Sandy Jiang Introduction
The genus Asparagus contains more than 200 species, of which Asparagus officinalis L., (Figure 1) is the most well- known; it can be found both at the supermarket and on our dinner tables. Asparagus belongs to the Asparagaceae family. “Asparagus” is supposedly of Persian origin (Hexamer, 1901), and it is believed to have originated in the eastern Mediterranean region, but can now be found growing in many parts of Europe. Naturalized in the Americas and even New Zealand, it is now a common crop grown for its young edible shoots that resemble spears. The lower fibrous parts of the plant are usually peeled off, leaving the tips to be consumed (Grubben, 2004). A. officinalis is high in nutrients, particularly carotenoids and sulfur containing compounds which both give the plant its distinctive taste. A. officinalis is also high in saponins, which have been shown to have antifungal, antioxidant, hypolipidaemic, hypoglycemic, and hepatoprotective properties. Recent studies have shown that compared to the stem, the often discarded bases actually contain more bioactive compounds. More research is being conducted on this exciting aspect.
Botanical Description
The asparagus plant (Figure 2) is a dioecious perennial herb with erect stems up to 2 meters tall. The thick stalks have bud clusters with leaves that resemble prickly brownish scales. The true leaves usually become spines at the base of the
Figure 1. A. officinalis. Image Source: http://2.bp.blogspot.com/- wchTZKfSOHY/T-
odkzJN9tI/AAAAAAAAIVo/p8qaIvATDUI/s1600/asparagus+draw.j pg
branches while the false leaves, termed cladolia, are actually the same as modified branches (Hexamer 1901). The flowers are unisexual, small, greenish-yellow and differ in size depending on of the gender of the plant. The fruit produced are red berries up to 1 cm in diameter that produce black, round, and flattened-on-one side shaped seeds (Grubben 2004).
Figure 2. A. officinalis plant structure. Image Source: http://www.mdidea.com/products/proper/asparagus- officinalis.jpg
Asparagus germination is slow even at optimum temperatures of 25-30°C. Flowering, which relies on insect pollination, is continuous and begins in the plant’s first year of life. An adequate amount of nutrients is necessary, and fertilizers are usually administered annually to these crops. Good balance of fertilizers and appropriate water drainage systems can protect the plant against certain Fusarium infections which can cause devastating results to crops. Most diseases that attack asparagus are fungi including Stemphylium botryosum,
Cercospora asparagi, and Phoma asparagi (Grubben 2004).
In warmer climates, the asparagus plant is green throughout the year, but in temperate climates, it senesces during autumn and resumes growth during spring. The seeds are usually grown in situ within a green house rather than directly sown into the field. The choice of the asparagus species is crucial as it is a long-term plant (Grubben 2004). The soil must be well- drained, sandy, naturally fertile, silicious, and deep so that the roots can penetrate deeply and absorbed all the nutrients from that soil (Ilot 1901). Older asparagus roots become hollow over time as young roots form above them. Thus, asparagus plants gradually rise above the original soil level and it is often necessary to cover up the exposed crowns with additional soil (Ilot, 1901).
Traditional Uses History
It is believed that asparagus was first cultivated by the Egyptians or Greeks. In his book De Re Rustica, Cato lauded the plant as a valuable garden vegetable for the Romans. Cultivated asparagus went back to being wild after the fall of
the Roman Empire before it was brought back into the monastic gardens of the Middle Ages. It has been said that the Italians cultivated the finest asparagus, and therefore many societies compared their asparagus to that of the Italians’. Also, the French Huguenot refugees brought asparagus to England, improving the delicious but not as robust English variety. The English colonists then brought asparagus to North America, where it became a commercial crop in the 19th
century (Chiffolo & Hesse, 2006).
Traditional medicinal uses
The Romans prized the asparagus highly and it was one of their oldest and most valued medicines. The fresh roots were used as a diuretic and as a sedative while syrups made from the young shoots and extract of the roots were used as a sedative for heart problems. Mixtures of asparagus, celery, parsley, holly, and fennel were used for the treatment of dropsy and gravel. Also, a liniment of asparagus and oil was believed to protect the user from bee stings, and the root was used for tooth aches (Hexamer 1901).
Since A. officinalis is a cultivated plant, most traditional uses in medicine came from Asparagus racemosus Willd as it was the wild variety. A. racemosus was used in traditional Indian medicine to increase fertility and to cure bodyaches. Women would take half a cup of root extract early in the morning for seven days to increase fertility and conception while tribal ladies took the root powder orally to cure bodyaches and leucorrhea. A. officinalis was used to increase sexual potency for both men and women (Jain et al., 2004).
The asparagus species has been used in India and China for its diuretic properties as it flushes the kidneys and helps prevent formation of kidney stones. An interesting folk belief is that
Chinese pharmacists save the best asparagus roots for their close friends and families, believing it will promote feelings of compassion and love. A. officinalis roots have been used as a remedy for schistosomiasis, tuberculosis, dropsy, and cardiac medicine in these societies as well as Western medicine (Negi et al., 2010).
Food uses
Asparagus is usually eaten cooked. The tips are usually eaten, with chefs cutting off most of the base. Asparagus can also be eaten raw, though thinner stalks are preferred as they tend to be tenderer compared to the fibrous thicker stalks Fresh asparagus must be consumed immediately as asparagus have high respiration rates and will become hard and more fibrous and thus, not consumable. Asparagus can be bottled, canned, or frozen. The seeds have been reported to be used to make a coffee like beverage while germinating seedlings have been used as vegetables (Ong, 2008). Asparagus, because of its buttery taste can be used in casseroles and almost any other dish including cream of asparagus soups, fried dishes, broths, and stir fries (Shulman,2010). A. officinalis is usually recognized for two varieities, green and white. The white asparagus is grown by covering the plant in dirt to keep it growing in the dark. This process, termed “etiolation” gives it a more bitter taste, but a tender, fiberless, soft, and more delicate flavor than the green variety.
Ethnobotanical Uses
Asparagus are high in saponins which give it its characteristic taste. Saponins have been shown to have spermicidic and antifungal properties. In India, asparagus has been used for its medicinal purposes for centuries, and it is believed that
Figure 3. Thiols are also known as mercaptans which give asparagus its famous odor.
saponins are the main active ingredients behind these physiological activities. The bottom parts that are usually chopped off and discarded are found to actually possess high amounts of saponins (Shimoyamada et al., 1990).
Pest Control/ Cultivation
The common asparagus beetle Crioceris asparagi was a huge pest in the early United States in both its larval and adult forms (Ilot 1901). The insect preys on the soft parts of the asparagus plant rendering it unfit for human consumption. The insect however was very susceptible to sudden changes in temperature and had a wide variety of predators. Chickens and ducks were efficient predators employed by farmers to curb disease. Prominent asparagus farmers used to cut down all plants in early spring to force the beetles to lay eggs on new shoots which were cut before the eggs could hatch. Other stalks were designated as sacrificial to lure the beetles before air slacked lime was dusted on the plants in the early morning to kill the pests (Hexamer 1901). Paraffin and soap were described by Charles Ilot to be efficient insecticides. It is interesting that such organic methods kept the shoots still safe to consume while efficiently removing the pests compared to modern chemicals.
Harvesting
Asparagus is perennial plant and can be harvested annually. It is typically not economical to harvest asparagus plants that are over 10-15 years of age, but asparagus plants over a hundred years of age have been located in western Europe. The spears of the plant are the most marketable and require high nutrition to ensure quality, meaning that there must be sufficient nutrients in the base of the plant to fuel its growth. Thus, most asparagus are not harvested until two years after planting to ensure proper nutrition for the plant. The spears are cut and washed before being sorted and packed for marketing. Asparagus have high respiration rates and will shrivel without water. Thus, they have short shelf lives and must be kept under high humidity conditions (Grubben 2004). Chemistry and Pharmacology
Like many plants, asparagus is high in many allelochemicals and other nutritious chemicals, including minerals and carotenoids. A. officinalis also contains sulfur compounds, which are responsible for its distinctive taste and smell.
Both the green and white varieties of A. officinalis are edible, though the green variety is more abundant in micronutrients. The characteristic odor of asparagus is derived from dimethyl sulphide, which is formed from the degradation of the amino acid S-methyl methionine (Grubben, 2004). Sulphur containing compounds are known as thiols or mercaptans (Figure 3). The pungent urinary odor produced by many individuals after the consumption of asparagus has been shown to be due to six mercaptans: methanethiol, dimethyl sulphide, dimethyl disulphide, bismethyl methane, dimethyl sulphoxide, and dimethyl sulphone (Waring, Mitchell,
Nutrient n=100g sample Percentage of 100g sample Water 75 g 75% Energy 25 kcal - Protein 2.9 g 2.9% Fat 0.6 g 0.6% Carbohydrate 2 g 2.0% Fiber 1.7g 1.7% Calcium 27 mg 0.027g% Magnesium 13 mg 0.013% Phosphorus 72 mg 0.072% Iron 0.7 mg 0.0007% Zinc 0.7mg 0.0007% Carotene 315 μg 0.000315% Riboflavin 0.06 mg 0.00006% Niacin 1 mg 0.001% Vitamin C 12 mg 0.012%
Table 1. Breakdown of nutrient components of Asparagus officinalis. Source: Grubben, J.G.H., (Ed.)(2004). Vegetables: plant resources of tropical Africa. (Vol.2). Wageningen,
Netherlands: PROTA foundation/Backhuys Publishers.
Fenwick, 1987). A. officinalis also contains a wide variety of nutrients, including calcium, phosphorus, and protein (Table 1).
A. officinalis is high in carotenoids, especially in its fruits. The
ripe fruits contain large amounts of capsanthin, β-carotene, and zeaxanthin and small amounts of capsorubin, cryptoxanthin, cryptocapsin, antheraxanthin, violaxianthin, and capsanthin isomers. Interestingly, the biosynthesis pathway of carotenoids in A. officinalis was found to be similar to that in paprika (Deli, Matus, Tth, (2000).
It is interesting to note that once old asparagus plants die, the field cannot be used to replant new asparagus crops because
the leftover tough roots release hytotoxic compounds and may have Fusarium oxysporum (FOA) infections (Grubben, 2004). Asparagus plants and their decaying root tissues have been shown to release allelochemicals such as autotoxins, which can make the plants more susceptible to FOA infections or exacerbate pre-existing FOA infections (Nair et al., 1990). Of the two varieties, the white asparagus is grown by covering the plant in dirt to keep it growing in the dark. This process, termed “etiolation” gives it a more bitter taste, but tender, fiberless, soft, and more delicate flavor than the green variety. Saponins are primarily responsible for the asparagus’s bitter taste. In 2012, Hofmann and Dawid isolated five other compounds that contribute to the bitter taste. Table 2 lists the names and the human taste thresholds for these compounds. Hofman and Dawid also found that asparagus plants have a buttery mouth-coating effect that was attributed to the two 1,2-dithiolan-4-carboxylic acid 6-D-glucopyranose esters.
Biological Activity
The edible portions have been shown to possess antifungal, antioxidant, hypolipidaemic, hypoglycemic, and hepatoprotective activies. During the industrial processing of
A. officinalis, around 30-40% of the spear is discarded as
waste which wastes food and leads to significant environment pollution. However, it has recently been shown that the base is rich in bioactive phytochemicals such as steroids, and in particular, saponins (Wang et al, 2012). Saponins have a large variety of biological properties including antioxidants, immunostimulants, antihepatotoxic, antibacterial, therapy for diabetic retinopathy, anticarcinogenic, antidiarrheal, antiulgerogenic, antioxytocic, and reproductive agents. Saponin rich plants, such as A. officinalis have been shown to improve growth, feed efficiency, and health in cattle such as
sheep and cows (Negin et al., 2010). This biological activity section explains the in vitro and in vivo studies performed by various studies on the bioactive properties of A. officinalis. Table 3 summarizes the plant parts, isolated compounds, and the activities of the compounds mentioned before and in this section.
In vitro
Proteolytic Properties
Proteolytic enzymes break down proteins and thus can tenderize meats for culinary purposes. Ha et al., (2012) performed a study comparing kiwifruit and asparagus extracts and their proteolytic activities in tenderizing meats. Although purer cysteine enzyme extracts are needed for further analysis, they found that asparagus had noticeable effects in tenderizing meats. Even though asparagus was not as effective as kiwifruit, ester hydrolysis in asparagus occurred over the entire assay pH range from 2-14 and between temperatures 45-75°C, whereas the same reaction in kiwifruit extracts was restricted to a pH range of 5.5-7 and a narrower temperature range. The asparagus enzyme hydrolyzed myofibrillar proteins slower than kiwifruit. Although it only targeted myosin heavy chains, after an extended incubation, the myofibrillar proteins, except troponin C were degraded.
Alcohol Metabolism
Another study was on the alleviation of alcohol hangover in which A.officinalis leaves and shoots extracts increase the activities of two key enzymes that metabolize ethanol, alcohol dehydrogenase (ADH) and CYP2E1. Chronic alcohol use can cause ethanol induced fatty liver as well as oxidative stress
Table 2. Five saponins found in Asparagus officinalis that give its bitter taste and the human taste recognition
thresholds. Source: Dawid, C., &Hofman, T., (2012). Structural and sensory characterization of bitter tasting steroidal
saponins from asparagus spears (Aspragus officinalis L.).
Journal of Agricultral of Food Chemistry.
caused by the production of cytochrome P-450E1. ADH metabolizes ethanol to acetaldehyde and then acetaldehyde dehydrogenase (ALDH) before becoming acetate. Acetaldehyde at high concentrations can cause toxic effects such as sweating, vomiting, and increase pulse rate and thus, there is a need to find an efficient and quick way to remove excess alcohols and their metabolites from the body. Kim et al.(2009) demonstrated that the leaves which are usually discarded have the most therapeutic use compared to the stem for alcohol hangover treatment especially on the HepG2 cell line. A. officinalis had significant effects on ADH and ALDH by providing strong antioxidant activity and acting as a potent
Compound
no. Compound Threshold (μmol/L)
1 3-O-[α-L-Rhap-(1→2)-{α-L-rhap-(1→4)}-β- D-glcp]-26-O-[β-D-glcp]-(25R/S)-22- hydroxyfurost-5-ene-3β,26-diole 65.9 2 (25R/S)-furost-5-en-3β,22,26-triol-3-O-[α- L-rhap-(1→4)-β-D-glcp]-26-O-β-D-glcp 10.9 3 (25R/S)-furostane-3β,22,26-triol-3-O-[α-L- rhap-(1→4)-β-D-glcp]-26-O-β-D-glcp 25.5
4 3-O-[{α-L-Rhap-(1→2)}{α-L-rhap-(1→4)}-β- D-glcp]-(25R/S)-spirost-5-ene-3β-o
70.6
5 3-O-[{β-D-Glcp-(1→2)}{β-D-xylp-(1→4)}-β-
D-glcp]-(25S),5β-spirostan-3β-ol 199.7
Aerial
parts 2-hydroxyasparenyn 4’trans-2hydroxy-1methoxy-4- 5(4methoxyphenoxy)-3- penten-1-ynyl-benzene
Inhibitory against cyclooxygenase -2
Fruits Capsanthin, capsorubin, capsanthin 5,6 epoxide 3-O-[a-L-rhamnopyranosyl (1- 2);] beta-o- glucopyranosyl](25S)spirost- 5-ene-3beta-ol Antifungal
Seeds Methyl protodioscin and
protodioscin Cytotoxic
Fruits Spirostanol glycoside Immobilization of human spermatozoa
Roots Sucrose-1-fructosyltransferase Cytotoxic Roots Sarsasapogenin and nine
asparagosides A,B,C,D,E,F,G,H, and I
Cytotoxic
Roots Steroids Cytotoxic Leaves Flavonoids and rutin Cytotoxic
Base Saponins Antitumor and anticancer Base Saponins Antifungal
Table 3. Chemical compounds found in A. officinalis and their activities.
catalytic factor to stimulate the enzymatic activities required to break down alcohol. The amino acid and inorganic mineral content was higher in leaves than in the shoots.
Antifungal Properties
Shimoyamada et al.(1990) have isolated saponins that have antifungal activity from A.officinalis extracts. They have determined that the antifungal properties of the saponins come from the waste products of asparagus processing. The compound was shown to have antifungal activity against fungi
including Candida albicans, Crytococcus albidus, Epidermophyton floccosum, Microsporum gypseum, and Trichophyton spp but was ineffective against other fungi such
as Rhizopus and Chaetomium.
Antitumor Activity
Cancer occurs when harmful mutated cells experience uncontrolled growth. Cells that experience uncontrolled growth usually form tumors, but those that mutate and then divide uncontrollably cause cancer. The global burden of cancer has made it necessary to find ways to inhibit the growth of malignant cells. Most cancers can be cured surgically before metastasis, but once metastasis has started, it is almost impossible to treat. Metastasis occurs when malignant cells escape from the original tumor and spread via blood and lymph vessels to other sites. It has been shown by Wang et al. (2012) that A. officinalis saponins (SSA) inhibit the viability of various cancer cells including breast, colon, and pancreatic cancer cells in a dose dependent manner. SSA also induces cancer cell apoptosis, which is the self destruction of cancer cells. SSA also inhibits cancer cell migration better than blocking cancer cell growth. It thus also inhibits cancer cell invasion because migrating cells’ cytoskeletal networks were seriously disrupted by them. Normal cells are usually round in shape, but they take on a sword shape after being disrupted; this shape reduces cell motility. Cell migration is regulated by Rho GTPases, and it has been shown that SSA targets the Rho GTPase signaling pathway. Wang et al., argue this potential use of asparagus waste can reduce environmental pollution and also potentially be used as anticancer and anti tumor medicines.
In vivo
Anti-diabetic Properties
Diabetes occurs when the body cannot efficiently break down sugar. This usually occurs when the body does not break down insulin or does not have insulin sensitive receptors, and thus there is a need to find treatments for this illness. Metabolism and metabolic studies were conducted by Hafizur et al. (2012) that demonstrated A. officinalis extracts can control blood glucose by improving beta cell function in type 2 diabetes induced rats. Streptozotocin was injected into rat pups to induce non obese diabetes. After the thirteenth week, the rats were treated with an extract of A. officinalis seeds before blood glucose, serum insulin, and total antioxidant status were measured. It was shown that the treatment with these extracts suppressed the elevated blood glucose level that would have been high in diabetic mice without insulin. The efficicacy of this extract depended on the dosage with a 500 mg/kg having higher efficacy than 250 mg/kg. The study thus shows that A.officinalis extract can have anti-diabetic effects by improving insulin secretion and beta cell function and antioxidant status.
Hypolipidaemic Effects
Hyperlipidaemia includes hypercholesterolaemia and hypertriclyceridaemia, and is a major risk factor in the development of cardiovascular diseases. There has been an emphasis on dietary plants that show the potential to lower cholesterol levels in plasma. A. officinalis has been shown to reduce levels of body weight gain, serum total cholesterol, and serum LDL cholesterol in mice with high cholesterol when they were administered a daily dose of 200 mg/kg for 8 weeks. HDL cholesterol levels were increased in mice treated
with aqueous extracts. Qu et al.(2009) found that the ethanolic (EEA) and aqueous (AEA) extracts of asparagus have strong hypolipidaemic and hepatoprotective properties that can be used in complementary and alternative medicinal treatments in combination with other hypoipidaemic drugs.
Clinical Studies
It has been found that Asparagus officinalis has been used as a medicinal plant for the treatment of several diseases. A.
officinalis is one of the many plants including broccoli,
butterhead lettuce, chickpea, dry beans, and spinach that are