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Bioactive properties of Sambucus nigra L. as a functional ingredient for food and pharmaceutical industry

Karolina  Młynarczyk, Dorota Walkowiak-Tomczak
Poznan University of Life Sciences, Institute of Food Technology of Plant Origin, ul. Wojska  Polskiego 31, 60-624 Poznan, Poland

Grzegorz  P. Łysiak
Poznan University of Life Sciences, Faculty of Horticulture and Landscape Architecture, ul. Wojska  Polskiego 28, Poznan 60-637, Poland

Abstract

European black elderberry naturally occurs in most of Europe and has been introduced into  various parts of the world for fruit and flower production. Elderberry is rich in nutrients, such as carbohydrates, proteins, fats, fatty acids, organic acids, minerals, vitamins and essential oils. Elderberry also contains cyanogenic glycosides which are  potentially toxic. Polyphenols, known for their free radical scavenging (antioxidant) activity, are  the  most important group of bioactive compounds present in elderberry in relatively high concentration. The high antioxidant activity of elderberry fruit and flowers is associated with their therapeutic properties. Elderberry has for a long time been used in folk medicine as a diaphoretic, antipyretic and diuretic agent. In recent years it was also found to have antibacterial, antiviral antidepressant and antitumour and hypoglycemic properties, and to reduce body fat and lipid concentration. Due to its health-promoting and sensory properties, elderberry is used primarily in food and  pharmaceutical industry. [Link to download the complete article in pdf.]

Observations on this Article’s Content by C. J. Patton

I encourage you to read the entire article by using the link above. However, I know that many will not want to wade through the technical terminology, so I have listed my observations roughly following the order of the article’s structure and contents. I am not an educated or trained researcher in this field, but I have had years of experience reading technical material, so I have done my best to glean that which may be of most interest to consumers and to food and beverage professionals thinking about using elderberry or elderflower ingredients in their product lines. I have intentionally endeavored to maintain the article’s content context but confess ignorance concerning the degree importance any of my observations to academically trained and experienced researchers such as the authors. 

The journal authors responsibly posted references to the research backing up their content from which I made my observations posted below. I did not include those original research references on this page to keep the comments as brief as possible. Please go to the article pdf to get them. My page references are relative to the pdf printout.

1. "Black elderberry favours disturbed, base-rich and nitrogen-rich soils, and phosphate-rich soils. High levels of available phosphate and potassium and of mineralizable nitrogen were observed in a series of soils from S. nigra sites...despite its preferred natural environment, elderberry can be grown on a wide variety of soils…” (p. 1)
   
2. "The most popular European cultivars were developed in Denmark. The largest European producers are Germany, Denmark, Poland, Italy, Austria and the Czech Republic. (p. 2) However, Bulgaria and Croatia are popular sources for imported to the USA, wild-collected elderberry, especially in dried or concentrate forms.
3. "In the USA, elderberries are grown commercially on a small scale in the states of New York, Ohio, Oregon, Missouri and Kentucky. However, in the USA, the most commonly grown are hybrids between S. nigra ssp. nigra and ssp. canadensis. Breeders at the Experiment Station in Geneva (Cornell University) discovered that such hybrids are resistant to viruses spread in elderberry plantations by nematodes…” (p. 2) These Polish researchers are understandably not sufficiently informed about commercial production of native North American elderberry due to the lack of academic research on that reality. Most commercial elderberry grown in the USA are from native cultivars either directly, or originally, selected from the wild and not hybrids of S. nigra nigra. 
4. "Elderberries are planted in single rows.” (p. 2) Yes, but not exclusively. Also, I personally recommend that different cultivars be planted in blocks of rows and not interspersed in order to maintain cultivar homogeneity. Native elderberry can spread from row to row, so planting rows of different cultivars next to each other increases the probability of mixed harvests over time since the native elderberry roots can manifest as new plants up to ten feet away from the original plant installation, perhaps more. As we do more research, ingredients buyers will become more demanding of specific cultivars for reasons outlined below. 
5. "The chemical composition of Sambucus nigra is rich and depends on different factors, such as cultivar, location, ripening stage and climatic conditions…"
6. “Elderberry is a source of whole protein – its content is 2.7–2.9% in berries, 2.5% in flowers and 3.3% in leaves. This protein includes sixteen amino acids, nine of which are essential…” (p. 2)
7. Elderberry contains organic acids in this order of abundance: citric, magic, shikimic and fumaric. Citric acid and fumaric acid are used in River Hills Harvest products. “Minerals are located in both berries and flowers.” (p. 2)
8. "Elderberry fruit and flowers also include essential oils (around 0.01% in fruit), consisting of approx. 53 compounds in berries and 58 compounds in flowers…” (p. 2)
9. "Furthermore, elderberry seed flour is a source of α-Tocopherol (0.49 µg/g of oil), which has the highest vitamin E bioactivity, as well as γ-Tocopherol (2.63 µg/g), which shows better antioxidant potential …” (p. 2)
10. "All parts of the elderberry contain cyanogenic glycosides, the most abundant of which are sambunigrin and prunasin. Furthermore, elderberry contains m-hydroxysubstituted glycosides, such as zierin and holocalin... These compounds are potentially toxic and life-threatening, because they can be hydrolysed resulting in the release of cyanide... However, they occur primarily in unripe berries and are degraded during heat treatment.” (p. 2) This does not seem to be the case for native North American elderberry, S. canadensis, which will soon be demonstrated when a multiyear research project on this topic is published by University of Missouri researchers. 
11. "Moreover, elderberry contains the allergen Sam n1, which causes type 1 allergy and some tryptic peptides of Sam n1 demonstrate a high amino acid sequence with lectins and type 2 RIPs located in Sambucus... However, it was discovered that incubation in a boiling water bath for 5–10 min, made lectins completely sensitive to hydrolytic en- zymes in vitro and thus reduced the risk of allergenicity…” (p. 2, 4)
12. “The main polyphenols in elderberry fruit are chlorogenic acid, neochlorogenic acid, crypto-chlorogenic acid, quercetin, quercetin-3-rutinoside (rutin), quercetin-3-glucoside (isoquercitrin), kaempferol-3-rutinoside, kaempferol-3-glucoside (astragaline), isorhamnetin-3-rutinoside and isorhamnetin-3- glucoside. The primary flavonol in this plant is rutin, while the other flavonols, isoquercitrin and astragaline occur in elderberries in smaller amounts…" (p. 4)
13. "Elderberry is a very rich source of anthocyanins in comparison to other fruits. The fruit of Sambucus nigra contains anthocyanins, especially cyanidin-3-glucoside and cyanidin-3-sambubioside. Two other (minor) anthocyanins are cyanidin-3,5-diglucoside, and cyanidin-3- sambubioside-5-glucoside. In addition, trace quantities of cyanidin-3- rutinoside, pelargonidin-3-glucoside and delphinidin-3-rutinoside were identified in the fruit of certain elderberry cultivars. Their content depends on cultivar/variety, ripening stage, growing season or kind and method of extraction… The polyphenol content changes at different stages of fruit ripening, and each compound shows its own individual change pattern during this process.” (p. 4)
14. “...wild elderberry have the lowest quantities of these bioactive compounds. Total anthocyanin content varies almost threefold depending on the cultivar…” (p. 4)
15. "Alcoholic fermentation of berries causes changes in the content of phenolic compounds and anthocyanins, which also leads to colour changes. The concentration of polyphenols, such as neochlorogenic acid, chlorogenic acid, quercetin-3-rutinoside, quercetin-3-glucoside, kaempferol-3-rutinoside, cyanidin-3-sambubioside-5-glucoside, cya- nidin-3,5-diglucoside, cyanidin-3-glucoside or cyanidin-3-rutinoside, was observed to be higher in wine than in must, except cyanidin-3- sambubioside, which significantly decreased during alcoholic fermentation. The storage and aging of elderberry wine resulted in the decrease in the content of each analysed compound, and after three years the total phenolic content fell by 21%, whereas the total anthocyanins content was lower even by 94% compared to the young wine. Due to the degradation of anthocyanins, the colour of elderberry wine also changed from bright-red to brown–red hues. Antioxidant activity was also higher  in young  wine than  in must  and  dropped after  aging…” (p. 4) 
16. "The content of anthocyanins in elderberry products is affected by pH, storage time and storage temperature. It was observed that the extension of storage time and increase in pH and storage temperature resulted in the decrease in the content of anthocyanins in elderberry juice concentrate…” (p. 4)
17. "Elderberry pomace, although it makes up 25–40% of total fruit weight, is very rich in anthocyanins: it contains 75–98% of total anthocyanins found in fresh elderberries…” (p. 4) Many potential uses as a powdered ingredient in foods for both humans and animals.
18. "Sambucus nigra flowers contain even higher amounts of phenolic compounds in comparison to the  fruit  and  leaves  of this  species... The main group of phenolic compounds found in elderflowers are hydro-xycinnamic acids, the most important of which is chlorogenic acid. Other hydro-xycinnamic acids present in elderflowers include, among others, neo-chlorogenic acid, cryptochlorogenic acid, 3- and 5-feruloylquinic acid, and  dicffeoylquinic acids,  including notably 1,5-Di-caffeoylquinic acid. The second important group of polyphenols comprise flavonols, from which several glycosides of quercetin, kaempferol and iso-rhamnetin were detected in elderflower extracts.” (p. 4-5)
19. "Elderberry fruit is characterized by high antioxidant activity, which ranges from 82.08 to 89.25% of inhibition in relation to the DPPH radical. The antioxidant properties of elderberries are primarily attributable to the presence of phenolic compounds and depend largely on the chemical structure of molecules and composition of individual berries (Pliszka et al., 2005; Rice-Evans, Miller, & Paganga, 1996; Zheng & Wang, 2003). Anthocyanins significantly influence the antioxidant activity of elderberries. With the increase of anthocyanin concentration the antioxidant activity also increases, but only to a certain level… These results indicate that elderberry fruit is able to protect colon cells against the harmful effects of oxidative stress ” (p. 5) This activity is also referred to as anti-inflammatory.
20. "Flowers of Sambucus nigra usually have higher antioxidant activity than berries and leaves. According to Kołodziej and Drożdżal, (time required to reduce the initial DPPH concentration by 50%) was 23–75 s for flowers, whereas TEC50for fruit was 91–133 s. In another study, elderflowers exhibited stronger DPPH radical inhibition activity (91.95–94.15%) in comparison to berries (50.25–67.69%) and leaves (16.76–48.52%). These values also depended on the temperature of alcoholic extraction–in each case, extraction at a temperature of 100 °C resulted in a higher percentage rate of free radical inhibition than ex- traction at a lower  temperature (20 °C)…” (p. 5)
21. “...the effect of the intake of 400 ml elderberry juice or water (control) on the content and antioxidant capacity of total phenolics and anthocyanins and of ascorbic and uric acid in blood plasma. Both the content and the antioxidant activity of total phenolics and anthocyanins increased after juice ingestion, reaching the highest  level 1 h after the intake,  whereas the values of these para- meters did not change in the control group. At the same time, the concentrations of ascorbic and uric acid were unaffected by the elderberry juice or water intake ... Czank et al. found that the bioavailability of anthocyanins was higher and the diversity of their metabolites was greater than previously thought.” (p. 6)
22. "Flowers and berries of Sambucus nigra are known as a traditional remedy for various kinds of ailments and diseases and both are commonly used in folk medicine.. They are primarily used to treat common symptoms related to cold, feverish conditions, coughing, nasal congestion, mucous discharge and influenza, as well as a preventively to  strengthen the  immune system... Due to the presence of flavonoids, elderflowers demonstrate primarily diaphoretic, antipyretic and  diuretic properties, they obturate the capillary walls, improve their flexibility and prevent infiltration of red blood cells and plasma outside the vessels thanks  to the content of compounds (rutin) having the properties of vitamin P. Moreover, elderflowers show anti-inflammatory and antibacterial properties and therefore are used for gargling to treat sore throats or as compresses to treat  conjunctivitis. They are most often used as infusions of dried flowers for internal or external application. The fruit of Sambucus nigra, similarly to flowers, exhibits diaphoretic, antipyretic and diuretic properties, but apart from that it act as a laxative and detoxifier, hence elderberries are often a component of herbal mixtures used as a remedy for constipation or to help slimming. In addition, elder fruit demonstrates a moderate analgesic effect and can be used as an adjuvant painkiller against migraine, sciatica and neuralgic pains…” (p. 6-7)
23. "The healing properties of elderberry are mostly associated with the presence of phenolic compounds, which are characterized by a strong antioxidant activity and therefore are able to eliminate free radicals and counteract the oxidative stress, a factor causing the degradation of the human body, thus contributing to the development of a number of diseases... used mass spectrometry and liquid chromatography-mass spectrometry to demonstrate the chemo-preventive potential of elderberry. It was found that elderberry fruit extract, or rather an extract fraction that in addition to the phenolic compounds included e.g. iridoid monoterpene glycosides, phytosterols and sesquiterpenes, caused a strong induction of quinone reductase and inhibition of cyclooxygenase-2. This indicates antitumor activity of Sambucus nigra fruit, especially that preventing the initiation and promotion of cancerogenesis stages…(p. 7) Anti-inflammatory and anti-cancer benefits.
24. "The antibacterial activity of elder flowers, berries and leaves (aqu- eous or ethanol extracts of freeze-dried elder concentrates) was studied against 13 nosocomial pathogens, including methicillin-resistant Staphylococcus aureus (MRSA), which is known as a clinically significant pathogen connected with infections of skin and soft tissue. Despite a 100-fold dilution, ethanol extracts of both elder flowers and berries exhibited inhibitory activity for most of the analysed bacteria, both Gram-positive, such as Staphylococcus sp. or Bacillus cereus, and Gram-negative, such as Salmonella poona or Pseudomonas aeruginosa. Elderflower extracts displayed a higher antimicrobial efficacy and larger zones of inhibition against a broad range of bacteria, particularly MRSA (17 mm) or Pseudomonas aeruginosa (9 mm), than other extracts…” (p. 7) Here is an indication for the  under utilized anti-bacterial potential of elderberries and especially elderflowers in treating bacteria that otherwise resist or are immune to most antibiotic medicines. 
25. "The antiviral activity of Rubini® was investigated against two different human pathogenic virus strains, such as influenza A (KAN-1, H5N1) and B (B/Mass), in the Madin-Darby canine kidney cell culture. Treatment with elderberry extract distinctly reduced the spread of the foci size of influenza B virus, whereas the foci size of KAN-1 was enlarged, but its number was reduced in comparison to the untreated control… “ (p. 7) Antiviral properties.
26. "The mechanism of action was shown in Fig. 2. Taking into account these parameters, the effect of elderberry flavonoids related to inhibition of H1N1 is comparable to that of the known anti-influenza medicines, such as Oseltamivir (Tamiflu®) and Amantadine…” (p. 7)
27. "Additionally, in vivo experiments showed that elderberry effectively suppressed viral replication and could stimulate the immune response...Furthermore, elderberry extracts demonstrate an inhibitory effect on infectious bronchitis virus (IBV), a pathogenic chicken coronavirus, at an early stage of the virus infection. Elderberry extract  reduced IBV titers by several orders of magnitude, in dependence of the dose applied. The increase in the elderberry extract concentration caused a decrease in virus titers and vice versa. In addition, electron microscopy of virions that were treated with elderberry extract demonstrated compromised envelopes and the presence of membrane vesicles. There are data that indicate that the pretreatment with elderberry extract of IBV infection leads to damage to the virus extensive membrane and probably renders the virus non-infectious…” (p. 7) Potential use in poultry feed.
28. "Elder may be an effective traditional remedy for diabetes, and as such, it could be used as a dietary adjunct in diabetes treatment. It was found that water-soluble compounds included in elder flowers were able to directly stimulate glucose metabolism and promote insulin secretion through clonal pancreatic β-cells. An extract of elder flowers (1 g/L) significantly increased glucose uptake, glucose oxidation and glycogenesis in vitro in mice abdominal muscles without added insulin...The fruit of Sambucus nigra posi- tively influences the treatment of diabetic osteoporosis. A polyphenolic extract of elderberry improved the bone mineral density and reduced the body fat of diabetic rats. Also, the antioxidative capacity of serum improved in rats treated with the polyphenolic extract as the concentration of reduced glutathione (GSH) was restored to normal… li-pophilic and polar elderberry extract, respectively. The polar extract lowered fasting blood glucose, whereas the lipophilic extract decreased secretion. Both extracts reduced insulin resistance and no significant alterations in the hematological indices, sera lipids and trace elements homeostasis from sera and tissues  were  observed..." (p. 8) Potential to significantly aid diabetics as a dietary adjunct to medical treatment.
29. "Hepatic and intestinal mRNA changes with an improvement in HDL function and a decrease in hepatic cholesterol levels were also reported in elderberry- fed mice. Additionally, this group showed significantly higher activity of serum paraxonase-1 arylesterase. The results indicate the reduction of elderberry in aorta total cholesterol content and then less atherosclerosis progression…” (p. 10) Potential to lower cholesterol. 
30. “... evaluated the antidepressant activity of elderberry extracts by exposing mice to the forced swimming test (FST) and the tail suspension test (TST). The tests demonstrated very good antidepressant properties of the extract tested... caused a far higher activity of mice in the FST than imipramine (10 mg/kg), a strong and effective antidepressant drug…” (p. 10) Anti-deppresant potential for elderberry.
31. "Being rich in anthocyanins, elderberry belongs  to several  berry species that are used as natural colorants in different industries. Particularly, elderberry fruit is used as a food colorant, an ingredient in pharmaceuticals, concentrates, juices, syrups, jams, jellies, powders and other food preserves, a filling in pies, cakes or desserts, and also for the production of alcoholic beverages, such as wine... Elderberry pomace, which is a waste by-product of juice production, is an important raw material used in the production of anthocyanin extracts and lyophilized dyes. It is also used as animal feed and organic fertilizer...Elderflowers, similarly to berries, are also widely used in food industry. They are natural flavouring components in alcoholic and non- alcoholic beverages, sparkling, bitter and white wine, fruit brandies and various spirits, as well as in tea and products like yoghurt or ice cream...According to a 2010 report by the European Herb Growers Association,  Sambucus nigra (flowers and berries) was the most harvested medicinal plants intended for export trade and for tea and phytopharmaceutical production in Bulgaria and Romania... Elderberry ranked as the 18th best-selling herbal dietary supplement on the medicine, food and mass market in the USA in 2011…” (p. 12)