Food as Medicine: Mustard (Brassica juncea and B. nigra, Brassicaceae)

HerbalEGram: Volume 14, Issue 3, March 2017 Editor’s Note: Each month, HerbalEGram highlights a conventional food and briefly explores its history, traditional uses, nutritional profile, and modern medicinal research. We also feature a nutritious recipe for an easy-to-prepare dish with each article to encourage readers to experience the extensive benefits of these whole foods. With this series, we hope our readers will gain a new appreciation for the foods they see at the supermarket and frequently include in their diets. The basic materials for this series were compiled by dietetic interns from Texas State University in San Marcos and the University of Texas at Austin through the American Botanical Council’s (ABC’s) Dietetic Internship Program, led by ABC Education Coordinator Jenny Perez. We would like to acknowledge Perez, ABC Special Projects Director Gayle Engels, and ABC Chief Science Officer Stefan Gafner, PhD, for their contributions to this project. By Hannah Baumana and Zachary Brownb a HerbalGram Associate Editor b ABC Dietetics Intern (TSU, 2015) Overview Mustard plants are herbaceous perennials (though often grown as annuals or biennials) and belong to the Brassicaceae, or cabbage, family.1 The three types of mustard most commonly consumed today are brown mustard (Brassica juncea), black mustard (B. nigra), and white mustard (Sinapis alba). This paper is concerned only with the brown and black species. Native to temperate regions in Europe, mustard was one of the continent’s first domesticated crops, and thereafter became a cultivated food crop in Asia, North Africa, and North America.2 All species yield edible leaves, while their seeds are used whole, powdered, or pressed to produce oil.1 Annually, the United States produces 160,000 tons of mustard seed.3 Mustard plants have alternate leaves with ruffled margins and produce the small, yellow four-petaled flowers typical of members of the Brassicaceae family (formerly referred to as the Cruciferae family due to the cross-like pattern of the four petals). Upon pollination, each seedpod elongates into an oblong fruit capsule that contains up to 20 spherical seeds, which can be dark brown or yellow depending on the species.4 Black mustard is sparsely branched and erect. It grows up to three meters in height and produces very small, pungent seeds (1.5 grams per 1,000 seeds) that are shed by the plant as the seedpod matures.1 Black mustard is grown for its edible greens in Argentina, Chile, and the United States, but it is rarely cultivated as a seed crop due to difficulties with the harvesting process and has largely been replaced by brown mustard because of this. Brown mustard, also known as Indian or Oriental mustard, originated in the Himalayan region of central Asia. Brown mustard grows 1-2 meters tall, has larger seeds (three grams per 1,000 seeds), and produces seedpods that are easier to mechanically collect and process. Brown mustard is commercially grown in North America, specifically in parts of the United States and Canada.3 Phytochemicals and Constituents Phytochemical differences in black mustard and brown mustard are minor, since B. juncea evolved from its ancestor B. nigra. The primary components of interest in mustard are the glucosinolates such as sinigrin, which are believed to be responsible for many of mustard’s health benefits.5 Mustard seed oil contains 90% allyl isothiocyanate (AITC). The seed contains 27% non-volatile oils (fixed oils), 30% proteins, and small amounts of lecithin, inositol, albumin, gums, mucilage, and pigments. Sinapine, an alkaloid, is also present in trace amounts. The fixed oils are composed of oleic, stearic, erucic, or brassic acids. Mustard seeds also contain terpenes, which have anti-inflammatory properties and are the primary constituents of mustard essential oil. Other constituents in significant amounts include flavonoids and other phenolic compounds. The concentrations of these compounds can vary widely based on the growing conditions of the mustard plant. Pathogenic attacks on the plant also result in an altered phytochemical profile. Thus, it is possible that the health effects of mustard can vary due to the different farming practices used to grow the mustard. It would be beneficial to standardize farming practices to maximize yields of specific plant chemicals.6 Mustard greens are nutrient dense and contain high amounts of vitamins, such as vitamin A, vitamin K, and vitamin C, and minerals, such as calcium. Mustard seeds contain fewer vitamins but are a good source of iron, calcium, magnesium, and other minerals. Mustard seeds are also a good source of omega fatty acids, as they contain an almost 1:1 ratio of omega-3 and omega-6 fatty acids. Both the seeds and greens can offer health-protective effects through their impressive nutrient profiles, although prepared mustard as a condiment should be used sparingly, since many commercial brands can contain high amounts of sodium.1 Historical and Commercial Uses The recorded use of mustard as a medicinal plant dates back to the first century CE in Greece, where the physician Dioscorides recommended the topical application of a mustard seed poultice to reduce inflammation in his herbal medicine encyclopedia De Materia Medica.7 In Unani literature (the Greco-Arabic system of traditional medicine), mustard seed is recommended for a variety of conditions, including neuralgia, epilepsy, sciatica, leprosy, gout, pleurisy, and pneumonia.5 In Ayurveda, the system of traditional medicine practiced for thousands of years in India, the therapeutic uses of mustard are well documented. The Ayurvedic practice considers mustard seed oil derived from the brown mustard plant to be pungent and warming, and documents external uses such as a massage oil and a hair tonic; for skin diseases like vitiligo; skin infections like acne; and hemorrhoids.8 Mustard seeds were processed into a paste and used as a poultice to treat internal conditions such as tumors of the thyroid gland and lymphadenitis (swelling of lymph nodes). Mustard seeds were also decocted in water and used as a poultice for cracked skin, leprosy, rheumatoid arthritis, acne, and as a rinse for mouth sores. Internally, mustard oil traditionally was used to lower blood lipid levels, reduce build-up of fat or adipose tissue, treat intestinal worms, and assist detoxification of the body. Mustard seeds were also included in traditional herbal formulas used to induce vomiting and cleanse the cranial cavity via nasal irrigation, and as a decoction in an enema therapy.8 Though mustard leaves were more commonly consumed as a vegetable, they were also used as an ingredient for steam fomentation and to cleanse the cranial cavity. Other ethnobotanical uses of the mustard plant exist in cultures around the world.1 In Africa, the roots are used as a galactagogue to stimulate milk production. Dried leaves and flowers are burned in Tanzania in spiritual rituals. The essential oil has been used to relieve constipation and as a counterirritant. In Java, the leaves are used internally to treat syphilis and stimulate blood flow to the pelvic area and topically to treat headaches. In Korea, the seeds are used for abscesses, colds, lower back pain, rheumatism, and stomach disorders. The oil of mustard has been used to treat skin eruptions and ulcers throughout Asia. In North America, black mustard has a history of use among indigenous tribes.9 It was used by the Cherokee to stimulate the appetite, treat fever and “nervous fever,” heal the kidneys, and treat various other diseases such as malaria. It was also used to treat palsy and asthma, and as a tonic for overall wellness. The Meskwaki used mustard due to its pungent nature to treat head colds. The Mohegan tribe applied mustard leaf poultices as an analgesic for body pains, headaches, and toothaches. The Shinnecock used it similarly to the Mohegan, but also mixed it with flour and water to induce vomiting. Brown mustard seed powder also has a widespread use as an emetic to treat acute and narcotic poisoning.10 Modern Research In recent studies, mustard has shown antitumor effects and other beneficial properties against chronic conditions, including diabetes, cardiovascular disease, weight gain, and neuropathic disease. It might also act as a protective agent against acute conditions such as fungal infection and influenza. Cytotoxic and Anti-Tumor Effects The anticancer effect of mustard may be due to the anti-proliferative activity of constituents such as sinigrin, the precursor to AITC. Many cytotoxicity studies have been performed in vitro to investigate how mustard and its constituents act against cancer cell proliferation. A hydrolyzed mustard seed powder that contained AITC caused cell cycle arrest and apoptosis (programmed cell death) in bladder cancer cell lines.11 This was further observed in rats, where an oral dose of the hydrolyzed mustard seed powder inhibited bladder cancer growth and blocked muscle invasion of cancerous cells. AITC specifically is thought to be selectively delivered to the bladder through urinary excretion. The mustard powder produced more significant results than pure AITC, suggesting that ingestion of the whole seed is more beneficial than ingestion of any isolated constituents. In an animal model, injections of mustard essential oil rich in AITC inhibited cell proliferation and blood vessel creation (angiogenesis, which is required for tumor growth).12 The oil also induced apoptosis, a pathway for cancer chemoprevention. Another study examined the effects of sinigrin on liver tumors in rats. This three-month study found that oral sinigrin administration significantly inhibited proliferation of tumor cells in the liver and reduced the number of tumors in the rat liver. The response was dose dependent, with the highest tumor suppression at 25 mg/kg of body weight. However, the lowest dose, 10 mg/kg, still caused a significant reduction of tumors on the liver surface compared to the positive control, reducing tumor size by half.13 An in vitro study examined the effects of several mustard extracts and found a dose-dependent protective response in human hepatocytes, colorectal cells, cervical cells, breast cancer cells, and larynx cells.5 The juice of the mustard leaf was also found to protect against induced DNA damage in human cells, again in a dose-dependent manner. These cancer chemopreventive effects were thought to be mediated not through inherent antioxidant properties of mustard extract, as is often seen with many plant materials, but by increasing expression of detoxification enzymes. Isothiocyanates may also decrease multidrug resistance in human cancer cell lines and inhibit the efflux (simply put, the removal of compounds from cells) of cancer-treating drugs, which enhances the effect of chemotherapy treatment. In an in vitro study, isolated compounds, including isothiocyanates and sulforaphane, increased the accumulation of chemotherapeutic drugs in multidrug resistant cancer cells through the inhibition of efflux of these drugs.14 Researchers also found that the isothiocyanates inhibited tumor formation in breast, colon, lung, and skin tissue. Diabetes, Cardiovascular Disease, and Neuropathic Effects Mustard leaves and seeds both can induce hypoglycemic effects in animals with type 2 diabetes. One rodent study found that administration of an extract made from mustard leaves significantly reduced lipid peroxidation, reduced free radicals, and ameliorated the damage caused by oxidative stress.15 Researchers speculated that mustard enhances glycolysis and glycogenesis, and decreases glycogenosis. These data were further confirmed by a follow-up study that also showed reduced levels of superoxide and nitrite/nitrates in a dose-dependent manner after oral administration of a mustard extract.16 Mustard may also delay or prevent the onset of diabetes in addition to mitigating its effects. A study examined the effects of feeding high-fructose diets to rodents for 30 days and found that the inclusion of mustard powder over the study period significantly decreased fasting serum glucose, insulin, and cholesterol levels, although not enough to normalize them.17 Researchers concluded that mustard powder may be beneficial for pre-diabetic patients and those who are genetically prone to the disease. Cardiovascular disease (CVD) is often studied in tandem with diabetes, as individuals with diabetes tend to suffer from CVD as well. One study examined the effects of two doses of mustard seed powder on serum cholesterol and triglycerides in diabetic rats.18 The lower dose did not significantly affect these markers; however, a higher dose (8 g/kg of body weight) significantly and consistently lowered both. The authors suggested that mustard might mimic or enhance the effectiveness of insulin, lowering the necessary amount and reducing insulin’s anabolic effect. There are often neurological complications associated with diabetes. In a rat model, researchers examined the effects of an ethanol mustard extract and found dose-dependent improvements in brain chemistry and cognitive function, and speculated that non-diabeties-induced neurological problems could be improved with mustard consumption or supplementation.19 The effect of mustard on the depletion of neurotransmitters norepinephrine, serotonin, and dopamine was further researched.20 Mustard was found to compensate for depleted levels of neurotransmitters in the brain, resulting in improvement of behavioral outcomes such as feelings of helplessness and despair, as well as impaired locomotion. Mustard’s rich polyphenol content may be the source of its therapeutic effects on cognitive issues. Antimicrobial Properties Mustard has antimicrobial and antiviral properties and shows protective effects against microbe- and virus-induced damage. One rodent study on viral hepatitis found that mustard extract protected against liver and kidney damage. The mechanism of this protective action is thought to be related to the anti-inflammatory activity of the compounds in mustard such as terpenes.21 This is of specific interest because it shows that the protective properties of mustard go beyond antibiotic properties and may protect against viruses as well. Mustard has also been shown to have antifungal properties. Mustard essential oil was able to inhibit or delay the growth of several types of fungi and prevent further growth even if mustard essential oil was in contact with the fungi through vapors.22 Furthermore, mustard was found to recognize the structural differences of microbes and targeted sphingolipids, specific regulators of pathogenicity unique to fungal pathogens.23 Consumer Considerations Mustard as a food generally is considered safe. There are no known nutrient-drug interactions with mustard, although high levels of vitamin K in the leaves could interact with certain blood-thinning medications such as warfarin due to vitamin K’s blood-coagulating properties. The vitamin K content could also be a concern to individuals with existing untreated thyroid issues or an iodine deficiency. Due to the high oxalate content of the leaves, those with a history of oxalate-containing kidney stones may wish to limit their intake of mustard leaves.24 Mustard essential oil can be highly irritable to the skin and mucous membranes. It is not recommended to use mustard oil either internally or externally. However, mustard oil must be specifically extracted and these side effects are not a concern when consuming the condiment, seeds, or leaves.25 While there is little concern about adulteration of culinary mustard, there is a history of adulterating mustard seed oil with argemone (Argemone mexicana, Papaveraceae) oil. In 1998, 2,300 people were affected and 41 people died from adulterated mustard oil in India, resulting in a complete ban of mustard seed oil.26 The ban was subsequently lifted after the adulteration was discovered and corrected. However, mustard seed oil for edible consumption is not recognized as safe in the United States, Canada, and European Union due to its high erucic acid content.27 Nutrient Profile28 Macronutrient Profile: (Per 1 cup [approx. 56 grams] chopped mustard greens, raw) 15 calories 1.6 g protein 2.6 g carbohydrate 0.2 g fat Secondary Metabolites: (Per 1 cup [approx. 56 grams] chopped mustard greens, raw) Excellent source of: Vitamin K: 144.2 mcg (180.3% DV) Vitamin C: 39.2 mg (65.3% DV) Vitamin A: 1,693 IU (33.9% DV) Very good source of: Manganese: 0.3 mg (15% DV) Good source of: Dietary Fiber: 1.8 g (7.2% DV) Calcium: 64 mg (6.4% DV) Potassium: 215 mg (6.1% DV) Vitamin E: 1.13 mg (5.6% DV) Iron: 0.92 mg (5.1% DV) Also provides: Vitamin B6: 0.1 mg (5% DV) Magnesium: 18 mg (4.5% DV) Riboflavin: 0.06 mg (3.5% DV) Thiamin: 0.05 mg (3.3% DV) Phosphorus: 32 mg (3.2% DV) Niacin: 0.45 mg (2.3% DV) Folate: 7 mcg (1.8% DV) DV = Daily Value as established by the US Food and Drug Administration, based on a 2,000-calorie diet. Recipe: Saag Paneer Adapted from Anita Jaisinghani29 Ingredients: 1/4 cup ghee or neutral vegetable oil, divided 1 medium yellow onion, chopped Salt and pepper to taste 3 garlic cloves, minced 2 serrano chilies, stems and seeds removed, minced 2-inch piece of ginger, peeled and minced/grated 1 pound of mustard greens, stems removed and leaves chopped 1 pound baby spinach leaves 2 teaspoons garam masala spice blend 3/4 cup heavy cream or plain, unsweetened yogurt 1 pound paneer or halloumi cheese, diced into 1-inch pieces Directions: In a large saucepan, heat 3 tablespoons of the ghee or oil. Add the onion and season with salt and pepper. Cook over moderately low heat, stirring occasionally, until soft and golden brown, about 20 minutes. Add the garlic, chilies, and ginger. Cook over moderate heat, stirring occasionally, until softened, about 5 minutes. Stir in the garam masala and cook until fragrant. In batches, add the mustard greens and spinach, letting each batch wilt before adding more. Season with salt and pepper. In a food processor, pulse half of the greens with half of the heavy cream or yogurt until finely chopped. Return to the saucepan and repeat with the remaining greens and cream/yogurt. Alternatively, use an immersion blender to process the greens and dairy in the saucepan. Keep the saag warm over very low heat, stirring occasionally. In a medium nonstick skillet, heat 1/2 tablespoon of the ghee or oil over moderate heat. Add half of the paneer and cook, turning once, until golden brown, about 5 minutes. Transfer to a paper towel-lined plate to drain. Repeat with the remaining ghee and paneer. Fold the paneer into the saag and cook over low heat until warmed through, 2 to 3 minutes. Season with salt and pepper. Serve with steamed basmati rice. References Duke J. Handbook of Energy Crops. Unpublished; 1983. 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Antifungal activity of plant defensin AFP1 in Brassica juncea involves the recognition of the methyl residue in glucosylceramide of target pathogen Candida albicans. Current Genet. 2014;60(2):89-97. Murray M, Pizzorno J, Pizzorno L. The Encyclopedia of Healing Foods. New York, New York: Atria Books; 2014. Tisserand T, Young R. Essential Oil Safety. 2nd ed. London, UK: Churchill Livingstone; 2014. Babu CK, Khanna SK, Das M. Adulteration of mustard cooking oil with argemone oil: do Indian food regulatory policies and antioxidant therapy both need revisitation? Antioxid Redox Signal. 2007;9(4):515-525. Agriculture and Consumer Protection. SECTION 2: Codex Standards for Fats and Oils from Vegetable Sources. Food and Agriculture Organization of the United Nations. 1999. Available at: www.fao.org/docrep/004/y2774e/y2774e04.htm. Accessed February 22, 2017. Basic report: 11270, mustard greens, raw. United States Department of Agriculture Agricultural Research Service Available at: https://ndb.nal.usda.gov/ndb/foods/show/3018. Accessed February 22, 2017. Jaisinghani A. Mustard Greens Saag Paneer. Food and Wine. January 2017. Available at: www.foodandwine.com/recipes/mustard-greens-saag-paneer. Accessed February 22, 2017.