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Articles

Antioxidant activity, antimicrobial and effects in the immune system of plants and fruits extracts

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Pages 90-98 | Received 09 Sep 2015, Accepted 02 Oct 2015, Published online: 20 May 2016

ABSTRACT

Nowadays, medicinal plants, and fruits and vegetables with antioxidant and antimicrobial activity are increasingly studied. In this review, the impact of the medicinal plant extracts on the immune system was discussed. The first part described the phenomenon of oxidative stress, followed by the mechanisms involved in the antioxidant activity and finally discussed on the evaluation of the antioxidant activity of plants and fruits. The second part revised the works that discuss about the antimicrobial activity of plants and fruits extracts, emphasizing in the factors that influence the evaluation of such characteristic. Finally, in the third part,  studies on the effect of the plant extracts over the immune response were discussed, describing the results of the enhancer effects, as well as those of the suppressing ones. This work allowed us to discern the necessity of a wider research on the chemical composition of the natural extracts, in order to establish a correlation with the effects observed in health.

Introduction

Humans generate knowledge and develop technologies. With them, they synthesize a wide variety of compounds to improve their quality of life. Such compounds (e.g. drugs or insecticides), although solve health problems, cause damage both to the consumers and to the environment. However, humans, in order to solve health and environmental problems, have turned their attention to the use of natural alternatives, such as plant extracts.

Plant extracts have the advantage of having a biological origin, are biodegradable and demonstrate a positive impact on human health and the environment (Bravo et al. Citation2000). The use of plant extracts to heal diseases has been documented since ancient times: the first apothecaries emerged in the ancient civilizations of Mesopotamia (4000–5000 BC), particularly the Babylonians; also Egyptians, Chinese and Indians made use of this resource (Jácome Citation2003).

Among the various properties that medicinal plants, vegetables and fruits possess, antimicrobial and antioxidant properties are chosen as the subject of this review. Furthermore, this paper documents the effect of extracts of such products on the immune system.

Plants with antioxidant activity

Although the human body has an antioxidant defense system, often this system is not sufficient to neutralize the multiple attacks that bombard the body day by day. In order to maintain a balance between oxidants and antioxidants in the body, typically substances acting on reactive oxygen species is used in the form of food supplements. However, in recent years, use of some synthetic antioxidants has been restricted because of their toxic and carcinogenic effects (Frankel et al. Citation1995).

Therefore, alternative medicine has been used, such as extracts or herbal teas and fruit with antioxidant properties. These properties are being increasingly studied by the scientific community. Various studies show that some medicinal plants have more potent antioxidant activity than some fruits and vegetables (Song et al. Citation2010).

Consumption of fruits and vegetables with antioxidant capacity, as well as medicinal herbs and plants that have this property can provide optimal health and nutritional outcomes. This is based on that quality nutrition may have beneficial effects in the prevention of some chronic diseases prevalent in society (Weisburger Citation2000).

Vegetables are an alternative of quality nutrition, as they have natural substances and enzymatic systems that retard or prevent oxidation and protect against free radical attack than are normally produced in the metabolism. These are endowed with a series of enzymes and small molecules which react with free radicals. For example, superoxide dismutases catalyze the dismutation of superoxide anion (O2−) to hydrogen peroxide (H2O2) and O2, while the nonspecific peroxidases and catalases destroy H2O2.

However, most of the antioxidant capacity of fruits and vegetables is provided by its content of vitamin E, C and carotenoids, as well as different polyphenols (Ko et al. Citation2005; Zugic et al. Citation2014) () which are essential for life. Polyphenols as antioxidants can protect cells against oxidative damage and therefore reduce the risk of various degenerative diseases associated with oxidative stress caused by free radicals (Scalbert et al. Citation2005; Huang et al. Citation2010). Among the more important phenolic compounds are flavonoids, which, besides its demonstrated antioxidant activity, has been attributed with a wide range of therapeutic effects, such as cardiotonic, anti-inflammatory, hepatoprotective, antineoplastic and antimicrobial activity. (Narayana et al. Citation2001).

Table 1. Natural and synthetic antioxidant molecules.

Food with vegetal origin contains a variety of hydroxylated flavonoids and other phenolic compounds in amounts, ranging from traces to several grams per kilogram of fresh weight. From above derives the importance of the study of the antioxidant properties of vegetables used in human nourishment. The daily intake of polyphenols in individuals who have a diet rich in these foods is approximately 1 g/day. It has been observed that there is a wide variation in bioavailability between polyphenols observed as between individuals (Scalbert et al. Citation2005). In general, bioavailability is in function of the solubility (Eastwood Citation1999) and therefore the polyphenols present different absorption levels in biological media (Bourne et al. Citation2000).

Some plants with antioxidant activity due to the polyphenols are: cat tail, ginseng, gingko biloba, eleu- therococcus, anamú, grapes, eucalyptus, mandarin, grapefruit, lemon, orange, rosemary, agrimony, tangerine, calendula and oat (Abad-Garcia et al. Citation2012) (). They have properties relevant to human health functioning as antiradicals, antimutagenics, anticarcinogenics, ratardants of senescence; antiatherogenics and antimicrobials (Reyes et al. Citation2009).

It is recognized that some plants have positive antioxidant effects when they were tested against reactive oxygen compounds in biological systems. Many subproducts of plants such as peanut hulls, red grape, carob seeds, citrus peel and some seeds, as well as malt root extracts have also been exploited because of their antioxidant potential (Bonnely et al. Citation2000).

Evaluation of antioxidant activity

Although there are different methods to evaluate the antioxidant activity, either in vitro or in vivo, in vitro methods allow us to have an approximate idea of what happens in complex situations in vivo. The most used methods are ABTS (2,2′-azino-bis [3-ethylbenzothiazoline]-6-sulfonic acid) and DPPH (2,2-diphenyl-1-picrilhidrazil). Both methods have excellent stability under certain conditions although they exhibit differences. DPPH is a free radical obtainable directly without prior preparation, while ABTS has to be generated after a reaction which may be chemically (manganese dioxide, potassium persulfate, 2,2′-azobis [2-amidino propane]), enzymatic (peroxidase, myoglobin) or also electrochemical. With ABTS, the activity of lipophilic and hydrophilic compounds can be measured, which makes it very useful in the simultaneous study of various plants (Castañeda et al. Citation2008).

Moreover, in a study conducted on 56 plants to determine the antioxidant properties and phenolic content, the 4 plants that showed a higher concentration of phenolic compounds were Dioscorea bulbifera (59.43 ± 1.03 mg GAE [gallic acid equivalents]/g), Eriobotrya japonica (31.47 ± 0.48 mg GAE/g), Tussilago fárfara (30.03 ± 0.19 mg GAE/g) and Ephedra sínica (27.70 ± 0.89 mg GAE/g).

D. bulbifera is a plant used in the prevention of tumors, diabetes and leprosy, and the more important compounds that give the antioxidant activity to the plant are (+)-catechin and myricetin; E. japonica has anticarcinogenic, inflammatory, hypoglycemic and hypolipidemic effects; T. fárfara has antimicrobial activity and is used in bronchitis treatments and asthmatic disorders; finally, E. sínica is employed for the treatment of multiple symptoms of cold and allergy, in body weight control, in the treatment of acute liver failure and to alleviate the inflammatory responses (Song et al. Citation2010).

After water and coffee, tea is the most consumed beverage in the world (Mantilla Citation2003). This last drink can be consumed in various varieties, black tea, oolong tea, white tea and green tea. A cup of green tea provides about 150 mg of flavonoids, most released during the first minutes of infusion.

Guava consumption reduces oxidative stress, and the risk of diseases caused by free radicals and hypercholesterolemia (Rahmat et al. Citation2004). However, the flavonoid content in the leaves of guava is greater than in the fruit; hence, the leaves could be used to extract flavonoids (Vargas et al. Citation2006) and also to suggest its use in less traditional ways as extracts or infusions.

Another study reported that the antioxidant capacity of a glass of wine equals 7 orange juices or 20 apple juices (Neira Citation2004).

It is known that the antioxidant properties of plants and fruits are related to not only the total amount of antioxidants, but also the presence of certain compounds. You could say that the total antioxidant content of fruits, vegetables, juices and beverages can be interpreted as the combined action of endogenous antioxidants.

The antiradical action of some fruit juices or beverages can be due to (i) differences in the content and the composition of bioactive (ii) diversity in structural features of the potential of phenolic antioxidants and (iii) a synergy of bioactive with other components present in each of the juices or drinks, and (iv) the differences in the kinetic behavior of possible antioxidants. All these factors may contribute to the efficiency of the antioxidant activity of juices and beverages (Ramadan Citation2008) ().

Table 2. Antioxidant capacity by DPPH method.

Antimicrobial activity

The use of plant extracts in alternative medicine has increased in recent years (Duraipandiyan et al. Citation2013), so that the health-care system has evolved among the Hispanic community in North America since Spanish colonialism. Initially the natives of American countries used plants to treat their illnesses, this goes back to Spanish colonialism and has its roots in the Spain occupied by Arabs, Greek humoral medicine and Aztec mythology (Van Wyk et al. Citation1997). Among the properties that are ascribed to plants is the antimicrobial activity. The ways to obtain the plant extracts, methods to evaluate the antimicrobial activity, as well as test microorganisms are diverse ().

Table 3. Methods for obtain extracts of plants and for measuring its antimicrobial activity.

The results of the evaluation of the antimicrobial activity differ substantially from each other. Among the factors influencing these differences are those that may be attributable to the substances under study, the method in which the activity is assayed and in the protocols variations between different research groups (Boorn et al. Citation2010). So, many reports of the antimicrobial activity of substances are difficult to compare because of the differences in methodology. In some cases the aqueous extract is the one that has higher antimicrobial activity (Velasco et al. Citation2005) and in others is the ethanolic extract (Tolosa & Cañizares Citation2002). Some authors have reported contradictory results from the antimicrobial activity of the extract of the same plant (Bommarito et al. Citation1998; Suárez et al. Citation2007). This suggests that the effectiveness of plant extracts may depend on the test microorganism, the method of extract obtainment and the method of evaluation of the antimicrobial activity.

The antimicrobial activity depends upon several factors. The kind of extraction and separation conditions of the fractions influence the antimicrobial activity of extracts (Rubilar et al. Citation2011). These show selectivity for inhibiting the growth of microorganisms (Gaetti-Jardim et al. Citation2011) since some extracts may inhibit the growth of pathogenic bacteria and show no activity against innocuous bacteria or against fungus (Shene et al. Citation2009), which is attributed to different mechanisms of growth or reproduction that have the groups of microorganisms.

Nevertheless, it has also been observed that the oil extracted from the leaves of certain plants may not have significant bacteriostatic effects, but demonstrate strong antifungal activity (Tomczykowa et al. Citation2008). They can also be more effective against Gram positive bacteria than against Gram negative, which is probably due to its thin murein layer that prevents the entry of inhibitors (Rabe & Van Staden Citation1997).

The antimicrobial activity of the plants is due to the presence of polyphenolic compounds, which are in larger quantities in the crude extracts of leaves than on fruit extracts, while the former has more antimicrobial activity (Rubilar et al. Citation2011). Such activity depends on intrinsic factors (genetic characteristics, concentration of components in the plant, part of the plant used and plant stage in which the cut is made in the same, extrinsic factors – environmental conditions), factors such as treatment methods and how to evaluate the antimicrobial activity, and synergistic factors, antagonistic and additives – result of the interaction of various compounds in the medium.

Results of many research papers on the antimicrobial activity of extracts are not directly comparable because there are no standardized methods for measuring antimicrobial activity. Al-Bakri and Afifi (Citation2007) reported that some methods are comparable when estimating the antimicrobial activity of the substances, in a general way, but there is not a strong linear correlation between them (Al-Bakri & Afifi Citation2007). Among the agar-based assays to measure the antimicrobial activity, Othman et al. (Citation2011) propose the disk diffusion method, in which agar is poured on plate, which presents more reproducible results (Othman et al. Citation2011). However, Boorn et al. (Citation2010) reported that the agar diffusion method is not the most appropriate to evaluate the activity of complex natural substances (Boorn et al. Citation2010). Among the limitations of the agar diffusion method, it is considered that low levels of antimicrobial activity may not be detectable (Allen et al. Citation1991), and also because non-polar compounds may not diffuse properly in aqueous-based agar (Griffin et al. Citation1999).

Despite the large number of papers published on the antimicrobial activity of extracts of natural products, standard methods to measure antimicrobial activity and in-depth details regarding the chemical characterization of these extracts are still missing, which, if provided, will help us to study the groups of compounds resoponsible for the above-said activity, isolate them and apply them with more specific antimicrobial purposes.

Immune system effects

In addition to the antimicrobial activity of plant extracts, studies concerning the effects therefore on the immune system have become more relevant in recent years. The interest of the scientific community to find new drugs with potential effects on the modulation of the immune response is strongly associated with the findings on the participation of the immune system in the development of cancer (León & Faxas Citation2004) and other conditions.

Therefore, the discovery of active substances that regulate the immune response could lead to significant advances in the treatment of immunologically mediated diseases, including cancer, allergies, autoimmune phenomena, immunodeficiencies, organ rejection and infectious diseases.

Plants with activity on immune system

Conventional medicine employs scientifically established treatments to treat conditions associated with abnormal function of the immune system. However, there are diseases whose symptoms are not completely beaten down by conventional medicine. In these cases, the patients appeal to the use of plant infusions as additional or alternative therapy. Although the use of the products listed is not scientifically based, there are several investigations that seek to describe the mechanisms of action of plant extracts on immune system components.

So far potentiating effects have been described () and suppressors () of the immune response induced by extracts of plants, so that the applications of these in current therapeutic become relevant.

Table 4. Natural products with potentiating effect of the immune response.

Table 5. Natural product with immunosuppressive effect.

Potentiating effects of the immune response

In conditions such as immune deficiencies and cancer, immune response decreases; that is why it is so desirable to increase the same in these patients. Also in some infectious disorders, such as tuberculosis, it is important to ensure that the immune response can be potentiated to eliminate microbial antigen. In all these conditions, stimuli and effector mechanisms of the immune response are different. However, they have a common factor, the need for the use of drugs which allow the increase of the immune response facing certain antigens. Historically adjuvants have been used, for example vaccines to enhance immune response against specific antigens. The classic example of this is Freud's complete adjuvant, used in the production of antisera in situations where limited quantities of antigen are available or when this present low immunogenicity (Morris et al. Citation1999). However, their use has high toxicity, so that science seeks alternatives with equal effect and fewer side effects.

Currently the alternative medicine is the one that has contributed to the study of the action mechanisms of the active principles of plants and substances employed in ethno pharmacy as modulators of the immune response. details the more relevant scientific findings related with the possible therapeutic potential of plant extracts regarding the potentiating effect.

Not all effects of the products listed in have been studied in pathological models. However, they produce a clear visible change in the immune response; either increasing the humoral or cellular immune response, or by inducing an increase in the inflammatory response by increased secretion of pro-inflammatory cytokines, as in the case of Andrographis paniculata (Rajagopal et al. Citation2003; Kumar et al. Citation2004).

The effects of Echinacea, ginseng and vitamin C on immune system cells have caught attention. These findings explain, at least in part, the effects of these products in cancer treatment.

Suppressive effects of the immune response

Unlike in cancer, in autoimmune processes, allergies and organ rejection phenomena, there is a not desirable exacerbated immune response, so these treatments are directed to reduce this response. In these phenomena, the immune response is exacerbated against different types of antigens -autoantigens, innocuous antigens, alloantigens, respectively- so they are used as nonspecific antigen immunosuppressive drugs with good results. However, so far no treatment has been found to cure these diseases, so therapies with fewer adverse reactions, and equal or better therapeutic effects are searched.

Alternative medicine has generated scientific research in pursuit of immunosuppressive treatments; summarizes some of the major findings in this respect.

Márquez et al. (Citation2008), Rodríguez et al. (Citation2005) and Domínguez and Bacallao (Citation2002) describe animal models of inflammation and have tested the effect of Pinus leiophylla, Bryophyllum pinnatum and Morinda citrifolia respectively. These investigations described the potential therapeutic effects of these species; however, they do not describe the mechanisms of action.

So far, there are relatively few investigations that are identifying the active principle of the plant extracts and the exact mechanism of action of the same. Such as in the example of the research made by Huang et al. (Citation2010), which examines the effect specifically on dendritic cells quercetin, finding inhibition of endocytosis by these cells (Huang et al. Citation2010). Furthermore the authors of this study also describe a decreased production of pro-inflammatory cytokines and chemokines. As a result of studies, the suppressive effect of natural extracts on the immune response is closely related to the decreased production of pro-inflammatory cytokines.

Currently, investigations are beginning to explore the effects of natural products on the number or function of regulatory T cells, which are intimately involved in the modulation of immune response. Such is the case of vitamin C found in citrus fruits, which is found to be a potential inducer, generating regulatory T cells (Tan et al. Citation2005). However, the findings of Tan et al. (Citation2005) contrast those of Wintergerst et al. (Citation2006) describing a leukocyte activation.

Conclusions

It is evident that plant extracts, and generally natural products, are potential sources of drug with antioxidant and antimicrobial activity as well as immune-response mediators. The effect of these products on health and their mechanisms of action must be studied. This will allow us to find the best form of administration of substances and the conditions in which they could deliver better benefits.

Disclosure statement

No potential conflict of interest was reported by the authors.

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