HerbalEGram: Volume 14, Number 4, April 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 (TSU) in San Marcos and the University of Texas (UT) 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 Bauman^a and Mariam Alhado^b

^a HerbalGram Associate Editor

^b ABC Dietetics Intern (TSU, 2017)

Overview

Spinach (Spinacia oleracea, Chenopodiaceae) is an annual plant that grows up to 23 inches tall (60 cm).¹ Spinach plants produce an edible rosette and toothed, fleshy leaves. There are two main types of spinach: crinkled savory-leaf spinach and smooth or flat-leaf spinach.² Spinach leaves are fleshy, deep green, and rich in essential nutrients and phytochemicals. Spinach requires deep and nitrogen-rich soil to grow, and prefers a cool climate, with spring and autumn being optimal growth seasons for the leaves.^2,3 The hot weather of summer may cause the spinach to bolt quickly, which causes the leaves to deteriorate.³ The plant produces greenish-yellow flowers when ready to set seed.⁴

Spinach is native to southwest Asia, in the area of present-day Iran.³ Spinach cultivation spread to China in 647 BCE, and spread across Europe by the 12th century CE. Now, spinach is cultivated throughout the world in temperate climate zones. In the United States, California is the largest producer of spinach, followed by Arizona and New Jersey. The annual per capita consumption of spinach in the United States was estimated to be 1.7 pounds in 2014.⁵

Phytochemicals and Constituents

Spinach is one of the most nutritious leafy vegetables, and ranks second behind kale (Brassica oleracea var. acephela, Brassicaceae) in total carotenoids and folate content.⁶ Spinach is high in protein and low in carbohydrates and fat.

The plant is a nutrient-dense source of vitamins and minerals, and maintains its nutritional value well after cooking. Spinach provides an array of B vitamins, which are important for carbohydrate metabolism, the nervous system, and the brain. Spinach contains other important minerals including calcium, magnesium, zinc, and selenium, and is a significant source of potassium, copper, iodine, and iron.⁷ It also contains abundant amounts of vitamins A, K, and C.⁷

The flavonoid, phenolic acid, and carotenoid content of spinach makes it a healthy, therapeutic food. These compounds are effective at neutralizing free radicals in the body and are able to protect the body from damage and disease by reducing inflammation.

The two major carotenoids present in spinach leaves are lutein and beta-carotene,⁸ and they compose more than 65% of the total carotenoids content. Lutein may help prevent vision loss from age-related degenerative disorders such as macular degeneration and cataracts.⁹ A yellow pigment, lutein is found in high amounts in the retina and absorbs blue light emitted by back-lit devices such as smart phones and computer screens. Other carotenoids in spinach include violaxanthin and neoxanthin.⁸

The carotenoids in spinach are very delicate and highly susceptible to degradation over time. Post-harvest handling of spinach from field to freezer does alter the phytochemical profile of the leaves. In one study, storing fresh spinach leaves for 24 hours at 39°F (4°C) did not impact the carotenoids content in fresh spinach.⁸ However, storing fresh spinach for 72 hours at the same temperature resulted in a reduction of the carotenoids content by almost 15%. Blanching fresh leaves for two minutes at 212°F (100°C) followed by freezing effectively preserved the carotenoid content of spinach.

Historical and Commercial Uses

Historically, spinach leaves have been used as a laxative, diuretic, antidote against poison or infection, and as a treatment for asthma and other breathing difficulties, sore throat, and kidney stones.¹ Spinach also has potential effects against hyperglycemia and inflammation. The seeds were used to control fever, to address back pain, and as a diuretic. In the Indian traditional medicine, the plant is known as palak and was used to treat liver injury or infection and jaundice. Spinach was prescribed and used in traditional Iranian medicine as an antidepressant.¹⁰ Due to its high iron and chlorophyll content, spinach often is used as a therapeutic food for patients with anemia.¹¹

Spinach leaves are available commercially fresh, frozen, or canned. Depending on the spinach cultivar and method of preservation, the nutrients and phytochemical profile of spinach may vary.² Spinach leaves can be eaten fresh or cooked. Several popular spinach-based dishes are said to be prepared “a la Florentine,” supposedly in honor of Catherine de Medici (1519-1589), who was born in Florence and introduced the vegetable to the French court upon her marriage to King Henry II.¹²

Modern Research

There are limited data regarding the effect of whole spinach leaves on diseases, metabolic pathways, and conditions. Most of the available literature reports the effects of leaf extracts or specific isolated phytonutrient components.

Oxidative Damage and Inflammation

The antioxidant content of spinach leaf, which contains high amounts of vitamins A and C, suggests protective effects against damage from cellular oxidation. A mouse study found that supplementation with 1,100 mg/kg per day of methanolic spinach leaf extract significantly decreased radiation-induced lipid peroxidation in the liver.¹³ This study further demonstrated that the leaf extract decreased the negative impact of radiation on glutathione levels.

A 2017 rat study used a different methanolic spinach leaf extract with high levels of lutein, luteolin, quercetin, and coumarin.¹⁴ High-performance liquid chromatography analysis of the extract confirmed the presence of these compounds in active amounts. The study reported that intraperitoneal injection of the extract showed a protective anti-inflammatory effect in mice that were given isoproterenol to induce a heart attack. Spinach extract intake led to changes in activities of multiple enzymes, including paraoxonase, lecithin-cholesterol acyltransferase, C-reactive protein, myeloperoxidase, and caspase-3. Furthermore, the levels of pro-inflammatory cytokines in the heart tissue were significantly lower in mice pretreated with spinach extract than the control group. These results indicate the potential protective effects of spinach against inflammation and atherogenesis (the formation of abnormal fatty masses in arterial walls) when used as a concentrated leaf extract.

Cancer Chemoprevention

An in vitro study demonstrated that neoxanthin significantly suppressed inflammation and proliferation of prostate cancer cells.¹⁵ Additionally, in a bacteria-based model, flavonoids found in spinach leaves showed anti-mutagenic potential.¹⁶

A study in mice reported that the antioxidants extracted from spinach leaves have protective effects against benign epithelial tumors.¹⁷ The potential mechanism of action was linked to the direct and indirect abilities of antioxidant compounds in spinach leaves to act as free-radical scavengers that inhibit the progression of carcinogenesis.

The abundant glycolipids in spinach leaves were found to possess inhibitory effects against gastric cancer cell and promyelocytic leukemia cell proliferation in vitro.¹⁸ These findings are considered positive, but preliminary, results of the potential therapeutic effects of spinach glycolipids to prevent cancer proliferation.

Cardiovascular Disease

In a semi-randomized crossover study in humans, the consumption of a fortified spinach beverage resulted in a significant increase in plasma nitrate concentration, which correlated with lower diastolic blood pressure within 150 minutes post-consumption and persisted for five hours thereafter.¹⁹ This study suggests the possible therapeutic uses of spinach as a safe alternative and effective carrier for nitrate medications.

Supplementation

Spinach, like most dark, leafy greens, contains a high amount of folate: 100 grams of raw spinach provides almost half of an average person’s daily recommended intake.⁷ Daily intake of spinach for three weeks showed a significant increase in plasma folate concentrations, and processing spinach leaves did not affect the bioavailability of folate when compared to fresh whole-leaf spinach.²⁰ Frozen whole-leaf spinach, minced spinach, and liquefied spinach have similar effects in terms of increasing plasma folate concentration.

Researchers currently are examining the potential benefits of fortifying flour with dehydrated spinach, with a goal to improve total folate content in bread.²¹ Fortification of white bread and whole grain bread with spinach (40 g spinach per 100 g of other ingredients) increased the total folate content, despite the effect of processing factors such as kneading and baking.

Diabetes

Spinach leaves contain many beneficial compounds such as vitamin C, iron, zinc, folic acid, polyphenols, and fatty acids. These compounds have protective effects topically as well as internally.²² In a study, diabetic rats were fed an aqueous spinach leaf extract to determine its effects on wound healing. The results showed that the spinach group had better wound-healing outcomes as indicated by significant improvements in epithelial and granulation tissue formation and blood vessels. These results indicate the potential beneficial effects of supplementation with spinach juice or other types of spinach extracts to treat wounds and ulcers in patients with diabetes.

Consumer Considerations

In August 2008, The US Food and Drug Administration (FDA) announced that it would allow the irradiation of spinach in order to kill the harmful bacteria Escherichia coli and Salmonella after numerous outbreaks of foodborne illness.²³ Strains of E. coli have the ability to survive and multiply in the absence of an animal host when soil, water, and plants become contaminated. Pathogenic bacteria can grow inside the leaf tissues of spinach, rendering typical antimicrobial surface treatments ineffective. Uniformity of crop management practices as well as environmental factors not only impact the vegetable quality, but also the survival rate of E. coli in the soil and on the leaf crops.²⁴ There are concerns, however, about the irradiation of food crops. Research indicates that the process generates harmful reactive oxygen species and decreases the phytonutrient content of the food in the process of eliminating foodborne pathogens.²³

The primary source of spinach leaf contamination with heavy metals is from pesticides containing lead arsenate, environmental pollution, contaminated irrigation water and rainwater, and runoff from nearby areas treated with plant pesticides and fertilizers.²⁵ Leaf crops are most sensitive to lead contamination and bioaccumulation. Commercially farmed spinach is most susceptible to heavy metal and pathogen contamination due to the reliance on pesticides and poor land management techniques such as continual replanting in contaminated soil.

Caution with spinach consumption may be warranted in populations susceptible to kidney stones. Spinach is one of a number of foods that naturally contains oxalates.³ The oxalate content in spinach is estimated to be about 0.77 mg/100 g. Oxalates bind to many minerals, including calcium, zinc, and magnesium, inhibiting their absorption.²⁶ Approximately 80% of kidney stones contain calcium and predominately consist of calcium oxalate.²⁷ High levels of urinary oxalate are a major risk factor and precursor to the formation of calcium oxalate kidney stones. Observational data indicate an inverse relationship between dietary calcium and the risk of kidney stone formation, since dietary calcium may bind to oxalates in the gut, and thereby limit the absorption of intestinal oxalates and subsequent excretion of urinary oxalates. However, a study of three diverse populations noted only a small association between oxalate and spinach consumption and the risk of kidney stone formation.²⁷

Nutrient Profile⁷

Macronutrient Profile: (Per 100 grams raw spinach)

23 calories

2.9 g protein

3.6 g carbohydrate

0.4 g fat

Secondary Metabolites: (Per 100 grams raw spinach)

Excellent source of:

Vitamin K: 482.9 mcg (603.6% DV)

Vitamin A: 9377 IU (187.5% DV)

Folate: 194 mcg (48.5% DV)

Vitamin C: 28.1 mg (46.8% DV)

Manganese: 0.9 mg (45% DV)

Magnesium: 79 mg (19.8% DV)

Potassium: 558 mg (15.9% DV)

Iron: 2.7 mg (15% DV)

Very good source of:

Riboflavin: 0.19 mg (11.2% DV)

Vitamin E: 2.03 mg (10.1% DV)

Vitamin B6: 0.2 mg (10% DV)

Calcium: 99 mg (9.9% DV)

Dietary Fiber: 2.2 g (8.8% DV)

Good source of:

Thiamin: 0.08 mg (5.3% DV)

Also provides:

Phosphorus: 49 mg (4.9% DV)

Niacin: 0.72 mg (3.6% DV)

DV = Daily Value as established by the US Food and Drug Administration, based on a 2,000-calorie diet.

Recipe: Savory Spinach-Onion Pastry

Courtesy of Mariam Alhado

Ingredients:

• 3 cups frozen chopped spinach, thawed
• 1 yellow onion, thinly sliced
• 1/4 cup freshly-squeezed lemon juice
• 1 tablespoon extra-virgin olive oil
• 1 tablespoon ground sumac or za’atar spice blend
• Salt to taste
• 1 package frozen puff pastry

Directions:

1. Heat oven to 350°F. Using several layers of paper towels, squeeze as much excess water from the frozen spinach as possible.
2. In a large bowl, combine spinach, onion, lemon juice, olive oil, sumac, and salt and form a uniform mixture.
3. Roll out the pastry until it is smooth and of even thickness. Divide into three-inch squares. Add a few tablespoons of the spinach mixture into the center of each square, then fold the corners in and press to seal.
4. Arrange the pastries on a baking sheet and bake for 15-20 minutes, until golden brown and heated through.

References

1. Metha D, Belemkar S. Pharmacological activity of Spinacia oleracea Linn.: A complete overview. Asian Journal of Pharmaceutical Research and Development. 2014;2(1):83-93.
2. Van Wyk B-E. Food Plants of the World. Portland, OR: Timber Press; 2006.
3. Barzegar M, Erfani F, Jabbari A, Hassandokht MR. Chemical composition of 15 spinach (Spinacea oleracea L.) cultivars grown in Iran. Italian Journal of Food Science. 2007;19(3):309-318.
4. Spinacia oleracea. Missouri Botanical Garden website. Available at: www.missouribotanicalgarden.org/PlantFinder/PlantFinderDetails.aspx?kempercode=e819. Accessed March 22, 2017.
5. Naeve L. Spinach. Agricultural Marketing Resource Center website. August 2015. Available at: www.agmrc.org/commodities-products/vegetables/spinach/. Accessed March 22, 2017.
6. Pandrangi S, LaBorde LF. Retention of folate, carotenoids, and other quality characteristics in commercially packaged fresh spinach. Journal of Food Science. 2004;69(9):C702-C707.
7. Basic Report: 11457, Spinach, raw. United States Department of Agriculture, Agricultural Research Service website. Available at: https://ndb.nal.usda.gov/ndb/foods/show/3167. Accessed March 22, 2017.
8. Bunea A, Andjelkovic M, Socaciu C, et al. Total and individual carotenoids and phenolic acids content in fresh, refrigerated and processed spinach (Spinacia oleracea L.). Food Chemistry. 2008;108(2):649-656.
9. Weil A. Lutein: good for your eyes and heart? Andrew Weil, MD website. May 2, 2002. Available at: www.drweil.com/health-wellness/body-mind-spirit/vision/lutein-good-for-your-eyes-and-heart/. Accessed March 22, 2017.
10. Tavakkoli-Kakhki M, Motavasselian M, Mosaddegh M, et al. Omega-3 and omega-6 content of medicinal foods for depressed patients: implications from the Iranian Traditional Medicine. Avicenna J Phytomed. 2014;4(4):225-230.
11. Grieve M. A Modern Herbal: The Medicinal, Culinary, Cosmetic and Economic Properties, Cultivation and Folk-lore of Herbs, Grasses, Fungi, Shrubs, & Trees with All Their Modern Scientific Uses. Vol 2. Chelmsford, MA; 1971.
12. Bauer BT. Just ask: An eggs Florentine mystery, cracked. Saveur. March 15, 2011. Available at: www.saveur.com/article/Kitchen/Mystery-Cracked. Accessed March 22, 2017.
13. Bhatia AL, Jain M. Spinacia oleracea L. protects against gamma radiations: a study on glutathione and lipid peroxidation in mouse liver. Phytomedicine. 2004;11:607-615.
14. Vutharadhi S, Jolapuram U, Kodidhela LD. Nutraceutical inherent of Spinacia oleracea Linn. methanolic leaf extract ameliorates isoproterenol induced myocardial necrosis in male albino Wistar rats via mitigating inflammation. Biomedicine & Pharmacotherapy. 2017;85:239-247.
15. Asai A, Terasaki M, Nagao A. An epoxide-furanoid rearrangement of spinach neoxanthin occurs in the gastrointestinal tract of mice and in vitro: formation and cytostatic activity of neochrome stereoisomers. The Journal of Nutrition. 2004;134(9):2237-2243.
16. Edenharder R, Keller G, Platt KL, Unger KK. Isolation and Characterization of Structurally Novel Antimutagenic Flavonoids from Spinach (Spinacia oleracea). Journal of Agricultural and Food Chemistry. 2001;49(6):2767-2773.
17. Nyska A, Boorman G, Spalding J, et al. Erratum: Topical and oral administration of the natural water-soluble antioxidant from spinach reduces the multiplicity of papillomas in the Tg.AC mouse model (Toxicology Letters (2001) 122 (33-44) PII: S0378427401003459). Toxicology Letters. 2001;123(2-3):237.
18. Kuriyama I, Musumi K, Yonezawa Y, et al. Inhibitory effects of glycolipids fraction from spinach on mammalian DNA polymerase activity and human cancer cell proliferation. The Journal of Nutritional Biochemistry. 2005;16(10):594-601.
19. Jonvik KL, Nyakayiru J, Pinckaers PJ, Senden JM, van Loon LJ, Verdijk LB. Nitrate-rich vegetables increase plasma nitrate and nitrite concentrations and lower blood pressure in healthy adults. The Journal of Nutrition. 2016;146(5):986-993.
20. Castenmiller JJM, van de Poll CJ, West CE, Brouwer IA, Thomas CM, van Dusseldorp M. Bioavailability of folate from processed spinach in humans: Effect of food matrix and interaction with carotenoids. Ann Nutr Metab. 2000(4):163.
21. López-Nicolás R, Frontela-Saseta C, Barado-Piqueras A, Perez-Conesa D, Ros-Berruezo G, González-Abellán R. Folate fortification of white and whole-grain bread by adding Swiss chard and spinach: Acceptability by consumers. LWT – Food Science and Technology. 2014;59(1):263-269.
22. Rahati S, Eshraghian M, Ebrahimi A, Pishva H. Effect of spinach aqueous extract on wound healing in experimental model diabetic rats with streptozotocin. Journal of the Science of Food and Agriculture. 2016;96(7):2337-2343.
23. Lester GE, Hallman GJ, Pérez JA. γ-irradiation dose: Effects on baby-leaf spinach ascorbic acid, carotenoids, folate, α-tocopherol, and phylloquinone concentrations. Journal of Agricultural and Food Chemistry. 2010;58(8):4901-4906.
24. Gutiérrez‐Rodríguez E, Gundersen A, Sbodio AO, Suslow TV. Variable agronomic practices, cultivar, strain source and initial contamination dose differentially affect survival of Escherichia coli on spinach. Journal of Applied Microbiology. 2012;112(1):109-118.
25. Tóth T, Kopernická M, Stanovič R, et al. Content of mercury and lead in leaves of spinach (Spinacia oleracea, L.). Journal of Microbiology, Biotechnology and Food Sciences. 2014;3(Special Issue 3):298-299.
26. Bonsmann SSG, Walczyk T, Renggli S, Hurrell RF. Oxalic acid does not influence non haem iron absorption in humans: a comparison of kale and spinach meals. European Journal of Clinical Nutrition. 2008;62(3):336-341.
27. Taylor EN, Curhan GC. Oxalate intake and the risk for nephrolithiasis. Journal of the American Society of Nephrology. 2007;18(7):2198-2204.