White Mulberry Leaf: Usefulness and Safety | NCCIH

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1. Introduction

Mulberry (Genus: Morus; Family: Moraceae) is an economical and widespread woody plant. In the Asian countries mulberry is widely cultivated for its leaf to feed the monophagous silkworm (Bombyx mori L.). The silkworm (B. mori L.) only naturally feed on mulberry leaf which makes mulberry the most vital component of sericulture industry that provides employment to a large number of people of India, China, Bangladesh, Pakistan, and many other Asian countries [1]. Other than sericulture it has an enormous economic value leads to its several unique and special features. Each single parts of mulberry plant can be used for various purposes. In India it is popularly known as ‘Kalpa Vriksha’ for its multipurpose utilities [2].

Main elements that determine the nutritional quality of any edible plant products are the qualitative and quantitative presence of protein, carbohydrate, dietary fiber and types of vitamin present inside the product; mulberry plant can be highly rated in this context [2]. Mulberry fruits in fresh condition contain carbohydrate which is present either in the form of simple sugars or in the form of starch, soluble and insoluble fibers. They are low in calorie value and high in water content. Iron, vitamin C, decent amount of potassium, vitamin E and K are predominantly found present in the fruits. They are also rich in plant compounds, like anthocyanins, that contribute to their color and positive health effects. Fruits can also improve the blood sugar level, can lower the amount of blood cholesterol, and can help in preventing fatty liver disease. Fruits are also found effective in decreasing the oxidative stress which can reduce the risk of cancer. Leaves of mulberry are also excellent food stuffs as they show nearly the same properties as the fruit. Recent findings mentioned that mulberry leaves contain high amount of bioactive compounds which mainly includes alkaloids, flavonoids, γ-aminobutyric acid (GABA) and phenolic acids [3]. These compounds are effectively involved with antioxidation property [4, 5], as it lowers glycemia [6, 7] minimizes hypertension [8], prevents atherosclerosis, [9] and also shows anti-inflammation property [10]. Bioactive compounds like 1-deoxynojirimycin (DNJ), found in mulberry, seems to be a powerful inhibitor of α-glycosidase and has also shown potential therapeutic capacity for minimizing many diseases, particularly type II diabetes [11, 12]. Recent investigations also explored the very interesting tyrosinase inhibition activity of mulberry. In this regards, white mulberry (Morus alba), black mulberry (Morus nigra) and red mulberry (Morus rubra) are the most accepted worldwide species of the genus Morus [2].

Unani, Ayurveda, and Chinese systems of medicine traditionally recognize almost all mulberry varieties for their several pharmacological properties. M. nigra fruits are considered as one of the most important components having anti-cancerous properties and popularly known as ‘Tuti Aswad or Toot Aswad’ in Unani literature [13]. Traditional medicine practitioners consider mulberry as one of the most efficient plant in the treatment of blood pressure, dental diseases, constipation, helminthic complications, diabetes, hypertension, anemia and arthritic pain [2].

Valuable constituents in mulberry plant; mainly the fruits and leaves categorizes it as a plant which can perfectly be placed in the category of a functional food that not only useful to human health but also having proper basic nutritional function [14]. The Ministry of Health of China in , declared M. alba as the first medicinally significant edible fruit [15]. Both leaves and fruits of M. alba are also considered as food and drugs along with its primary considerations [16].

The population of Earth been never before as huge as it is today [17]. Rise of nutrient deficiencies is also tied with this population growth has become a serious global crisis, predominantly in the areas where the diet lacks variety. Cheap, easily available, nutritious and pharmaceutically influential plant resources are seems to be the solution of this global crisis. In this context the current review attempts to provide an insight into the potential of mulberry as a valuable resource for food and pharmaceutical industries. An overview of importance of mulberry in food and pharmaceutical industry is shown in Figure 1.

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2. Geographical distribution of mulberry

Worldwide appreciable availability of any biological resource is extremely important from its exploitation point of view especially for the food and pharmaceutical industries. Presently, Mulberry is distributed in all regions between 500N Lat. and 100S Lat., and from sea level to  m altitudes [18, 19], including Asia, Europe, North and South America, and Africa (Figure 2). American continent has four mulberry species (M. insignis, M. celtidifolia, M. corylifolia, and M.mexicana). In India, four mulberry species are reported; among them M. alba and M. indica are domesticated whereas M. serrata and M. laevigata grow wildly in the Himalayan territory [1]. China has 24 species but only four species has been spotted for its massive exploitation in sericulture (M. alba, M. multicaulis, M.atropurpurea, and M. mizuho). Only M. alba, M. bombycis, and M. latifoila are in use in Japan though presence of 19 species has been recorded there. In Africa, presence of M. mesozygia has been reported from humid, sub-humid, and semi-arid areas [20].

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3. Botanical description of mulberry plant

Before any sort of investigations of a plant it is extremely urgent to go through its overall botanical details. Mulberry is a perennial, fast growing, woody, deciduous, deep and wide rooted plant [21]. Generally the height of Mulberry plant is approximately 5-6 feet from the ground level [22]. Stem of mulberry is cylindrical in shape with milky sap and fissured bark [23]. Mulberry leaves are generally 5-7.5 cm long and 6-10 cm wide, but they vary widely in their size and shape. Leaves are mostly deeply lobed or having serrate margins; leaf apex is mostly acute with cordate or truncate base. Basal nerves are generally 3; near the margins lateral nerves are forked. Flowers are yellowish green in color with chromosome number 2n = 28. There are differentiations between female and male spikes shape and size in mulberry. Male spikes (catkins) are cylindrical and broad where as female spikes (catkins) are ovoid and stalked, and female spikes (catkins) shorter than male spikes (catkins). Mulberry fruits are arranged longitudinally around the central axis in cluster of small fruits similar with blackberry or loganberries. Mulberry fruits are white to pinkish white in color and during the time of ripening it becomes purple or black in color. Fruits contain many drupes which are enclosed in a fleshy perianth, upto 5 cm long, sub-globose or ovoid in shape. Ovary of mulberry is unicellular with presence of a bifid stigma [2].

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4. Mulberry as a potential food resource

Increasing consumer demand has been one of the driving forces in exploration of new natural food resources, keeping in mind that the food product must satisfy both basic dietary requirements and health benefits. In this respect it is evident that mulberry fruits are already famous throughout the world for their mouth-watering taste that makes it suitable to consume either in fresh or as an ingredient in value-added products and for culinary uses (Table 1). It is gradually becoming popular to the consumers not only because of their taste but also due to its high nutritional importance along with low calorie value. Opportunity of exploiting other parts of mulberry as processed food resource is also very high. This has led to increased demand of mulberry also in the food processing industries.

Food itemsUsesReferenceSquashFruits of M. alba used for the preparation of spiced squash and appetizer.Hamid and Thakur, [24].PastryBuckwheat flour, hulls, inulin and chokeberry along with M. alba extraction used for the production of pastry which is rich in fiber and low in calorie.Komolka et al., [25].ChocolateFrom dried M. nigra fruit obtained anthocyanins can be used in chocolate preparation.Gultekin-Ozguven et al., [26].PastaExtraction of M. nigra having hypoglycaemic effect, it reduces the glycemic index is vastly used to produce pasta.Yazdankhah et al., [27].Minced meatShelf life of minced meat increased by methanolic extraction of mulberry leaves.Yazdankhah et al., [27].YogurtAnthocyanins of M. rudra acts as a coloring agent of strawberry flavored yogurt.Byamukama et al., [28].ProbioticsFor the isolation and culture of lactic acid forming bacteria M. alba silage is very important. These bacteria can stabilize the gastrointestinal tract microbial flora.Jan et al., [2].Fruit jamMixed fruit jam prepared based on ratios of 70:30 rosella and mulberry fruit extract.Wongchalat and Chatthongpisut., [29].Cup cakeThe concentrated amount of M. alba paste used to prepared cupcakes.Jan et al., [2]SyrupFor the preparation of syrup M. alba fruit used and it can be stored for 6 months under refrigerated condition.Thakur et al., [30].VinegarM. alba is exploited to prepare vinegar.Karaagac et al., [31].Alcholic beverageFruit of M. alba used to produce alcoholic beverage and also used as a raw material to brew fruit wine.Daris-Martin et al., [32].

Mulberry fruits can be directly used for the preparation of jam and soft drinks [33]. Fresh fruits of mulberry are highly rated for human health because it contains vitamins, amino acids, and different minerals such as Zn, Ca, Mn, and Fe along with pectin and fibrin. Mulberry leaf is used for making tea, dhokla, pakoda and many other delicious different foodstuffs [34]. Mulberry is already a popular vegetable, along with the presence of high level of sugar makes mulberry an ideal resource for the food industry. It can be used for making breads, cakes, fruit drink pulp, fruit wine, fruit sauce, fruit powder and also chocolate. Fresh or dried or frozen forms of mulberry fruits can be utilized to produce different kinds of tonic, wine, syrups, amaretto. Mulberry seeds also can be used to produce oil. Unripe and immature mulberry fruits can be used for chutney preparation [35]. Famous Turkish food ‘Kome’ and ‘Pestil’ is prepared by mixing walnut, honey and flour with mulberry [36, 37]. Mulberry juice kept under a cold storage at a particular temperature for six months to one year has proven effective for healthy skin and in prevention of throat infection [38]. Mulberry paste popularly known as ‘sangshengao’ used to make tea in China and it also found effective in improving liver and kidney function, vision and hearing. Use of dehydrated mulberry fruit as a sweetening agent in black tea is extremely popular among the Iranian people. In some specified regions of China young leaves of mulberry is in use as vegetables [2]. Mulberry fruit powder can be consumed as an anti-aging substance as it protects the cell from the aging effect. It also stabilizes cholesterol level and increases the carbohydrate absorption capacity of the human digestive system. Over-ripened mulberry fruits are used to produced Mulberry wine, this also known as a ‘lady’s drink’ in Europe. Anthocyanin obtained from of M. rubra used for yogurt coloration having no difference with strawberry brand yogurt [28]. M. alba extract can be used to produce pastry along with Buckwheat flour, buckwheat hulls, chokeberry and inulin [25]. Shelf life of minced meat can be increased with the help of methanolic extraction of mulberry plant [27]. M. alba fruits can also be used to prepare spiced squash and appetizers [24].

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5. Pharmaceutical and therapeutic importance of mulberry

Mulberry having exclusive therapeutic properties that are primarily due to their indigenous chemicals along with their anti-oxidant, anti-diabetic, anti-hypertensive, anti-cancer, hepatoprotective properties, and many more. Most important and relevant pharmaceutical ability of mulberry to improve human health and well-being is discussed in this section (Table 2).

Pharmaceuticals importance of mulberrySpecisParts usedMajor findingsRef.Anti-oxidantM. alba
M. nigraTwigs, Bark
Fruit
Leaves
Stem

• Twigs, bark consists morin, maclurin that is important for inflammatory responses, and nervous system functioning.

• Scavenging activities against super oxide and anion radicals.

• Shows strongest protective effect on H2O2-induced injury.

• Moracin extracted from leaves it shows anti-oxidant activities.

• Stem extract shows anti-oxidant activity that increase superoxide and NO scavenging activity.

Kadam et al., [14], Wang et al., [16], Jan et al., [2].Anti- CancerM. albaFruit
Root bark
Leaves

• Fruits containing anthocyanin shows an invasion against human lung metastatic.

• Albanol A that isolated from root bark that induced potent cytotoxicity in Human Leucamia cell line

• Anti-proliferation activity against human ovarian cancer.

• Anti-proliferative lectin induced cell death in human breast cancer.

• Flavonoids present in leaves that acts as a cancer inhibiting profile agent.

Khalid et al., [22], Kadam et al., [14], Naowaratwattana et al., [39]Anti- DiabeticM. albaLeaves
Fruits
Stem bark

• Help to decrease blood glucose levels observed in brown rat.

• Help to decrease fasting blood glucose (FBG) and glycosylated serum protein in diabetic mice.

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• Alternation of glutathione and insulin levels in STZ induced diabetic rats.

Kadam et al., [14],
Wang et al., [16]
Alanazi et al., [40]Anti-InflammatoryM. albaLeaves
Stem
Fruit
Root

• Reduce the production of cytokine and pro-inflammatory mediators.

• Inhibit NO production shows anti-inflammatory effect.

• Presence of anthocyanins that can inhibit pro-inflammatory effect of cytokine in mice.

• Inhibit histamine release and act as a natural source of anti-histamine and anti-allergic agent.

Park et al., [10]
Jan et al., [2].Anti-microbialM. mesozygia
M. alba
M. nigraBark
Stem bark
Fruit

• Used for the micro-organisms associated infections.

• Antimicrobial activity against Enterococcus faecalis, E. coli, S. aureus.

• Prevent growth of S. mutans.

Kuete et al., [41], Fukai et al., [42], Thabti et al., [43], Budiman et al., [44].Activity against Skin diseaseM. albaLeaf

• Help in the inhibition of mammalian tyrosinase, melanin synthesis effects.

• It also contain carotenoids that can help to decrease age spot, blemishes effect on skin.

Chang et al., [46].
Kadam et al., [14].

5.1 Anti-cancer activity

Across the globe different forms of cancer is the most fatal disease. Many types of medicines are available in the market for the treatment of cancer but the number of successful and safe drug is very few. Anthocyanins extracted from the M. alba fruit shows an invasion in human lung metastatic A549 carcinoma cells. Flavonoids isolated from the leaves of this plant acts as a cancer inhibiting profile agent [22]. From root bark of mulberry Albanol A (Mulberrofuran G) can be extracted which induce potent cytotoxicity in HL60 (Human Leucamia Cell line) by inhibiting topoisomerase II activity [14, 39]. M. alba leaf extract shows anti- proliferative lectin induced cell death by apoptosis in human breast cancer (MCF-7) and colon cancer (HCT-15) by inducing DNA fragmentation and morphological changes. Flavanone glycosides present in the root bark of M. alba having anti-proliferation activity against human ovarian cancer in H0- cells [2].

5.2 Anti-hyperlepidemia

Obesity develops due to unusual fat deposition which is a risk for the human health. It is one of the serious problems across the globe because it can increase the chance of cardiac failure, cancer, diabetes and many other diseases. Daily consumption of M. alba fruit found effective in lowering the total cholesterol (TC) and lipoprotein levels in blood of both young and senior citizens. M. alba leaves extract which is DNJ rich if taken before meals can help to reduced the lipoproteins and triglycerides [2]. The root bark of M. alba plays an important role as inhibitor of the LDL (Low density lipo_protein) anthrogenic alternation and also act as a hypo-chlesterolemic element [22].

5.3 Anti-diabetic

Diabetes mellitus is characterized by high glucose levels (Blood sugar) which is a type of metabolic disorder. Insulin secretion, or insulin action or both can be defective in response to the high blood sugar (glucose) levels in this disease. Type 2 diabetes have two features- low gradic chronic inflammatory and the insulin resistance. Cardiovascular diseases and many other multi organ disorders can be developed by type 2 diabetes. Leaves of M. alba helps to decrease the blood glucose level and also prevents potential histo-pathological alterations in pancreas and kidneys which is observed in brown rats, in a recent experiment [14]. Soluble extract of M. alba fruit found effective in decreasing fasting blood glucose (FBG) and glycosylated serum protein (GSP) in STZ induced diabetic mice. In STZ induced diabetic rats M. alba stem bark also helps in the alternation of glutathione and insulin levels [2, 16, 40].

5.4 Anti- inflammatory

In some particular tissues presence of some microorganisms like bacteria, viruses, and fungi and their circulation in blood can cause complex vascular biological problems known as inflammation. If within a certain time period it is not diagnosed properly then it can cause severe health complications and also can cause some acute chronic diseases such as- cardiovascular disease, cancer and rheumatoid arthritis. Leaf extract of M. alba helps to reduce production of cytokine and pro-inflammatory mediators by nuclear factor- κB (NF-κB) activation suppression [10]. Twigs and root bark of mulberry consists maclurin, morin, resveratrol and isoquercitrin and the fruits of mulberry contains other essential fatty acids like palmitic, linoleic and oleic acids which are also important for inflammatory responses [14]. Stem extract of M. alba can inhibit NO production by suppressing both Inos mRNA and protein which shows an inflammatory effect. Anthocyanin present in the fruits of M. nigra shows an anti-inflammatory effect by inhibiting pro-inflammatory cytokine which is experimentally proven in mice. Root extract of M. alba is potential anti-histamine and anti-allergic natural drug resource as it successfully inhibits the histamine release and systemic allergic reaction [2].

5.5 Anti-oxidant

Different parts of mulberry consists variety of phytochemicals that have the potential of anti-oxidant properties. Moracin available in mulberry fruits help to prevent oxidative stress [14]. Fruit extract of M. alba showed radical-scavenging activities against anion radicals and superoxide that increases the level of antioxidants [16]. Moracin which can also be extracted from the leaves of M. alba shows better antioxidant activity better than other anti-oxidants like resveratrol. Stem of M. alba increase NO scavenging and superoxide activity. Fruits of M. nigra show the strongest protective effect against H2O2-induced oxidative injury in PC12 cells [2].

5.6 Anti-microbial

Anti-microbial property of mulberry is also well known. The bark of M. mesozygia used for the treatment of micro-organism associated infections [41]. Flavonoids isolated from M. alba shows positive response in the treatment of antiviral and antifungal diseases [14]. Hydro-methanolic stem bark extract of M. alba shows antimicrobial activity against Enterococcus faecalis, Escherichia coli, Staphylococcus aureus and Salmonella typhimurium [42, 43, 44]. Similarly, ethanolic extract of M. nigra prevent the growth of Staphylococcus epidermidis, and Propionibacterium acnes. Fruits of M. alba contain the anti-bacterial compound Morin which strongly inhibits Streptococcus mutans. The juice of M. nigra contain anti-microbial properties against Bacillus spizizenii and Pseudomonas aeruginosa. Vinegar produced from M. alba shows potential antimicrobial action against Erwinia carotovora, Streptococcus pyogenes, Bacillus cereus and anti-fungal activities against Candida albicans [2].

5.7 Neurodegenerative actions

For treating cognitive disorders and different types of neuronal dysfunction medicinal plants play an important role and mulberry is one of the most prominent among them. Polyphenolics, alkaloids found in M. alba can improve cognitive function and delay in neural-degeneration [45]. Mulberry fruits’ lycophilised ethanolic extract can protect against oxidative stress-induced apoptosis in neural cells by the enhancement of the antioxidant enzymes production. In mulberry fruit rutin, quercetin anthocyanins are found present which have an impact on Parkinson’s disease (PD) by interfering MPTP-induced dopaminergic neuronal damage and bradykinesia [2, 45].

5.8 Hepatoprotective

A few bioactive compounds obtained from the twigs of M. mesozygia esspecially shows the hepatoprotective activities. From M. indica a glycoprotein (MIL) is purified which protects against CC14 induced liver damage. In CC14 treated mice MIL found decreasing the activity of Lactate dehydrogenase (LDH), thiobarbituric acid-reactive substances (TBARS), and alanine aminotransferase (ALT). M. alba extract found effective in decreasing the activity gastric mucosal injury in rats [14].

5.9 Activity against skin problem due to anti-tyrosinase property

Use of tyrosinase inhibitors is getting huge importance in the cosmetic industry due to their skin-whitening effects. Tyrosinase can be used as a whitening agent as it is a copper-containing primary regulatory multifunctional enzyme that is responsible for the biosynthesis of melanin and determines the color of the skin. Deposition of excessive melanin causes numerous dermatological disorders, such as melasma and age spots [48]. Twigs and roots of mulberry can be utilized as natural agents to react against the tyrosinase activity in cosmetics [49]. In a recent experiment, M. alba fruit ethanolic extract has been utilized to formulate an emulsion-based cream to observe its clinical effect on skin melanin, moisture content and erythema for eight weeks. The formulated cream shown significant decrease in melanin content without causing any sort of skin irritation [50]. Betulinic acid (C30H48O3) which has been successfully isolated from M. alba (hexane extract of stem and root bark) can be utilized as a whitening agent owing to its tyrosinase inhibitory activity [51]. Ethanolic extract of M. nigra shows excellent tyrosinase inhibition activity and also can be exploited for the formulation of peel-off mask and for acne treatment [44, 45]. Mulberries can help to reduce skin problems such as spots and blemishes appears with age and also provides healthier and shiny appearance to skin and hair. From the above discussion, it is clear that mulberry exhibits remarkable tyrosinase inhibition activity, hence can be included as a necessary component of cosmetic products and de-pigmentation agents for the treatment of disorders like hyper-pigmentation.

5.10 Cardiovascular activity

M. alba mostly used in eastern countries to treat cardiovascular diseases. Chinese people also use M. alba for decreasing blood pressure which can lead to cardiovascular disorder. It also helps to reduce serum cholesterol, hypertension and also prevents artherosclerosis [47]. From the root bark of M. alba morusinol is extracted which prevents collagen and arachidonic acid which induces TXB2 formation in cultured platelets known as the main causative agent of congestive cardiac failure. Mulberries contain Reveratrol, which is a very important flavonoid is found to increase the formation of Nitric oxide (NO) that acts as a vasodilator. Richness of flavanoids and vitamin C makes mulberry also ideal for treating other cold, flu-like problems [14].

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6. Conclusion

Best way to find out the solution of hunger and pharmaceutical demand is the discovery and exploitation of new biological resources. Products from natural resources are now being re-emphasized to encounter these issues. Connection between the health and diet is very clear and consumers are now-a-days very much concern about their health. The solution of rural hunger and helping them to come out of the nutritional deficiency is not only a matter of deep concern. Investigating these connections has drawn the attention of the scientists in exploration of biological functional foods and pharmaceuticals, which can dominate the global nutrition market. The current review attempts to point out the potentiality of mulberry species in different areas and it is clear that mulberry is a versatile plant from both food and pharmaceutical aspects with huge possibilities. Mulberry is a jewel of food industry. Being low in calories, this plant can be exploited in the preparation of hypo-caloric foodstuffs and also can be added as a new ingredient to enhance the functional properties of different popular foods. Products like jam, jelly, wine, vinegar, tea, syrup, squash and many more are successfully formulated from mulberry that aids industrialists for further effective utilization of its fruits, leaves and other plant parts. Mulberry is also among the major ingredients in many traditional formulations sold worldwide. In addition to its exceptional usage in the food industry, recent studies have revealed that Morus species and their bioactive phytochemicals are having important biomedical activities, including anti-diabetic, antioxidants, anti-obesity, hypo-lipidemic, antihypertensive, and anti-atherosclerosis, etc. Tyrosinase inhibition activity of mulberry is comparable with kojic acid that makes it a wonderful ingredient in cosmetics. Different isolated chemical compounds like maclurin and morin, oxyresveratrol from different parts of M. alba shows potential tyrosinase inhibition activity. There are still some unidentified biological novel compounds present in mulberry that require proper exploration. Proper investigation, exploration and exploitation of mulberry in both food and pharmaceutical industry having the potentiality of creating a history.

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7. Recommendations

Sericulture is mainly known as a women friendly enterprise, because of the high percentage of involvement of rural women which is about 53.45% of the total employment generated in silk industry. Though broad involvement of rural women are significantly high in the silk industry, but the involvement of tribal people is still scanty [52] which should be considered for extension for financial support and development of small scale industries, mainly in the developing countries. It is the most important fact that the main concentration of the sericulture industry moves around the silkworm feeding, cocoon generation and silk rearing. The proper exploitation of the mulberry in terms of food product and pharmacologically potent substance is still far from the goal. Lack of proper infrastructure for cocoon production and reeling often becomes a barrier for the cultivation of mulberry plant, because B. mori moth can only feed upon the fresh and juicy mulberry leaves [53]. Rural people will be able to overcome these constrains if they will be properly trained about the other economic importance of mulberry.

In this context, it is highly recommendable that proper training, campaigning, infrastructure and market development along with broad research and development projects on proper scientific exploitation of mulberry other than feeding the silkworm is absolutely essential and urgent.

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Acknowledgments

Authors are grateful to the Hon’ble Vice Chancellor of Raiganj University, India for providing necessary facilities. This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

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