pathogenic bacteria. J Nat Sci 8(2): 219-227.). The plant leaves contain pterigospermin, a compound that easily dissociates into two benzyl-isothiocyanate molecules, which has antibacterial and antifungal effects (Jayawardana et al. 2015JAYAWARDANA BC, LIYANAGE R, LALANTHA N, IDDAMALGODA S & WETHTHASINGHE P. 2015. Antioxidant and antimicrobial activity of drumstick (Moringa oleifera) leaves in herbal chicken sausages. Lwt - Food Sci Technol 64(2): 1204-1208. https://doi.org/10.1016/j.lwt.2015.07.028.). The presence of many phytochemicals in Moringa seeds can explain its antimicrobial activity, but, as well as in the leaves, benzyl-isothiocyanate is remarkable. This compound can act directly on microorganisms, interrupting the cell membrane synthesis or inhibiting essential enzyme synthesis, disrupting microorganisms’ growth (Bukar et al. 2010BUKAR A, UBA A & OYEYI T. 2010. Antimicrobial profile of Moringa oleifera Lam. extracts against some food–borne microorganisms. Bayero J Pure Appl Sci 3: 43-48. https://doi.org/10.4314/bajopas.v3i1.58706.).

Different Moringa leaves extracts showed activity against bacteria ranging from pathogenic to toxinogenic, such as E. coli, S. aureus, and P. aeruginosa, responsible for causing food deterioration and possibly causing foodborne diseases (Salem et al. 2015SALEM AS, SALAMA WM & RAGAB WA. 2015. Prolonged shelf life of sour cream by adding Moringa oleifera Leaves Extract (MOLE) or Moringa oleifera Oil (MOO). Am J Food Technol 10: 58-67. https://doi.org/10.3923/ajft.2015.58.67.). However, the work conducted by Bukar et al. 2010BUKAR A, UBA A & OYEYI T. 2010. Antimicrobial profile of Moringa oleifera Lam. extracts against some food–borne microorganisms. Bayero J Pure Appl Sci 3: 43-48. https://doi.org/10.4314/bajopas.v3i1.58706. indicated that Pseudomonas aeruginosa, a resistant bacteria that defy researches in the food area, was sensitive only to the ethanolic extract of Moringa leaves at 200 mg/mL, demonstrating that Moringa extracts may have uses limitations in food products.

Moringa leaves and seeds extracts, obtained through percolation with the solvents ethanol and chloroform (1:10 w/v), showed sanitizers and preservatives properties. These extracts contain substances that act as antimicrobial agents against bacteria and fungi that are frequently associated with food spoilage and food contamination (Bukar et al. 2010BUKAR A, UBA A & OYEYI T. 2010. Antimicrobial profile of Moringa oleifera Lam. extracts against some food–borne microorganisms. Bayero J Pure Appl Sci 3: 43-48. https://doi.org/10.4314/bajopas.v3i1.58706.). The extracts analyzed can be potential substitutes for artificial preservatives, satisfying the emerging consumers’ interest, who have shown a change in nutritional habits with a preference for natural additives (Carocho et al. 2014CAROCHO M, BARREIRO MF, MORALES P & FERREIRA IC. 2014. Adding molecules to food, pros and cons: A review on synthetic and natural food additives. Compr Rev Food Sci F 13(4): 377-399. https://doi.org/10.1111/1541-4337.12065.).

One product that can be challenging for the food market is raw sugarcane juice, as it deteriorates shortly after extraction. To extend the validity of the product, manufacturers often use chemical preservatives. To offer other alternatives for this problem, Ramachandran et al. 2017RAMACHANDRAN C, SUDHA RANI R, LAVANYA K, NIVETHA S & USHA A. 2017. Optimization of shelf stability of sugarcane juice with natural preservatives. J Food Process Pres 41(1). https://doi.org/10.1111/jfpp.12868. studied the effectiveness of combining different natural preservatives (Moringa leaf and seed extract, lemon, and ginger) at low temperature (2.0 °C). The authors found that the combination of Moringa seed extract and lemon at 10% v/v promoted a satisfactory antimicrobial effect, with a minimum inhibitory concentration (MIC) of 25 µL/mL against 15 bacterial strains. This combination promoted the highest acceptance among all samples, and was more effective against bacterial growth than sodium benzoate (0.1%) and sodium metabisulfite (0.5%), chemical preservatives used as standard at its maximum allowed concentration.

To gather information on the Moringa application as a natural food additive in livestock products, Singh et al. 2015SINGH TP, SINGH P & KUMAR P. 2015. Drumstick (Moringa Oleifera) as a food additive in livestock products. Nutr Food Sci 45(3): 423-432. https://doi.org/10.1108/NFS-02-2015-0018. described works carried out with the plant in a review article. The authors indicated that the dietary supplementation of goats, pigs, and broiler birds with Moringa leaves improves attributes such as meat color, odor, and lipid profile. It also improves the chemical composition and oxidative stability, without causing adverse effects on carcass characteristics (Singh et al. 2015SINGH TP, SINGH P & KUMAR P. 2015. Drumstick (Moringa Oleifera) as a food additive in livestock products. Nutr Food Sci 45(3): 423-432. https://doi.org/10.1108/NFS-02-2015-0018.).

The same work describes that Moringa leaf powder applied in meat products improved safety during the storage, reducing microbial counts. It also improved its nutritional value, ameliorated its physicochemical, sensory quality, and microbiological characteristics, and reduced the production cost (Singh et al. 2015SINGH TP, SINGH P & KUMAR P. 2015. Drumstick (Moringa Oleifera) as a food additive in livestock products. Nutr Food Sci 45(3): 423-432. https://doi.org/10.1108/NFS-02-2015-0018.). The crude aqueous extract from Moringa leaves raised softness and juiciness in buffalo ground meat, suggesting that it can execute a proteolytic activity, as indicated by Shi et al. (2019)SHI Y, PRABAKUSUMA AS, ZHAO Q, WANG X & HUANG A. 2019. Proteomic analysis of Moringa oleifera Lam. leaf extract provides insights into milk-clotting proteases. Lwt - Food Sci Technol 109: 289-295. https://doi.org/10.1016/j.lwt.2019.04.035.. Aqueous extract can also prevent TBARS increase during storage, being more effective than the synthetic additive BHT (butylated hydroxytoluene, E321).

To improve the quality and prolong the shelf life of sour cream, Salem et al. 2015SALEM AS, SALAMA WM & RAGAB WA. 2015. Prolonged shelf life of sour cream by adding Moringa oleifera Leaves Extract (MOLE) or Moringa oleifera Oil (MOO). Am J Food Technol 10: 58-67. https://doi.org/10.3923/ajft.2015.58.67. evaluated the addition of aqueous leaf extract and Moringa oil to the product. The results showed that both the addition of the oil and the Moringa leaves extract did not modify the samples’ composition. Furthermore, the oil and extract did not lead to a standard of identity problems of the sour cream. All the products containing extract or Moringa oil resulted in good sensory evaluation, with an acceptable taste, texture, and appearance throughout the storage period. Changes in pH were observed in all treated samples during storage. Lipolytic and proteolytic bacteria, yeasts, and molds were present in the control samples after 15 days of storage, but not in the products fortified. Therefore the authors concluded that the aqueous Moringa leaves extract and Moringa oil can be added to the sour cream, lengthening its stability and, thus, extending its shelf life (Salem et al. 2015SALEM AS, SALAMA WM & RAGAB WA. 2015. Prolonged shelf life of sour cream by adding Moringa oleifera Leaves Extract (MOLE) or Moringa oleifera Oil (MOO). Am J Food Technol 10: 58-67. https://doi.org/10.3923/ajft.2015.58.67.).

Table III contains a summary of the use of Moringa in food products made by different authors and the benefits provided by the plant.

Table III
Summary of the benefits promoted by the incorporation of Moringa oleifera in different food products.

FOOD PRODUCTS INCORPORATED WITH Moringa oleifera AND ITS SENSORY ATTRIBUTES

Cardines et al. 2018CARDINES PH, BAPTISTA AT, GOMES RG, BERGAMASCO R & VIEIRA AM. 2018. Moringa oleifera seed extracts as promising natural thickening agents for food industry: Study of the thickening action in yogurt production. Lwt - Food Sci Technol 97: 39-44. https://doi.org/10.1016/j.lwt.2018.06.028. evaluated the Moringa seed extracts thickening action in yogurt formulations. The authors obtained the extracts by saline extractions, followed by ultrafiltration, and added it at 1.5% (v/v) in yogurt fermented by probiotic lactic culture. The seed extracts promoted thickening and improved the product’s characteristics by increasing the protein content, reducing syneresis values, and forming a more cohesive casein net.

Nadeem and Imran 2016 reported favorable characteristics of the oil extracted from Moringa seeds. The authors signalized that the plant seeds have 35 to 40% oil content, with a light yellow color and pleasant nutty flavor. For these sensory characteristics, besides low peroxides levels, different areas can use Moringa oil without needing to pre-process it (refining, bleaching, and deodorization), being suitable for both food and non-food applications, such as the production of biodiesel and cosmetics formulations.

Moringa seed oil has high oxidative stability, is resistant to auto-oxidation, and can be used to stabilize other edible oils, acting as an antioxidant and preventing their deterioration after a storage time. The addition of Moringa oil in sunflower, canola, and soybean oil promoted a lower concentration of primary and secondary oxidation products throughout the storage period (Nadeem & Imran 2016NADEEM M & IMRAN M. 2016. Promising features of Moringa oleifera oil: recent updates and perspectives. Lipids Health Dis 15(1): 1-8.). Oleic acid is the principal fatty acid in Moringa oil (75 - 77% of fatty acids). This high content may raise HDL cholesterol and reduce serum cholesterol and triglyceride levels. Therefore, Moringa seed oil can be considered a functional food (Nadeem & Imran 2016NADEEM M & IMRAN M. 2016. Promising features of Moringa oleifera oil: recent updates and perspectives. Lipids Health Dis 15(1): 1-8.).

Nadeem et al. 2013NADEEM M, ABDULLAH M, HUSSAIN I, INAYAT S, JAVID A & ZAHOOR Y. 2013. Antioxidant potential of Moringa oleifera leaf extract for the stabilisation of butter at refrigeration temperature. Czech J Food Sci 31(4): 332-339. https://doi.org/10.17221/366/2012-CJFS. studied the effects of ethanolic leaves extract of Moringa on the stabilization of butter. The extract addition in all concentrations evaluated did not cause negative changes in the final composition of the product. The incorporating at 600 and 800 ppm efficiently inhibited the oxidative process and also promoted a decrease in the free fatty acids formation after 90 days of storage under refrigeration. However, the highest concentration (800 ppm) caused a negative sensory acceptance of the product, with a significant change in the product’s organoleptic properties. Residual flavor and aroma of phenolic compounds, known to have an astringent taste, were observed (Nadeem et al. 2013NADEEM M, ABDULLAH M, HUSSAIN I, INAYAT S, JAVID A & ZAHOOR Y. 2013. Antioxidant potential of Moringa oleifera leaf extract for the stabilisation of butter at refrigeration temperature. Czech J Food Sci 31(4): 332-339. https://doi.org/10.17221/366/2012-CJFS., Angelo & Jorge 2007ANGELO PM & JORGE N. 2007. Compostos fenólicos em alimentos - uma breve revisão. Rev Insti Adolfo Lutz 66: 01-09.).

To verify the addition of interesterified Moringa oil effects on the physicochemical characteristics and oxidative stability in ice cream, Nadeem et al. 2016NADEEM M, ULLAH R & ULLAH A. 2016. Improvement of the physical and oxidative stability characteristics of ice cream through interesterified Moringa oleifera oil. Pak J Scienti Ind Res Ser B: Biol Sci 59(1): 38-43. substituted the milk fat with Moringa oil at three levels (10, 20, and 30%). The authors concluded that no significant changes in pH, fat content, protein, mineral content, and total solids occurred, comparing the control sample (without the oil addition). There were no differences in the ice cream viscosity or in melting time. This result diverges from other studies that replaced milk fat with vegetable oils, which caused a decrease in the melting time. This effect is due to the interesterification process of Moringa oil that promotes an increase in its temperature melting point, going from 18.0 to 35.6°C (Nadeem et al. 2016NADEEM M, ULLAH R & ULLAH A. 2016. Improvement of the physical and oxidative stability characteristics of ice cream through interesterified Moringa oleifera oil. Pak J Scienti Ind Res Ser B: Biol Sci 59(1): 38-43.).

Interesterified Moringa oil, at all levels used, increased the oleic acid level and the storage stability. The supplemented ice cream samples became less susceptible to the formation of oxidation products. There was a reduction in the loss rate of oleic and linoleic acids. The supplementation also decreased peroxide and p-anisidine values. However, it was not effective in interrupting the formation of free fatty acids during three months of storage (Nadeem et al. 2016NADEEM M, ULLAH R & ULLAH A. 2016. Improvement of the physical and oxidative stability characteristics of ice cream through interesterified Moringa oleifera oil. Pak J Scienti Ind Res Ser B: Biol Sci 59(1): 38-43.).

Mouminah 2015MOUMINAH HH. 2015. Effect of dried Moringa oleifera leaves on the nutritional and organoleptic characteristics of cookies. Alex Sci Exch J 36(4): 297-302. https://doi.org/10.21608/asejaiqjsae.2015.2934. formulated cookies using blends of wheat flour and Moringa dried leaves (95:5, 90:10, and 85:15 w/w). The addition of Moringa in the formulation increased total ash, protein, fibers, iron, calcium, and magnesium levels. Although the fat content of the formulations with the plant showed a slight increase, the addition of nutrients and beneficial health compounds in a dose-dependent manner indicates that the use of Moringa as an ingredient provides a better nutritional profile to the food. Samples containing 5.0% of leaves did not show a sensory difference compared to the control sample, whereas samples containing 10 and 15% had a acceptability decreasing (Mouminah 2015MOUMINAH HH. 2015. Effect of dried Moringa oleifera leaves on the nutritional and organoleptic characteristics of cookies. Alex Sci Exch J 36(4): 297-302. https://doi.org/10.21608/asejaiqjsae.2015.2934.).

A summary of positive and negative biochemical changes in foods supplemented with Moringa is available in Table IV.

Table IV
Biochemical aspects in foods fortified with Moringa oleifera.

NUTRITION AND FUNCTIONAL BENEFITS

One of the most studied and published aspects involving the applicability of Moringa in food is its nutritional benefits, especially in populations with a diet low in essential nutrients. Thus, this plant has been used for formulations of supplements against malnutrition and as an additive or fortifier of the most varied foods (Leone et al. 2018LEONE A, BERTOLI S, DI LELLO S, BASSOLI A, RAVASENGHI S, BORGONOVO G, FORLANI F & BATTEZZATI A. 2018. Effect of Moringa oleifera leaf powder on postprandial blood glucose response: In vivo study on Saharawi people living in refugee camps. Nutrients 10(10): 1-14. https://doi.org/10.3390/nu10101494.).

The use of dried and powdered Moringa leaves is relatively common to fortify dairy drinks, increasing the drink’s nutritional benefits. Singh et al. 2015SINGH TP, SINGH P & KUMAR P. 2015. Drumstick (Moringa Oleifera) as a food additive in livestock products. Nutr Food Sci 45(3): 423-432. https://doi.org/10.1108/NFS-02-2015-0018. reported in a review article that these milk products incorporated with Moringa presented good sensory acceptance, except for the color. The use of dry leaves in the curd improved nutritional, microbiological, and organoleptic properties. In buttermilk, the leaves demonstrated the potential to increase health benefits and sensory attributes. Moringa seed extract was incorporated into cottage cheese, increasing yield, protein, and mineral content (Singh et al. 2015SINGH TP, SINGH P & KUMAR P. 2015. Drumstick (Moringa Oleifera) as a food additive in livestock products. Nutr Food Sci 45(3): 423-432. https://doi.org/10.1108/NFS-02-2015-0018.).

Madane et al. 2019MADANE P, DAS AK, PATEIRO M, NANDA PK, BANDYOPADHYAY S, JAGTAP P, BARBA FJ, SHEWALKAR A, MAITY B & LORENZO JM. 2019. Drumstick (Moringa oleifera) flower as an antioxidant dietary fibre in chicken meat nuggets. Foods 8(307): 1-19. https://doi.org/10.3390/foods8080307. added Moringa flower extract in chicken nuggets formulation (1.0 and 2.0%) to evaluate its potential as an antioxidant dietary fiber or as a functional ingredient, based on nutritional content, quality, storage stability, and product acceptability. The authors concluded that the extract enhanced dietary fibers level and extended the product shelf life by increasing its lipid stability. Furthermore, it acted as an antioxidant and did not affect the product acceptability (Madane et al. 2019MADANE P, DAS AK, PATEIRO M, NANDA PK, BANDYOPADHYAY S, JAGTAP P, BARBA FJ, SHEWALKAR A, MAITY B & LORENZO JM. 2019. Drumstick (Moringa oleifera) flower as an antioxidant dietary fibre in chicken meat nuggets. Foods 8(307): 1-19. https://doi.org/10.3390/foods8080307.).

Hekmat et al. 2015HEKMAT S, MORGAN K, SOLTANI M & GOUGH R. 2015. Sensory evaluation of locally-grown fruit purees and inulin fibre on probiotic yogurt in Mwanza, Tanzania and the microbial analysis of probiotic yogurt fortified with Moringa oleifera. J Health Popul Nutr 33(1): 60-67. elaborated probiotic yogurts with Moringa leaves in different proportions. The work indicated that, although studies show that the seeds of the plant have an antibacterial effect, the use of Moringa as a functional ingredient did not inhibit the growth of bacteria present in yogurt, except for the formulation with higher doses of the plant and without sugar. That suggests that the Moringa addition in yogurt formulation can stimulate bacteria growth, and may have prebiotic properties. Moringa leaves at 0.5% enhanced the product’s nutritional value, but did not increase the vitamin A levels in the yogurt (Hekmat et al. 2015HEKMAT S, MORGAN K, SOLTANI M & GOUGH R. 2015. Sensory evaluation of locally-grown fruit purees and inulin fibre on probiotic yogurt in Mwanza, Tanzania and the microbial analysis of probiotic yogurt fortified with Moringa oleifera. J Health Popul Nutr 33(1): 60-67.).

Shiriki et al. 2015SHIRIKI D, IGYOR MA & GERNAH DI. 2015. Nutritional evaluation of complementary food formulations from maize, soybean and peanut fortified with Moringa oleifera leaf powder. Food Nutr Sci 6(5): 494-500. https://doi.org/10.4236/fns.2015.65051. blended maize, soybean, and peanuts in a ratio of 60:30:10, based on the protein content to provide 16 g of protein for each 100 g of food, content recommended for infant diets. The authors divided the mixture into four samples, one part used as control (without leaves addition) and three parts fortified with 5, 10, and 15% Moringa leaves powder. Protein, fiber, and ash levels increased considerably with the product’s fortification (from 16.04% to 17.59%, 2.25% to 4.42%, and 1.40% to 2.50%, respectively). Contrarily, fat and carbohydrate decreased, with a consequent decrease in energy value. Protein efficiency ratio (PER) and net protein ratio (NPR) improved significantly with fortification up to 10%, indicating an increase in protein quality, even though all samples had lower PER values ​​than recommended by the Protein Advisory Group. However, 15% fortification decreased PER and NPR values. At this level, a bitter taste is noticeable and, therefore, the animals’ consumption was lower. The feed conversion efficiency (FCE) and apparent digestibility (AD) had a similar tendency to PER and NPR, as the proportion of Moringa leaf powder increased. The augment of PER, NPR, FCE, and AD values ​​of the fortified products may be a consequence of the content of proteins and micronutrients increased that the Moringa powder provided (Shiriki et al. 2015SHIRIKI D, IGYOR MA & GERNAH DI. 2015. Nutritional evaluation of complementary food formulations from maize, soybean and peanut fortified with Moringa oleifera leaf powder. Food Nutr Sci 6(5): 494-500. https://doi.org/10.4236/fns.2015.65051.).

To determine the consequences of Moringa leaves addition in snacks, Zungu et al. 2020ZUNGU N, VAN ONSELEN A, KOLANISI U & SIWELA M. 2020. Assessing the nutritional composition and consumer acceptability of Moringa oleifera leaf powder (MOLP)-based snacks for improving food and nutrition security of children. S Afr J Bot 129: 283-290. https://doi.org/10.1016/j.sajb.2019.07.048. substituted a flour blend (50% wheat flour and 50% cornflour) for 0% (control), 1, 3, and 5% (w/w) of powdered Moringa leaves and evaluated the products’ color, texture, nutritional components, and acceptability. They verified that the snack color was affected as the Moringa leaves increased, changing from light brown (control) to dark green with brown traces, which can be due to the chlorophyll present in the plant leaf. The leave addition at higher levels caused a reduction in the snacks’ breaking force, making them more crumbly (Zungu et al. 2020ZUNGU N, VAN ONSELEN A, KOLANISI U & SIWELA M. 2020. Assessing the nutritional composition and consumer acceptability of Moringa oleifera leaf powder (MOLP)-based snacks for improving food and nutrition security of children. S Afr J Bot 129: 283-290. https://doi.org/10.1016/j.sajb.2019.07.048.). Formulation at 1% of Moringa leaves was the only well accepted by the public. At this level, the Moringa leaves promoted an increase in mineral content and higher calcium, magnesium, potassium, and iron levels were observed. The fortified snacks can be a possibility to improve the food and nutrition of children from communities with low economic levels and malnutrition (Zungu et al. 2020ZUNGU N, VAN ONSELEN A, KOLANISI U & SIWELA M. 2020. Assessing the nutritional composition and consumer acceptability of Moringa oleifera leaf powder (MOLP)-based snacks for improving food and nutrition security of children. S Afr J Bot 129: 283-290. https://doi.org/10.1016/j.sajb.2019.07.048.).

In the same intention of formulating snacks to counter malnutrition, Lopez & Bhaktikul 2018LOPEZ JCC & BHAKTIKUL K. 2018. Bromatological and sensory analyses of a snack based corn flour and cassava root fortified with moringa to combat the malnutrition. Bangl J Bot 47(3): 487-493. https://doi.org/10.3329/bjb.v47i3.38716. defined a formulation containing maize flour, cassava root, and Moringa leaves at 1%, which resulted in good acceptability. The authors observed positive results in the protein, moisture, and ash content (Lopez & Bhaktikul 2018LOPEZ JCC & BHAKTIKUL K. 2018. Bromatological and sensory analyses of a snack based corn flour and cassava root fortified with moringa to combat the malnutrition. Bangl J Bot 47(3): 487-493. https://doi.org/10.3329/bjb.v47i3.38716.).

Rocchetti et al. 2020ROCCHETTI G, RIZZI C, PASINI G, LUCINI L, GIUBERTI G & SIMONATO B. 2020. Effect of Moringa oleifera L. leaf powder addition on the phenolic bioaccessibility and on in vitro starch digestibility of durum wheat fresh pasta. Foods 9(5): 628. https://doi.org/10.3390/foods9050628. replaced durum wheat with powdered Moringa leaves at 5, 10, and 15 g/100g (w/w) for fresh pasta formulation. The authors investigated the bioaccessibility of phenolic compounds and starch digestibility and concluded that the fortified pasta had 152 phenolic compounds, with the highest content in the formulation containing 15% of leaves. Low molecular weight phenolic compounds were the most abundant, identified as equivalents of tyrosol, flavonoids, and phenolic acids (Rocchetti et al. 2020ROCCHETTI G, RIZZI C, PASINI G, LUCINI L, GIUBERTI G & SIMONATO B. 2020. Effect of Moringa oleifera L. leaf powder addition on the phenolic bioaccessibility and on in vitro starch digestibility of durum wheat fresh pasta. Foods 9(5): 628. https://doi.org/10.3390/foods9050628.). The replacement of durum wheat by Moringa promoted a decrease in the rapidly digestible starch, which causes a fast elevation of blood glucose levels. Also, it increased the slowly digestible starch levels, which provides prolonged glucose release (Rocchetti et al. 2020ROCCHETTI G, RIZZI C, PASINI G, LUCINI L, GIUBERTI G & SIMONATO B. 2020. Effect of Moringa oleifera L. leaf powder addition on the phenolic bioaccessibility and on in vitro starch digestibility of durum wheat fresh pasta. Foods 9(5): 628. https://doi.org/10.3390/foods9050628.). In contrast, the resistant starch levels, considered as a prebiotic food, decreased as there was an increase in Moringa levels in the formulation (Rocchetti et al. 2020ROCCHETTI G, RIZZI C, PASINI G, LUCINI L, GIUBERTI G & SIMONATO B. 2020. Effect of Moringa oleifera L. leaf powder addition on the phenolic bioaccessibility and on in vitro starch digestibility of durum wheat fresh pasta. Foods 9(5): 628. https://doi.org/10.3390/foods9050628., Pereira 2007PEREIRA KD. 2007. Resistant starch, the latest generation of energy control and healthy digestion. Food Sci Technol 27: 88-92. http://dx.doi.org/10.1590/S0101-20612007000500016.).

When added to food products, Moringa promotes many beneficial effects. In the literature, several studies report these improvements. Despite the advantages associated with the plant, there are limitations in its applicability, generally associated with the negative sensory characteristics promoted to the fortified products. Boateng et al. 2018BOATENG L, NORTEY E, OHEMENG AN, ASANTE M & STEINER-ASIEDU M. 2018. Sensory attributes and acceptability of complementary foods fortified with Moringa oleifera leaf powder. Nutr Food Sci 49(3): 393-406. https://doi.org/10.1108/NFS-07-2018-0192. described in a review article some studies that observed certain disadvantages concerning the organoleptic properties of foods fortified with Moringa leaves powder. Unwanted descriptions of sensory attributes have been reported, emphasizing the taste and color. Herbaceous and bitter flavor increases as the Moringa content is high. A study demonstrated that the minimum percentage of powdered Moringa leaves for significant improvements in nutritional value is 10%, the same level in which acceptability becomes lower. Another relevant aspect is that the plant leaf powder is not satisfactory to replace wheat flour in the formulation of bread once it may cause undesirable changes in its characteristics (Boateng et al. 2018BOATENG L, NORTEY E, OHEMENG AN, ASANTE M & STEINER-ASIEDU M. 2018. Sensory attributes and acceptability of complementary foods fortified with Moringa oleifera leaf powder. Nutr Food Sci 49(3): 393-406. https://doi.org/10.1108/NFS-07-2018-0192.).

Since Moringa can cause unwanted sensory changes to the fortified products, more studies are necessary to determine the appropriate level of the plant addition. This level needs to promote beneficial effects, maintaining product acceptability. Besides, new studies on the toxicity and safety of using Moringa need to be carried out (Boateng et al. 2018BOATENG L, NORTEY E, OHEMENG AN, ASANTE M & STEINER-ASIEDU M. 2018. Sensory attributes and acceptability of complementary foods fortified with Moringa oleifera leaf powder. Nutr Food Sci 49(3): 393-406. https://doi.org/10.1108/NFS-07-2018-0192.).

A possible alternative to improve biochemical, functional, and nutritional aspects without causing a negative sensory change is the microencapsulation of Moringa extracts. Microencapsulation is a technique typically used to promote protection and resistance to bioactive compounds (Zorzenon et al. 2020ZORZENON MRT ET AL. 2020. Spray drying encapsulation of stevia extract with maltodextrin and evaluation of the physicochemical and functional properties of produced powders. J Food Sci 85(10): 3590-3600. https://doi.org/10.1111/1750-3841.15437.). Thammarat & Airouyuwa 2020THAMMARAT K & AIROUYUWA JO. 2020. Storage stability, gastrointestinal release and sensory properties of cookies incorporated with protein-based Moringa oleifera leaf extract microcapsule. Chiang Mai Univ J Nat Sci 19(1): 139-154. https://doi.org/10.12982/CMUJNS.2020.0009. microencapsulated the Moringa leaf extract by the spray drying method, using pea protein isolate and isolated soy protein as encapsulating agents, with a ratio of encapsulated material to wall material in 1:4 w/w.

A summary of Moringa supplementation effects on food products is available in Table V.

Table V
Summary of nutritional and functional aspects promoted by the addition of Moringa oleifera in food products.

TOXICITY AND FOOD SAFETY

There is a lack of researches about the safety of Moringa and its possible adverse reactions. Since it is a plant, there may be an idea that the higher the dose consumed, the greater the benefits.

Thus, Asare et al. 2012ASARE GA, GYAN B, BUGYEI K, ADJEI S, MAHAMA R, ADDO P, OTU-NYARKO L, WIREDU EK & NYARKO A. 2012. Toxicity potentials of the nutraceutical Moringa oleifera at supra-supplementation levels. J Ethnopharmacol 139: 265-272. https://doi.org/10.1016/j.jep.2011.11.009. carried out a study to identify possible acute toxicity with the supra-supplementation of aqueous Moringa leaves extract. The authors used human peripheral blood mononuclear cells and ministered gradual doses of extract to induce cytotoxicity. Acute toxicity was verified using two groups of mice, one receiving low doses (1000 mg/Kg body weight) while the other received high doses (3000 mg/Kg body weight). The authors determined that extract levels at 20 mg/mL presented cytotoxicity. They discarded the occurrence of toxicological syndromes since the animals showed no differences in behavior, and there was no mortality. The animals that received a supra-supplementation at the highest level (3000 mg/Kg) did not have hepatorenal toxicity. Furthermore, the hematological results were within normality (Asare et al. 2012ASARE GA, GYAN B, BUGYEI K, ADJEI S, MAHAMA R, ADDO P, OTU-NYARKO L, WIREDU EK & NYARKO A. 2012. Toxicity potentials of the nutraceutical Moringa oleifera at supra-supplementation levels. J Ethnopharmacol 139: 265-272. https://doi.org/10.1016/j.jep.2011.11.009.).

The administration of aqueous Moringa extract, at both doses, reduced the levels of serum chloride. There was a reduction in sodium at the highest dose, suggesting that Moringa can reduce the aldosterone effects in the reabsorption of sodium from the renal tubules. Therefore, the plant has hypotensive and diuretic properties. The increase in blood urea observed was not considered pathological since no change in the serum creatinine level (renal dysfunction marker) occurred, suggesting a physiological response to the high levels of nitrogen compounds, especially proteins, provided by the plant. Serum albumin levels decreased, indicating the presence of toxic substances in the animals’ bodies, such as isothiocyanate and glycoside cyanides. The dose of 3000 mg/Kg was genotoxic, but the exact level for its beginning has not been determined yet (Asare et al. 2012ASARE GA, GYAN B, BUGYEI K, ADJEI S, MAHAMA R, ADDO P, OTU-NYARKO L, WIREDU EK & NYARKO A. 2012. Toxicity potentials of the nutraceutical Moringa oleifera at supra-supplementation levels. J Ethnopharmacol 139: 265-272. https://doi.org/10.1016/j.jep.2011.11.009.). Figure 1 contains a schematic representation of the results discussed.

Figure 1
Schematic representation of data referring to the study carried out by Asare et al. 2012ASARE GA, GYAN B, BUGYEI K, ADJEI S, MAHAMA R, ADDO P, OTU-NYARKO L, WIREDU EK & NYARKO A. 2012. Toxicity potentials of the nutraceutical Moringa oleifera at supra-supplementation levels. J Ethnopharmacol 139: 265-272. https://doi.org/10.1016/j.jep.2011.11.009. on the toxicity of the aqueous Moringa oleifera leaves extract.

To verify liver, renal and cardiac toxicity, along with histopathological changes in liver, kidney, and heart, Kasolo et al. 2012KASOLO JN, BIMENYA GS, OJOK L & OGWAL-OKENG JW. 2012. Sub-acute toxicity evaluation of Moringa oleifera leaves aqueous and ethanol extracts in Swiss Albino rats. Int J Med Plant Res 1(6): 075-081. evaluated the sub-acute toxicity of aqueous and ethanolic Moringa leaves extracts. The authors provided different single daily doses of extracts to albino Swiss rats for 30 days. Four groups received the aqueous extract, and four other groups received the ethanolic one. The authors calculated the doses based on the median lethal dose (LD50).

The rats that received aqueous extract showed less weight gain, suggesting a reduction in the animals’ consumption of food or less body fat deposition. Moringa leaves may cause hypocholesterolemia (in vitro study). Therefore, its aqueous extract can be used in herbal medicines for weight loss (Kasolo et al. 2012KASOLO JN, BIMENYA GS, OJOK L & OGWAL-OKENG JW. 2012. Sub-acute toxicity evaluation of Moringa oleifera leaves aqueous and ethanol extracts in Swiss Albino rats. Int J Med Plant Res 1(6): 075-081.).

All groups that received aqueous extract had a significant increase in the mean value of total white blood cells, Cl-, K+, and Ca2+. This result is contrary to the work described by Asare et al. 2012ASARE GA, GYAN B, BUGYEI K, ADJEI S, MAHAMA R, ADDO P, OTU-NYARKO L, WIREDU EK & NYARKO A. 2012. Toxicity potentials of the nutraceutical Moringa oleifera at supra-supplementation levels. J Ethnopharmacol 139: 265-272. https://doi.org/10.1016/j.jep.2011.11.009., where there was a decrease in serum chloride and sodium levels in rats treated with aqueous Moringa extract. Kasolo et al. 2012KASOLO JN, BIMENYA GS, OJOK L & OGWAL-OKENG JW. 2012. Sub-acute toxicity evaluation of Moringa oleifera leaves aqueous and ethanol extracts in Swiss Albino rats. Int J Med Plant Res 1(6): 075-081. identified higher levels of alkaline phosphatase (ALP), alanine aminotransferase (ALT), aspartate aminotransferase (AST), and serum bilirubin in the rats that received the aqueous extract. These increases indicate damage to the liver and the biliary system. The serum alkaline phosphate increase, in particular, is associated with the incidence of cholestasis, which is also a confirmation by the total bilirubin increase in rats. Despite the bilirubin increase, the rats did not show visible jaundice, suggesting that most bilirubin was not conjugated. Kasolo et al. 2012KASOLO JN, BIMENYA GS, OJOK L & OGWAL-OKENG JW. 2012. Sub-acute toxicity evaluation of Moringa oleifera leaves aqueous and ethanol extracts in Swiss Albino rats. Int J Med Plant Res 1(6): 075-081. found no differences in serum urea and creatinine in all groups, another disagreement with Asare et al. 2012ASARE GA, GYAN B, BUGYEI K, ADJEI S, MAHAMA R, ADDO P, OTU-NYARKO L, WIREDU EK & NYARKO A. 2012. Toxicity potentials of the nutraceutical Moringa oleifera at supra-supplementation levels. J Ethnopharmacol 139: 265-272. https://doi.org/10.1016/j.jep.2011.11.009..

Most histopathological changes occurred in the animals that received doses equivalent to LD50. Aqueous extract single daily doses, according to LD50, are associated with moderate hepatic necrosis, glomerulonephritis, tubulointerstitial nephritis, and chronic myocarditis. Hence, aqueous Moringa extract is related to moderate organ toxicity. The ethanolic Moringa extract did not show any toxicity characteristics.

A schematic representation of the results is available in Figure 2.

Figure 2
Schematic representation of data referring to the study carried out by Kasolo et al. 2012KASOLO JN, BIMENYA GS, OJOK L & OGWAL-OKENG JW. 2012. Sub-acute toxicity evaluation of Moringa oleifera leaves aqueous and ethanol extracts in Swiss Albino rats. Int J Med Plant Res 1(6): 075-081. on the toxicity of the aqueous and ethanol Moringa oleifera leaves extracts.

Studies on evaluations of possible toxicities of Moringa are still scarce, and some data found in the literature are controversial. New tests that evaluate its toxicokinetics, acute, subchronic, and chronic toxicity are essential. Moreover, studies about Moringa neurotoxicity, immunotoxicity, and allergenicity are required. This evaluation will help to define clearly the dosage considered safe.

OTHER BENEFITS ASSOCIATED WITH Moringa oleifera CONSUMPTION

Moringa contains several substances associated with functional and medicinal benefits. These compounds can regulate osmotic control, enzymatic and hormonal activities. They can also act in several metabolic pathways. Moringa arouses interest for its application as a functional food or as a nutraceutical, especially its leaves and seeds. Researchers report the plant’s ability to intervene in human diseases, which can bring positive results in the treatment of diabetes, obesity, inflammation, cancer, hypertension, and infections caused by microorganisms (Udechukwu et al. 2018UDECHUKWU MC, ABBEY L, NWODO U & UDENIGWE CC. 2018. Potential of Moringa oleifera seeds and leaves as functional food ingredients for human health promotion. J Food Nutr Res 57(1).).

Despite the interest, Moringa products development focused on health applications has a key impediment: the lack of data and clear evidence of its efficiency and safety, principally concerning chronic diseases. Yet, there is preclinical evidence that can stimulate more rigorous studies. Currently, the therapeutic use of Moringa is carried out in South Asia medicine. Its use is performed widely in the Ayurvedic and Unani medical systems, traditional in India. The plant is a bet for the intervention of diseases based on diet, however, further studies are essential to develop this potential (Udechukwu et al. 2018UDECHUKWU MC, ABBEY L, NWODO U & UDENIGWE CC. 2018. Potential of Moringa oleifera seeds and leaves as functional food ingredients for human health promotion. J Food Nutr Res 57(1)., Kumar et al. 2010KUMAR PS, MISHRA D, GHOSH G & PANDA CS. 2010. Medicinal uses and pharmacological properties of Moringa oleifera. Int J Phytomedicine 2(3): 210-216. https://doi.org/doi:10.5138/ijpm.2010.0975.0185.02031.).

To evaluate the chemical composition of powdered Moringa leaves, their sensory acceptability, their ability to inhibit the enzyme α-amylase in vitro, and their effect on the postprandial glycemic response, Leone et al. 2018LEONE A, BERTOLI S, DI LELLO S, BASSOLI A, RAVASENGHI S, BORGONOVO G, FORLANI F & BATTEZZATI A. 2018. Effect of Moringa oleifera leaf powder on postprandial blood glucose response: In vivo study on Saharawi people living in refugee camps. Nutrients 10(10): 1-14. https://doi.org/10.3390/nu10101494. supplemented meals for volunteers from the refugee camp in southwest Algeria. 20 g of powdered Moringa leaves (corresponding to 8.0% of the meal weight, stipulated based on the literature and informal tests by the authors on sensory acceptability) were added to the meals of 17 diabetic and 10 non-diabetic volunteers. The diabetic individuals were patients with type 2 diabetes for at least one year, without being submitted to insulin therapy, treated only with oral hypoglycemic agents.

The results showed that Moringa leaves reduce the α-amylase activity, a key enzyme in the digestion of carbohydrates in the diet, suggesting a decrease in the postprandial glucose level. It also suggests a reduction in the starch hydrolysis rate mediated by enzyme and glucose absorption by the intestine. Indeed, supplementation with Moringa leaves determined a lower increase in postprandial glycemia in diabetic individuals, who in general had a mean change in the baseline concentration of postprandial glycemia when they consumed the supplemented meal, compared to the meal control, without supplementation. In the case of non-diabetic individuals, there was no effect. Thus, the constant consumption of Moringa leaves can improve glycemic control in diabetics and can be a hypoglycemic herbal medicine (Leone et al. 2018LEONE A, BERTOLI S, DI LELLO S, BASSOLI A, RAVASENGHI S, BORGONOVO G, FORLANI F & BATTEZZATI A. 2018. Effect of Moringa oleifera leaf powder on postprandial blood glucose response: In vivo study on Saharawi people living in refugee camps. Nutrients 10(10): 1-14. https://doi.org/10.3390/nu10101494.).

Regardless of the positive results found by Leone et al. 2018LEONE A, BERTOLI S, DI LELLO S, BASSOLI A, RAVASENGHI S, BORGONOVO G, FORLANI F & BATTEZZATI A. 2018. Effect of Moringa oleifera leaf powder on postprandial blood glucose response: In vivo study on Saharawi people living in refugee camps. Nutrients 10(10): 1-14. https://doi.org/10.3390/nu10101494., there was a low acceptance, especially on the flavor of supplemented meals with Moringa leaves, mainly due to the bitter taste. It is necessary to evaluate the effect of lower doses of supplementation. In addition, studies that assess long-term effects on blood glucose need to be carried out (Leone et al. 2018LEONE A, BERTOLI S, DI LELLO S, BASSOLI A, RAVASENGHI S, BORGONOVO G, FORLANI F & BATTEZZATI A. 2018. Effect of Moringa oleifera leaf powder on postprandial blood glucose response: In vivo study on Saharawi people living in refugee camps. Nutrients 10(10): 1-14. https://doi.org/10.3390/nu10101494.). To better evaluate the hypoglycemic effect and other benefits attributed to the plant, the bioavailability and bioaccessibility of Moringa phytochemicals should be better elucidated (Udechukwu et al. 2018UDECHUKWU MC, ABBEY L, NWODO U & UDENIGWE CC. 2018. Potential of Moringa oleifera seeds and leaves as functional food ingredients for human health promotion. J Food Nutr Res 57(1).). The polyphenolic compounds found in the plant, for example, usually contain sugar molecules, which can prevent their intestinal absorption. In particular, glycosides linked to rhamnose must undergo hydrolysis by the intestinal microbiota and therefore are absorbed with difficulty. Biologically active compounds present in Moringa extracts may be involved in complex interactions, which may hinder their accessibility and availability. An explanation of the bioavailability of plant compounds may assist in determining the right ingestion levels so that the desired physiological effects occur (Udechukwu et al. 2018UDECHUKWU MC, ABBEY L, NWODO U & UDENIGWE CC. 2018. Potential of Moringa oleifera seeds and leaves as functional food ingredients for human health promotion. J Food Nutr Res 57(1).).

CONCLUSIONS

This review showed relevant aspects, not yet described with this approach, of Moringa oleifera use in food products, gathering data on its characterization, antimicrobial, and food preservation potential. This work collected information about food biochemistry and chemistry attributes, compiling data on Moringa safety and toxicity. Therefore, this study contributes to the literature and encourages new researches with Moringa. This plant has several properties that can be explored in many potentialities, mainly acting as a natural food additive and food preservative due to its bioactive substances and compounds with antimicrobial and antioxidant activity. The plant has a high potential to be used in functional food formulation, promoting nutritional and health benefits. However, dose-effect and sensory attributes still need a better evaluation. Despite being promising, Moringa use must be analyzed to define a safe dosage since studies are either scarce or inconclusive, and some data are contradictory. Thus, studies to elucidate its toxicology are necessary. Another barrier that deserves attention is its sensory acceptance, which is low, especially when Moringa is incorporated in higher concentrations. Studies point out that attributes such as its color and its particular herbal flavor can be a problem, especially when larger doses of the plant is added to the foods formulations. Even with limitations, the use of Moringa has grown worldwide, and new technological properties of this plant have been discovered, especially in the area of ​​food.

ACKNOWLEDGMENTS

We gratefully acknowledge the support provided by professor Silvio Claudio da Costa and professor Rosângela Bergamasco.

REFERENCES

  • ADEYEMI KD, EL-IMAM AMA, DOSUNMU OO & LAWAL OK. 2013. Effect of Moringa oleifera marinade on microbial stability of smoke-dried African catfish (Clarias gariepinus). Ethiop J Environ Stud Manag 6(1): 104-109. https://doi.org/10.4314/ejesm.v6i1.12.
  • ANGELO PM & JORGE N. 2007. Compostos fenólicos em alimentos - uma breve revisão. Rev Insti Adolfo Lutz 66: 01-09.
  • ASARE GA, GYAN B, BUGYEI K, ADJEI S, MAHAMA R, ADDO P, OTU-NYARKO L, WIREDU EK & NYARKO A. 2012. Toxicity potentials of the nutraceutical Moringa oleifera at supra-supplementation levels. J Ethnopharmacol 139: 265-272. https://doi.org/10.1016/j.jep.2011.11.009.
  • BARAUSKAITE D, GINEIKIENE J, FENNIS BM, AURUSKEVICIENE V, YAMAGUCHI M & KONDO N. 2018. Eating healthy to impress: How conspicuous consumption, perceived self-control motivation, and descriptive normative influence determine functional food choices. Appetite 131: 59-67. https://doi.org/10.1016/j.appet.2018.08.015.
  • BEARTH A, COUSIN ME & SIEGRIST M. 2014. The consumer’s perception of artificial food additives: Influences on acceptance, risk and benefit perceptions. Food Qual Prefer 38: 14-23. https://doi.org/10.1016/j.foodqual.2014.05.008.
  • BOATENG L, NORTEY E, OHEMENG AN, ASANTE M & STEINER-ASIEDU M. 2018. Sensory attributes and acceptability of complementary foods fortified with Moringa oleifera leaf powder. Nutr Food Sci 49(3): 393-406. https://doi.org/10.1108/NFS-07-2018-0192.
  • BRAZIL. 2019. Resolução n° 1.478, de 3 de junho de 2019. Diário Oficial da União. Retrieved from https://www.in.gov.br/web/dou/-/resolucao-re-n-1.478-de-3-de-junho-de-2019-152008784
    » https://www.in.gov.br/web/dou/-/resolucao-re-n-1.478-de-3-de-junho-de-2019-152008784
  • BUKAR A, UBA A & OYEYI T. 2010. Antimicrobial profile of Moringa oleifera Lam. extracts against some food–borne microorganisms. Bayero J Pure Appl Sci 3: 43-48. https://doi.org/10.4314/bajopas.v3i1.58706.
  • CARDINES PH, BAPTISTA AT, GOMES RG, BERGAMASCO R & VIEIRA AM. 2018. Moringa oleifera seed extracts as promising natural thickening agents for food industry: Study of the thickening action in yogurt production. Lwt - Food Sci Technol 97: 39-44. https://doi.org/10.1016/j.lwt.2018.06.028.
  • CAROCHO M, BARREIRO MF, MORALES P & FERREIRA IC. 2014. Adding molecules to food, pros and cons: A review on synthetic and natural food additives. Compr Rev Food Sci F 13(4): 377-399. https://doi.org/10.1111/1541-4337.12065.
  • CONTRERAS-RODRIGUEZ O, MATA F, VERDEJO-ROMÁN J, RAMÍREZ-BERNABÉ R, MORENO D, VILAR-LOPEZ R, SORIANO-MAS C & VERDEJO-GARCÍA A. 2020. Neural-based valuation of functional foods among lean and obese individuals. Nutr Res 78: 27-35. https://doi.org/10.1016/j.nutres.2020.03.006.
  • COZ-BOLAÑOS X, CAMPOS-VEGA R, REYNOSO-CAMACHO R, RAMOS-GÓMEZ M, LOARCA-PIÑA GF & GUZMÁN-MALDONADO SH. 2018. Moringa infusion (Moringa oleifera) rich in phenolic compounds and high antioxidant capacity attenuate nitric oxide pro-inflammatory mediator in vitro. Ind Crop Prod 118: 95-101. https://doi.org/10.1016/j.indcrop.2018.03.028.
  • DAS AK, HAJKUMAR V, VERMA AK & SWARUP D. 2012. Moringa oleiferia leaves extract: a natural antioxidant for retarding lipid peroxidation in cooked goat meat patties. Int J Food Sci Technol 47(3): 585-591. https://doi.org/10.1111/j.1365-2621.2011.02881.x.
  • EL SOHAIMY SA, HAMAD GM, MOHAMED SE, AMAR MH & AL-HINDI RR. 2015. Biochemical and functional properties of Moringa oleifera leaves and their potential as a functional food. Global Adv Res J Agric Sci 4(4): 188-199.
  • FARAG MA ET AL. 2020. Metabolomics reveals impact of seven functional foods on metabolic pathways in a gut microbiota model. J Adv Res 23: 47-59. https://doi.org/10.1016/j.jare.2020.01.001.
  • FARID AS & HEGAZY AM. 2019. Ameliorative effects of Moringa oleifera leaf extract on levofloxacin-induced hepatic toxicity in rats. Drug Chem Toxicol 43(6): 616-622. https://doi.org/10.1080/01480545.2019.1574811.
  • FERNANDES Â ET AL. 2021. Nutritional and phytochemical profiles and biological activities of Moringa oleifera Lam. edible parts from Guinea-Bissau (West Africa). Food Chem 341. https://doi.org/10.1016/j.foodchem.2020.128229.
  • HAZRA S, BISWAS S, BHATTACHARYYA D, DAS SK & KHAN A. 2012. Quality of cooked ground buffalo meat treated with the crude extracts of Moringa oleifera (Lam.) leaves. J Food Sci Technol 49(2): 240-245. https://doi.org/10.1007/s13197-011-0383-3.
  • HEKMAT S, MORGAN K, SOLTANI M & GOUGH R. 2015. Sensory evaluation of locally-grown fruit purees and inulin fibre on probiotic yogurt in Mwanza, Tanzania and the microbial analysis of probiotic yogurt fortified with Moringa oleifera. J Health Popul Nutr 33(1): 60-67.
  • HISAM EEA ET AT. 2018. Combined extract of Moringa oleifera and Centella asiatica modulates oxidative stress and senescence in hydrogen peroxide-induced human dermal fibroblasts. Turk J Biol 42(1): 33-44.
  • JAYAWARDANA BC, LIYANAGE R, LALANTHA N, IDDAMALGODA S & WETHTHASINGHE P. 2015. Antioxidant and antimicrobial activity of drumstick (Moringa oleifera) leaves in herbal chicken sausages. Lwt - Food Sci Technol 64(2): 1204-1208. https://doi.org/10.1016/j.lwt.2015.07.028.
  • KASOLO JN, BIMENYA GS, OJOK L & OGWAL-OKENG JW. 2012. Sub-acute toxicity evaluation of Moringa oleifera leaves aqueous and ethanol extracts in Swiss Albino rats. Int J Med Plant Res 1(6): 075-081.
  • KUMAR PS, MISHRA D, GHOSH G & PANDA CS. 2010. Medicinal uses and pharmacological properties of Moringa oleifera. Int J Phytomedicine 2(3): 210-216. https://doi.org/doi:10.5138/ijpm.2010.0975.0185.02031.
  • LEONE A, BERTOLI S, DI LELLO S, BASSOLI A, RAVASENGHI S, BORGONOVO G, FORLANI F & BATTEZZATI A. 2018. Effect of Moringa oleifera leaf powder on postprandial blood glucose response: In vivo study on Saharawi people living in refugee camps. Nutrients 10(10): 1-14. https://doi.org/10.3390/nu10101494.
  • LEONE A ET AL. 2015. Nutritional characterization and phenolic profiling of Moringa oleifera leaves grown in Chad, Sahrawi Refugee Camps, and Haiti. Int J Mol Sci 16(8): 18923-18937. https://doi.org/10.3390/ijms160818923.
  • LOPEZ JCC & BHAKTIKUL K. 2018. Bromatological and sensory analyses of a snack based corn flour and cassava root fortified with moringa to combat the malnutrition. Bangl J Bot 47(3): 487-493. https://doi.org/10.3329/bjb.v47i3.38716.
  • MADANE P, DAS AK, PATEIRO M, NANDA PK, BANDYOPADHYAY S, JAGTAP P, BARBA FJ, SHEWALKAR A, MAITY B & LORENZO JM. 2019. Drumstick (Moringa oleifera) flower as an antioxidant dietary fibre in chicken meat nuggets. Foods 8(307): 1-19. https://doi.org/10.3390/foods8080307.
  • MAHAMI T, OCLOO FCK, ODONKOR ST, OWULAH C & COFFIE SA. 2012. Preliminary study on the influence of moringa seed extracts supplementation on the yield and quality of cottage cheese. Int J Recent Trends Sci Technol 2(1): 04-08.
  • MAHMOOD KT, MUGAL T & HAQ IU. 2010. Moringa oleifera: a natural gift-A review. J Pharm Sci Res 2(11): 775-781.
  • MOUMINAH HH. 2015. Effect of dried Moringa oleifera leaves on the nutritional and organoleptic characteristics of cookies. Alex Sci Exch J 36(4): 297-302. https://doi.org/10.21608/asejaiqjsae.2015.2934.
  • NADEEM M, ABDULLAH M, HUSSAIN I, INAYAT S, JAVID A & ZAHOOR Y. 2013. Antioxidant potential of Moringa oleifera leaf extract for the stabilisation of butter at refrigeration temperature. Czech J Food Sci 31(4): 332-339. https://doi.org/10.17221/366/2012-CJFS.
  • NADEEM M & IMRAN M. 2016. Promising features of Moringa oleifera oil: recent updates and perspectives. Lipids Health Dis 15(1): 1-8.
  • NADEEM M, JAVID A, ABDULLAH M, ARIF AM & MAHMOO T. 2012. Improving nutritional value of butter milk by blending with dry leaves of Moringa oleifera. Pak J Nutr 11(9): 714-718. https://doi.org/10.3923/pjn.2012.812.816.
  • NADEEM M, ULLAH R & ULLAH A. 2016. Improvement of the physical and oxidative stability characteristics of ice cream through interesterified Moringa oleifera oil. Pak J Scienti Ind Res Ser B: Biol Sci 59(1): 38-43.
  • NAJEEB AP, MANDAL PK & PAL UK. 2014. Efficacy of leaves (drumstick, mint and curry leaves) powder as natural preservatives in restructured chicken block. J Food Sci Technol 52(2): 3129-3133. https://doi.org/10.1007/s13197-014-1316-8.
  • PADAYACHEE B & BAIJNATH H. 2020. An updated comprehensive review of the medicinal, phytochemical and pharmacological properties of Moringa oleifera. S Afr J Bot 129: 304-316. https://doi.org/10.1016/j.sajb.2019.08.021.
  • PEREIRA KD. 2007. Resistant starch, the latest generation of energy control and healthy digestion. Food Sci Technol 27: 88-92. http://dx.doi.org/10.1590/S0101-20612007000500016.
  • RAHMAN MM, SHEIKH MMI, SHARMIN SA, ISLAM MS, RAHMAN MA, RAHMAN MM & ALAM MF. 2009. Antibacterial activity of leaf juice and extracts of Moringa oleifera Lam. against some human pathogenic bacteria. J Nat Sci 8(2): 219-227.
  • RAMACHANDRAN C, SUDHA RANI R, LAVANYA K, NIVETHA S & USHA A. 2017. Optimization of shelf stability of sugarcane juice with natural preservatives. J Food Process Pres 41(1). https://doi.org/10.1111/jfpp.12868.
  • ROCCHETTI G, RIZZI C, PASINI G, LUCINI L, GIUBERTI G & SIMONATO B. 2020. Effect of Moringa oleifera L. leaf powder addition on the phenolic bioaccessibility and on in vitro starch digestibility of durum wheat fresh pasta. Foods 9(5): 628. https://doi.org/10.3390/foods9050628.
  • SAADABI AM & ZAID IA. 2011. An in vitro antimicrobial activity of Moringa oleifera L. seed extracts against different groups of microorganisms. Aust J Basic Appl Sci 5(5): 129-134.
  • SALEM A, SALAMA WM & GHANDOUR E. 2013. Enhancement of nutritional and biological values of labneh by adding dry leaves of Moringa oleifera as innovative dairy products. World Appl Sci J 22(11): 1594-1602. https://doi.org/10.5829/idosi.wasj.2013.22.11.13024.
  • SALEM AS, SALAMA WM & RAGAB WA. 2015. Prolonged shelf life of sour cream by adding Moringa oleifera Leaves Extract (MOLE) or Moringa oleifera Oil (MOO). Am J Food Technol 10: 58-67. https://doi.org/10.3923/ajft.2015.58.67.
  • SHARAF AM, EBRAHIUM ME, AMMAR MS & ABD EG. 2009. Influence of using Moringa meal flour as meat extender on quality characteristics of beef burger patties during frozen storage. World J Dairy Food Sci 4(1): 32-40.
  • SHI Y, PRABAKUSUMA AS, ZHAO Q, WANG X & HUANG A. 2019. Proteomic analysis of Moringa oleifera Lam. leaf extract provides insights into milk-clotting proteases. Lwt - Food Sci Technol 109: 289-295. https://doi.org/10.1016/j.lwt.2019.04.035.
  • SHIRIKI D, IGYOR MA & GERNAH DI. 2015. Nutritional evaluation of complementary food formulations from maize, soybean and peanut fortified with Moringa oleifera leaf powder. Food Nutr Sci 6(5): 494-500. https://doi.org/10.4236/fns.2015.65051.
  • SILVA MM & LIDON F. 2016. Food preservatives–An overview on applications and side effects. Emir J Food Agr 28(6): 366-373. https://doi.org/10.9755/ejfa.2016-04-351.
  • SINGH TP, SINGH P & KUMAR P. 2015. Drumstick (Moringa Oleifera) as a food additive in livestock products. Nutr Food Sci 45(3): 423-432. https://doi.org/10.1108/NFS-02-2015-0018.
  • STRINGHETA PC, OLIVEIRA TTD, GOMES RC, AMARAL MDPHD, CARVALHO AFD & VILELA MAP. 2007. Health policies and functional property and health claims for food in Brazil. Rev Bras Cien Farm 43(2): 181-194. https://doi.org/10.1590/S1516-93322007000200004.
  • TEYE GA, BAFFOE F & TEYE M. 2013. Effects of Moringa (Moringa oleifera) leaf powder and dawadawa (Parkia biglobosa), on sensory characteristics and nutritional quality of frankfurter-type sausages – A preliminary study. Glob Adv Res J Agric Sci 2(1): 29-33.
  • THAMMARAT K & AIROUYUWA JO. 2020. Storage stability, gastrointestinal release and sensory properties of cookies incorporated with protein-based Moringa oleifera leaf extract microcapsule. Chiang Mai Univ J Nat Sci 19(1): 139-154. https://doi.org/10.12982/CMUJNS.2020.0009.
  • UDECHUKWU MC, ABBEY L, NWODO U & UDENIGWE CC. 2018. Potential of Moringa oleifera seeds and leaves as functional food ingredients for human health promotion. J Food Nutr Res 57(1).
  • YAMÉOGO CW, BENGALY MD, SAVADOGO A, NIKIEMA PA & TRAORE SA. 2011. Determination of chemical composition and nutritional values of Moringa oleifera leaves. Pak J Nutr 10(3): 264-268. https://doi.org/10.3923/pjn.2011.264.268.
  • ZIANI BE, RACHED W, BACHARI K, ALVES MJ, CALHELHA RC, BARROS L & FERREIRA IC. 2019. Detailed chemical composition and functional properties of Ammodaucus leucotrichus Cross. & Dur. and Moringa oleifera Lamarck. J Funct Foods 53: 237-247. https://doi.org/10.1016/j.jff.2018.12.023.
  • ZORZENON MRT ET AL. 2020. Spray drying encapsulation of stevia extract with maltodextrin and evaluation of the physicochemical and functional properties of produced powders. J Food Sci 85(10): 3590-3600. https://doi.org/10.1111/1750-3841.15437.
  • ZUNGU N, VAN ONSELEN A, KOLANISI U & SIWELA M. 2020. Assessing the nutritional composition and consumer acceptability of Moringa oleifera leaf powder (MOLP)-based snacks for improving food and nutrition security of children. S Afr J Bot 129: 283-290. https://doi.org/10.1016/j.sajb.2019.07.048.

Publication Dates

  • Publication in this collection
    22 Oct 2021
  • Date of issue
    2021

History

  • Received
    14 Apr 2021
  • Accepted
    23 Aug 2021
Academia Brasileira de Ciências Rua Anfilófio de Carvalho, 29, 3º andar, 20030-060 Rio de Janeiro RJ Brasil, Tel: +55 21 3907-8100 - Rio de Janeiro - RJ - Brazil
E-mail: aabc@abc.org.br