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CHAPTER

18

Almond (Prunus dulcis) Seeds and Oxidative Stress


Arash Mirrahimi1, 3, Korbua Srichaikul1, 3, Amin Esfahani1,3, Monica S. Banach1, 5, John L Sievenpiper1, 6, Cyril W.C. Kendall1,3, 7, David J.A. Jenkins1, 2, 3,4 1 Clinical Nutrition & Risk Factor Modication Center, 2 Department of Medicine, Division of Endocrinology and Metabolism, St Michaels Hospital, Toronto, Ontario, Canada 3 Department of Nutritional Sciences, 4 Department of Medicine, 5 Department of Pharmaceutical Sciences, Faculty of Medicine, University of Toronto, Toronto, Ontario, Canada 6 Department of Pathology and Molecular Medicine, Faculty of Health Sciences, McMaster University, Hamilton, Ontario, Canada 7 College of Pharmacy and Nutrition, University of Saskatchewan, Saskatoon, Saskatchewan, Canada

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CHAPTER OUTLINE
Introduction 161 Botanical Description 162 Historical Cultivation and Usage 162 Present-Day Cultivation and Usage 162 Applications to Health Promotion and Disease Prevention 163 Adverse Effects and Reactions (Allergies and Toxicity) 165 Summary Points 165 References 165

LIST OF ABBREVIATIONS
BMI, body mass index CHD, coronary heart disease CVD, cardiovascular disease LDL, low-density lipoprotein MUFA, monounsaturated fatty acid ROS, reactive oxidative species

INTRODUCTION
The word almond, sometimes used to dene the shape of objects, comes from the Greek amygdala, which literally refers to the well known seed. Though the commonly used term nut
Nuts & Seeds in Health and Disease Prevention. DOI: 10.1016/B978-0-12-375688-6.10018-0 Copyright 2011 Elsevier Inc. All rights reserved.

PART 2 Effects of Specic Nuts and Seeds

refers to a wide range of seeds, based on botanical denitions almonds are not actually true nuts (Rushforth, 1999). While hazelnuts meet the botanical denition of nuts, almonds (along with pistachios and walnuts) are seeds of drupe fruits. Despite this inconsistency, these variable seeds have been clustered together under the collective term tree nuts. Almonds have historically and culturally been associated with good health, in India with good brain health, and in China with female beauty. Years of research have come to validate some of the age-old beliefs about these seeds. The various bioactive components and the unique macronutrient prole of nuts have been linked to lowering oxidative stress and inammation, improving lipid proles (Sabate et al., 2003), endothelial function (Ros, 2009), and blood pressure (Estruch et al., 2006). The ability of these seeds to improve the blood lipid prole and assist in diabetes management (Kris-Etherton et al., 2001; Lovejoy et al., 2002; Josse et al., 2007; Kendall et al., 2010), as well as reducing coronary heart disease (CHD) risk, has progressively become more established and considered as therapeutic (Ternus et al., 2006). Furthermore, with increasing rates of chronic diseases (including diabetes and cancer), known for causing greater levels of oxidative stress, the antioxidant effects of almonds are, now more than ever, of particular interest.

BOTANICAL DESCRIPTION
The almond is the seed of Prunus Dulcis, a small deciduous species of tree (4e10 m tall). The Prunus Dulcis drupe consists of an outer hull (exocarp) and a hard shell (endocarp) with the seed inside. Almond trees are not immediately productive, and only bear fruit after 5 years. It is in autumn, 7 to 8 months after owering, that the fruit becomes mature (Grifths & Anthony, 1992; Rushforth, 1999).

HISTORICAL CULTIVATION AND USAGE


162 Prunus Dulcis is native to regions of the Middle East with Mediterranean climates. The wild form of domesticated almonds grows in parts of the Levant, suggesting that almonds must rst have been cultivated in this region. The fruit of the wild form contains the glycoside amygdalin, which is transformed into hydrogen cyanide upon iniction of injury to the seed. Domesticated almonds are not toxic due to a common genetic mutation resulting in the absence of glycoside amygdalin, and this mutant was grown by early farmers. Almonds are believed to have been one of the earliest domesticated fruit trees (Zohary & Maria, 2000). Domesticated almonds appear to have been cultivated as early as the Early Bronze Age (3000e2000 BC) of the Near East. An archaeological example of almond consumption, likely imported from the Levant, is the fruit found inTutankhamuns tomb in Egypt (c. 1325 BC) (Zohary & Maria, 2000). The almond has since been spread by humans along the Mediterranean shores into northern Africa, southern Europe, and, more recently, other parts of the world, including California (Rieger, 2006). Almonds have been an integral part of the diet in many of the Levant region cultures, being frequently used in pastries and other foods. For centuries, almonds have also been utilized therapeutically e both the wild variant (bitter) and the domesticated variant (sweet). For example, sweet almond oil, obtained from the dried kernel of sweet almonds, has traditionally been used for massage therapy, and medicinally ingested in the Greco-Persian system of medicine.

PRESENT-DAY CULTIVATION AND USAGE


The global production of almonds is around 1.7 million tonnes annually, with the USA (41%), Spain (13%), Syria (7%), Italy (6%), Iran (6%), and Morocco (5%) being the major producers, according to Food and Agriculture Organization (FAO). In the United States, production is mainly in California, with almonds being Californias third leading agricultural product. India imports over 94% of its almond consumption, and is the largest global and US market for in-shell almonds. Interestingly, the pollination of Californias almonds is the largest annually managed pollination event in the world; approximately half of all USA beehives

CHAPTER 18 Almonds and Oxidative Stress

(1 million beehives) are trucked in to the almond groves in February for this task. Pollination of almonds has been heavily impacted by the colony collapse disorder affecting the bee population globally. In 2006, because of two cases of Salmonella traced to almonds, the Almond Board of California proposed pasteurization of almonds available to the public; the USDA has approved this as part of the almond distribution process. Almonds continue to be used in various foods, but they have now become of particular interest in nutraceuticals as a means of therapy. They have been linked to disease prevention and management in numerous studies. An example of almond incorporation into present-day diets is the use of almond milk. Almond milk, a dairy milk substitute, is processed from almonds, and makes an efcient and well-liked soy-free choice analog for lactose-intolerant people and for vegans. More innovative methods of incorporating almonds in diets as healthy alternatives continue to be explored and developed. Recently, a low carbohydrate nut-bread recipe was conceived at the St Michaels Hospital Clinical Nutrition and Risk Factor Modication Center in Toronto, and this, due to its high palatability and benecial nutrient prole, was used in the successful EcoAtkins weight loss and cholesterol lowering trial (see Table 18.1 for the recipe) (Jenkins et al., 2009).

APPLICATIONS TO HEALTH PROMOTION AND DISEASE PREVENTION


At one time, nuts (including almonds) were considered to be unhealthy foods in western societies due to their high fat content. This perception has since changed, with the determination of the fatty acid prole of almonds and other nuts, as well as the association of their consumption with reduced BMI and their inclusion in weight-maintaining diets (Bes-Rastrollo et al., 2009). The metabolic benets of almonds stem from their low saturated fat and high monounsaturated fatty acid (MUFA, regarded as a healthy fat) content, as well as their vegetable protein, ber, phytosterols, polyphenols, vitamins, and minerals (Table 18.2). It has been proposed that the almond bioactive compounds may help lower the risk factors for cardiovascular disease (CVD) by improving endothelial function (Ros, 2009), blood pressure (Estruch et al., 2006), and the serum lipid prole (Kris-Etherton et al., 2001; Lovejoy et al., 2002; Sabate et al., 2003; Kendall et al., 2010), in addition to lowering oxidative stress (Kendall et al., 2010) and inammation (Ros, 2009; Kendall et al., 2010).

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TABLE 18.1 Recipe for Low Carbohydrate Bread


Mix all of the ingredients below together in a large bowl, using a wooden spoon or your hands l Let it rest for 10 minutes l Continue to knead on a at surface, using up all remaining nuts and gluten, before transferring dough to a loaf pan (or shape into two round loaves, and place on a baking sheet) l Let dough rise for about 20 minutes or so  l Bake for 30 minutes at 300 F. l Keep an eye on the loaves, baking them until they are lightly browned on top. Ingredients: 180 g ground almonds (13/4 cups) 180 g ground, toasted hazelnuts (13/4 cups) 220 g gluten our (12/3 cups) 10 g sugar (2 tsp) 8 g salt (1 tsp) 16 g instant yeast (1 tbsp) 20 g psyllium ( cup) Add: 400 g warm water (12/3 cups)
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Ideally, all ingredients should be weighed, but if you dont have a scale, approximate volumes are provided.

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TABLE 18.2 Constituents of Almond Seeds


Nutrients* Energy (kcal) Protein (g) Fat (g) SFAs (g) MUFAs (g) PUFAs (g) Carbohydrate (g) Fiber (g) Sugars (g) a-tocopherol (mg) b-tocopherol (mg) g-tocopherol (mg) D-tocopherol (mg) Selenium (mg) Vitamin C (mg) Thiamin (mg) Folate (mg) Arginine (g) Flavanoids and/or polyphenols Almond (Prunus Dulcis) 575 21.2 49.4 3.7 30.89 12.1 21.7 12.2 3.89 26.22 0.29 0.65 0.05 2.5 0 0.21 50 2.45 EGC, cyanidin, GCG, EC, CIsorhamnetin 3-O-glucoside, isorhamnetin 3-O-rutinoside, C, kaempferol 3-o-rutinoside, EC, quercetin 3-O-galactoside, isorhamnetin 3-O-galactoside

*Estimates are based on United States Department of Agriculture (USDA) National Nutrient Database standard references; values

are given per 100 grams. All approximations are based on different numbers of data points.

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Almonds have also been linked to the risk of developing type 2 diabetes. According to the American Diabetes Association, glycemic control is of crucial importance for the prevention and management of diabetes (American Diabetes Association, 2007). Evidence suggests that when eaten alone or in combination with mixed meals, the low available carbohydrate content of nuts can help lower the postprandial glucose and insulin responses, and, as such, play a benecial role in glycemic control (Josse et al., 2007; Kendall et al., 2010). Moreover, it has been suggested that high MUFA consumption can also improve glycemic control (Kendall et al., 2010), possibly by displacing the carbohydrates and effectively decreasing the glycemic load. Since hyperglycemia is a major cause of oxidative stress in diabetic patients (Brownlee, 2001), these benets of almond consumption may have considerable potential in reducing reactive oxidative species (ROS) through reducing the glycemic excursions of foods consumed with almonds (Monnier et al., 2006; Kendall et al., 2010). ROS have been associated with multiple disease states, including CVD and cancer (Mercuri et al., 2000). Almonds and other nuts contain a multitude of antioxidants (Table 18.2) that may prove to reduce the extent of oxidative damage incurred to cells through metabolism (Chen et al., 2005). A recent study examined the acute effects of nut consumption in healthy human subjects. The investigators found that both almonds and walnuts (in the form of smoothies) led to signicant increases in the plasma polyphenol concentration following the nut meals (Torabian et al., 2009). The same study showed that the susceptibility of plasma lipids to peroxidation decreased after 90 minutes on both nut treatments, but not on the control. Similar results have been noted in a trial of 60 male smokers, where almonds were shown to decrease lipid peroxidation and reduce oxidative damage to DNA (Li et al., 2007). Moreover, avonoids found in the skin of almonds may further contribute to oxidative protective benets. Flavonoids are considered to possess a variety of biological activities, including antioxidant and anti-inammatory capability. The antioxidant properties of almond avonoid were recently shown to be highly biologically available and work synergistically with other

CHAPTER 18 Almonds and Oxidative Stress

antioxidants (Vitamins C and E) to protect against LDL oxidation in vitro, as well as enhancing resistance to Cu2 induced oxidation of LDL ex vivo (Chen et al., 2005). These data suggest that almonds are a rich source of bioactive compounds and antioxidants that can prevent lipid, DNA, and protein peroxidation. In conclusion, through the many macro- and micronutrients that almond seeds contain (Table 18.2), they may contribute to lowering oxidative damage in both healthy individuals and patients with chronic disease. These effects may be achieved either indirectly, via lowering the overall glycemic load and the glycemic index of meals consumed concomitantly (Brownlee, 2001; Monnier et al., 2006; Kendall et al., 2010), or more directly through their intrinsic polyphenols and avonoids. Therefore, it is not surprising that almond seeds and other nuts have been so prevalently associated with signicant reductions in risk factors for developing CHD, CVD, diabetes, and other chronic diseases (Ros, 2009; Kendall et al., 2010).

ADVERSE EFFECTS AND REACTIONS (ALLERGIES AND TOXICITY)


Almonds are ranked third (15% reactive), behind walnut and cashew nuts, as a tree nut allergen (Roux et al., 2003). The total annual number of anaphylactic mortalities in the United States due to all food allergens is 100, most of which are due to peanuts, but also include shellsh, eggs and other tree nuts, including almonds (Matasar & Neugut, 2003). The wild bitter variants of almonds contain trace amounts of cyanide (found in most seeds). However, the sweet or domesticated variant of almonds does not contain this toxin. Hence, cyanide toxicity resulting from almond seed consumption has been rarely reported (Roux et al., 2003). Another consideration when harvesting and storing almonds is the possibility of the presence of aatoxins. The UK Food Standards Agency, in a survey of nut products available in the market, tested 154 samples of tree nuts (including almonds) for aatoxins. The ndings of this survey suggested that of the almond samples tested, only one had aatoxin levels higher than the acceptable limit of 4 mg/kg (The Food Standards Agency, 2004).

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SUMMARY POINTS
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The high levels of MUFAs in almond (Prunus Dulcis) have been shown to improve glycemic control; hence the management of type 2 diabetes. The low carbohydrate content of nuts results in a low glycemic index and a moderate postprandial serum glucose excursion. The highly bioavailable avonoids and polyphenols that almonds contain help to reduce lipid, protein, and DNA peroxidation. Through reduction of postprandial glycemia, almonds have been shown to reduce oxidative stress, and therefore to decrease the risks of CHD and cancer. Nut consumption has been indicated for weight loss, and as a part of a weight-maintaining diet.

References
American Diabetes Association. (2007). Nutrition Recommendations and Interventions for Diabetes: a position statement of the American Diabetes Association. Diabetes Care, 30(Suppl. 1), S48eS65. Bes-Rastrollo, M., Wedick, N. M., Martinez-Gonzalez, M. A., Li, T. Y., Sampson, L., & Hu, F. B. (2009). Prospective study of nut consumption, long-term weight change, and obesity risk in women. The American Journal of Clinical Nutrition, 89, 1913e1919. Brownlee, M. (2001). Biochemistry and molecular cell biology of diabetic complications. Nature, 414, 813e820. Chen, C. Y., Milbury, P. E., Lapsley, K., & Blumberg, J. B. (2005). Flavonoids from almond skins are bioavailable and act synergistically with vitamins C and E to enhance hamster and human LDL resistance to oxidation. Journal of Nutrition, 135, 1366e1373.

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Estruch, R., Martinez-Gonzalez, M. A., Corella, D., Salas-Salvado, J., Ruiz-Gutierrez, V., Covas, M. I., et al. (2006). Effects of a Mediterranean-style diet on cardiovascular risk factors: a randomized trial. Annals of Internal Medicine, 145, 1e11. Grifths, M. D., & Anthony, J. H. (1992). The New Royal Horticultural Society dictionary of gardening. London, UK: Macmillan Press. Jenkins, D. J., Wong, J. M., Kendall, C. W., Esfahani, A., Ng, V. W., Leong, T. C., et al. (2009). The effect of a plantbased low-carbohydrate ("Eco-Atkins") diet on body weight and blood lipid concentrations in hyperlipidemic subjects. Archives of Internal Medicine, 169, 1046e1054. Josse, A. R., Kendall, C. W., Augustin, L. S., Ellis, P. R., & Jenkins, D. J. (2007). Almonds and postprandial glycemia e a doseeresponse study. Metabolism, 56, 400e404. Kendall, C. W., Esfahani, A., Truan, J., Srichaikul, K., & Jenkins, D. J. (2010). Health benets of nuts in prevention and management of diabetes. Asia Pacic Journal of Clinical Nutrition, 19, 110e116. Kris-Etherton, P. M., Zhao, G., Binkoski, A. E., Coval, S. M., & Etherton, T. D. (2001). The effects of nuts on coronary heart disease risk. Nutrition Reviews, 59, 103e111. Li, N., Jia, X., Chen, C. Y., Blumberg, J. B., Song, Y., Zhang, W., et al. (2007). Almond consumption reduces oxidative DNA damage and lipid peroxidation in male smokers. Journal of Nutrition, 137, 2717e2722. Lovejoy, J. C., Most, M. M., Lefevre, M., Greenway, F. L., & Rood, J. C. (2002). Effect of diets enriched in almonds on insulin action and serum lipids in adults with normal glucose tolerance or type 2 diabetes. The American Journal of Clinical Nutrition, 76, 1000e1006. Matasar, M. J., & Neugut, A. I. (2003). Epidemiology of anaphylaxis in the United States. Current Allergy and Asthma Reports, 3, 30e35. Mercuri, F., Quagliaro, L., & Ceriello, A. (2000). Oxidative stress evaluation in diabetes. Diabetes Technology & Therapeutics, 2, 589e600. Monnier, L., Mas, E., Ginet, C., Michel, F., Villon, L., Cristol, J. P., et al. (2006). Activation of oxidative stress by acute glucose uctuations compared with sustained chronic hyperglycemia in patients with type 2 diabetes. The Journal of the American Medical Association, 295, 1681e1687. Rieger, M. (2006). Introduction to fruit crops. New York, NY: Food Products Press. Ros, E. (2009). Nuts and novel biomarkers of cardiovascular disease. The American Journal of Clinical Nutrition, 89, 1649Se1656S.

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Roux, K. H., Teuber, S. S., & Sathe, S. K. (2003). Tree nut allergens. International Archives of Allergy and Immunology, 131, 234e244. Rushforth, K. (1999). Collins Wildlife Trust guide to trees: a photographic guide to the trees of Britain and Europe. London, UK: Harper Collins. Sabate, J., Haddad, E., Tanzman, J. S., Jambazian, P., & Rajaram, S. (2003). Serum lipid response to the graduated enrichment of a Step I diet with almonds: a randomized feeding trial. The American Journal of Clinical Nutrition, 77, 1379e1384. Ternus, M., McMahon, K., Lapsley, K., & Johnson, G. (2006). Qualied health claim for nuts and heart disease prevention: development of consumer-friendly language. Nutrition Today, 41, 62e66. The Food Standards Agency. (2010). The Food Standards Agency Aatoxins in Nuts Survey. London, UK: FSA. Torabian, S., Haddad, E., Rajaram, S., Banta, J., & Sabate, J. (2009). Acute effect of nut consumption on plasma total polyphenols, antioxidant capacity and lipid peroxidation. Journal of Human Nutrition and Dietetics, 22, 64e71. Zohary, D., & Maria, H. (2000). Domestication of plants in the old world: the origin and spread of cultivated plants in West Asia, Europe, and the Nile Valley. Oxford, UK: Oxford University Press.

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