Which Vitamin Is Found Only In Animal-derived Foods?
Nutrients. 2014 May; 6(5): 1861–1873.
Vitamin B12-Containing Plant Food Sources for Vegetarians
Received 2014 Mar 10; Revised 2013 April 23; Accepted 2014 Apr 28.
Abstruse
The usual dietary sources of Vitamin B12 are beast-derived foods, although a few plant-based foods contain substantial amounts of Vitamin B12. To foreclose Vitamin B12 deficiency in loftier-risk populations such as vegetarians, it is necessary to identify constitute-derived foods that contain high levels of Vitamin B12. A survey of naturally occurring plant-derived food sources with high Vitamin B12 contents suggested that stale purple laver (nori) is the nigh suitable Vitamin B12 source shortly bachelor for vegetarians. Furthermore, stale purple laver also contains loftier levels of other nutrients that are lacking in vegetarian diets, such equally iron and n-3 polyunsaturated fat acids. Dried royal laver is a natural plant product and it is suitable for almost people in diverse vegetarian groups.
Keywords: cobalamin, dried purple laver, nori, vitamin B12 deficiency
ane. Introduction
Vitamin B12 (molecular weight = 1355.4) belongs to the "corrinoids" group, which comprises compounds that contain a corrin macrocycle. The term "Vitamin B12" is usually restricted to cyanocobalamin, which is the almost chemically stable and unnatural form of cobalamin [i], but Vitamin B12 refers to all potentially biologically agile cobalamins in the present review. Cyanocobalamin is included in most human dietary supplements, and it is readily converted into the coenzyme forms of cobalamin, i.e., methylcobalamin functions equally a coenzyme for methionine synthase (EC two.i.1.13; involved in methionine biosynthesis), and 5′-deoxyadenosylcobalamin functions as a coenzyme for methylmalonyl-CoA mutase (EC 5.4.99.ii; involved in amino acid and odd-chain fatty acrid metabolism in mammalian cells) [2,three] (Figure one). Corrinoids with a base other than 5,half dozen-dimethylbenzimidazole as the lower ligand (cobalt-coordinated nucleotide) were recently institute in sure foods and they are inactive in humans [4].
Structural formula of Vitamin B12 and partial structures of Vitamin B12 compounds. The fractional structures of the Vitamin B12 compounds only show the regions of the molecule that differ from Vitamin B12. (ane) 5′-Deoxyadenosylcobalamin; (2) methylcobalamin; (three) hydroxocobalamin; and (4) cyanocobalamin or Vitamin B12.
Vitamin B12 is synthesized only past sure leaner, and it is primarily concentrated in the bodies of predators located higher in the nutrient concatenation [5]. Vitamin B12 is well-known to be the sole vitamin that is absent from plant-derived food sources. Foods (meat, milk, eggs, fish, and shellfish) derived from animals are the major dietary sources of Vitamin B12 [four]. The recommended dietary assart (RDA) of Vitamin B12 for adults is gear up at 2.iv μg/twenty-four hour period in the United states (and Nihon) [six,7]. The major signs of Vitamin B12 deficiency are megaloblastic anemia and neuropathy [six]. Vegetarians are at a higher risk of Vitamin B12 deficiency than non-vegetarians [8]. The frequencies of the deficiency amongst vegetarians were estimated as 62%, 25%–86%, 21%–41%, and 11%–90% in meaning women, children, adolescents, and elderly subjects, respectively, by review of the 18 reports evaluating Vitamin B12 status of vegetarians [9]. The objective of this review is to present up-to-appointment information on Vitamin B12-containing plant-derived food sources to prevent vegetarians from developing Vitamin B12 deficiency.
ii. Main Types of Vegetarian Diets
In that location are several main types of vegetarian groups: (1) Lacto-ovo vegetarianism [10]: many people are familiar with this type of vegetarianism, which comprises virtually vegetarians. "Lacto" indicates that a person consumes milk and milk products (butter, yogurt, cheese, etc.), and "ovo" ways that a person consumes eggs. In full general, lacto-ovo vegetarians do non eat animal meats (including fish and shellfish). Some vegetarian groups are ovo but or lacto only, i.due east., they consume but eggs or but milk and its products, respectively, equally animal products; (two) Raw veganism [eleven]: this diet is mostly or entirely based on fresh fruits, vegetables, basics, and seeds; (3) Fruitarianism [12]: this is by and large a raw mode of eating that primarily depends on fruits, nuts, and seeds; (four) Buddhist vegetarianism [13]: this is a vegan nutrition that excludes all animal products and Allium family vegetables (onion, garlic, leeks, and shallots) on ethical grounds; (5) Macrobiotic [fourteen]: this nutrition is primarily focused on grains, beans, and similar staples, including some vegetables and other whole foods. Processed foods and most fauna products are strongly avoided; and (6) Jain vegetarianism [15]: another religious dietary practice that includes dairy products, but excludes eggs and honey as well as root vegetables.
3. Nutritional Characterization of Vegetarian Diets
From a food intake perspectives, vegetarian diets are usually rich in carbohydrates, due north-half-dozen polyunsaturated fat acids, dietary fibers, carotenoids, folic acid, Vitamin C, Vitamin E, and magnesium (Mg), merely these diets are relatively low in proteins, saturated fatty acids, n-3 polyunsaturated fatty acids (specially eicosapentaenoic and docosahexaenoic acids), Vitamin A (retinol), Vitamin B12, Vitamin Dthree (chlolecalciferol), zinc, iron, and calcium [sixteen,17,xviii] (Table 1). In item, Vitamins A, B12, and Dthree are found just in animal-derived foods, whereas Vitamin D2 (ergocalciferol) and provitamin A (β-carotene) are found in mushrooms and vegetables, respectively [nineteen,20]. Furthermore, Vitamin Diii tin be synthesized in the man skin nether sunlight [21]. A vegetarian diet usually provides a low intake of saturated fatty acids and cholesterol but a loftier intake of dietary fibers and health-promoting phytochemicals (e.g., various polyphenol compounds) due to an increased consumption of fruits, vegetables, whole-grains, legumes, basics, and diverse soy products. As a outcome, vegetarians typically have lower body mass index, serum cholesterol levels, and blood pressure [xviii]. Compared with non-vegetarians, vegetarians also have reduced rates of mortality due to ischemic centre disease, probably because of lower blood cholesterol. However, there are no clear differences with respect to other major causes of decease such as stroke and cancers [17]. Craig [17] reported that, compared with non-vegetarians, vegetarians have lower incidences of hypertension, stroke, type 2 diabetes, and certain cancers. Pawlak et al. [9] showed that vegetarians can develop Vitamin B12 depletion or deficiency regardless of their demographic characteristics, place of residency, historic period, or type of vegetarian diets. The Vitamin B12 content is non high in whole eggs (approximately 0.9–1.iv μg/100 g), most of which is located in the egg yolk [22]. The average bioavailability of Vitamin B12 from cooked eggs is 3.seven%–9.ii% [23]. Thus, the Vitamin B12 in eggs is more often than not poorly absorbed compared with that in other animal-derived products [24]. The Vitamin B12 content of various types of milk is very depression (approximately 0.3–0.four μg/100 g) [4], and appreciable losses of Vitamin B12 occur during the processing of milk [25,26]. Approximately twenty%–60% of the Vitamin B12 that is initially present in milk is recovered in cottage cheese, difficult cheese, and bluish cheese [27]. The Vitamin B12 content in the whey is considerably reduced during lactic acid fermentation [28]. These observations explain why Vitamin B12 deficiency is relatively mutual in lacto-ovo-vegetarians. Furthermore, nutrient-jump Vitamin B12 malabsorption occurs with certain gastric dysfunctions, specially atrophic gastritis with low tum acid secretion [29]. The trunk storage level of Vitamin B12 is significantly depleted by a persistent vegetarian diet; thus Vitamin B12 deficiency may readily develop in elderly vegetarians. Withal, Vitamin B12 deficiency may go undetected in vegetarians because their diets are rich in folic acid, which may mask vitamin B12 deficiency until astringent health problems occur [thirty]. Vitamin B12 deficiency contributes to the development of hyperhomocysteinemia, which is recognized as a risk factor for atherothrombotic [31] and neuropsychiatric disorders [32], thereby negating the beneficial health effects of a vegetarian lifestyle. Thus, many investigators have suggested that vegetarians should maintain an acceptable intake of Vitamin B12 by consuming supplements that contain Vitamin B12 or Vitamin B12-fortified foods [29,33].
Table ane
Food imbalance in vegetarian diets.
| Rich | Depression |
|---|---|
| Cobweb | Vitamin A |
| Vitamin C | Vitamin D3 |
| Vitamin E | Vitamin B12 |
| Folate | Atomic number 26 |
| Magnesium | Cholesterol |
| north-6 Polyunsaturated fatty acids | n-3 Polyunsaturated fatty acids |
| Carbohydrates | Saturated fat acids |
iv. Vitamin B12-Containing Found-Derived Nutrient Sources
In the United States, ready-to-eat cereals fortified with Vitamin B12 comprise a high proportion of the dietary Vitamin B12 intake [6]. Several enquiry groups have suggested that eating a breakfast cereal fortified with folic acrid, Vitamins B12 and B6 increases the blood concentrations of these vitamins and decreases the full homocysteine concentrations in the plasma of elderly subjects [34]. Thus, Vitamin B12-fortified breakfast cereals may be a especially valuable source of Vitamin B12 for vegetarians. Withal, processed foods are strongly avoided by virtually vegetarians in addition to animal products. Thus, it is necessary to place plant-derived food sources that naturally contain a large amount of Vitamin B12 to prevent Vitamin B12 deficiency in vegetarians.
4.1. Vitamin B12-Enriched Beans and Vegetables Produced Using Organic Fertilizers or Hydroponics
Mozafar [35] demonstrated that adding an organic fertilizer such as cow manure significantly increased the Vitamin B12 content of spinach leaves, i.due east., approximately 0.14 μg/100 g fresh weight. However, the consumption of several hundred grams of fresh spinach would exist insufficient to meet the RDA of 2.4 μg/twenty-four hours for adult humans [6,7]. Furthermore, our recent [36] and unpublished research indicates that most organic fertilizers, particularly those made from animal manures, contain considerable amounts of inactive corrinoid compounds. These compounds are likewise present in human being carrion where they account for more than 98% of the total corrinoid content [37].
Some researchers attempted to gear up Vitamin B12-enriched vegetables past treating them with a solution that contains high levels of Vitamin B12 [38,39]. This resulted in significant increases in the plant Vitamin B12 contents, thereby suggesting that Vitamin B12-enriched vegetables may be particularly benign to vegetarians. However, artificially Vitamin B12-enriched vegetables may not fit the philosophy of vegetarians.
4.2. Fermented Beans and Vegetables
The Vitamin B12 contents of soybeans are low or undetectable. Still, a fermented soybean-based food chosen tempe contains a considerable corporeality of Vitamin B12 (0.7–viii.0 μg/100 g) [xl]. Bacterial contagion during tempe production may contribute to the increased Vitamin B12 content of tempe [41]. Other fermented soybean products contain infinitesimal amounts of Vitamin B12 [42,43].
Only trace amounts of Vitamin B12 were constitute in broccoli, asparagus, Japanese butterbur, mung bean sprouts, tassa jute, and water shield [44]. Fermented Korean vegetables (kimuchi) incorporate traces (<0.one μg/100 m) of Vitamin B12 [43]. High Vitamin B12 (approximately x μg/100 k)-enriched vegetable products tend to exist produced by fermentation with sure lactic acrid or propionic bacteria [45,46].
Vitamin B12 is constitute in various types of tea leaves (approximately 0.1–1.ii μg Vitamin B12 per 100 thousand dry out weight) [47]. For instance, Vitamin B12-scarce rats were fed a Japanese fermented black tea (Batabata-cha) potable (50 mL/day, equivalent to a daily dose of 1 ng Vitamin B12) for 6 weeks, and the urinary methylmalonic acrid excretion (an index of Vitamin B12 deficiency) levels in the tea beverage-supplemented rats was significantly lower than in those of the deficient rats [48]. These results betoken that Vitamin B12 plant in fermented blackness tea is bioavailable in rats. However, the consumption of ane–2 L of the fermented tea beverage (typical regular consumption in Japan), which is equivalent to 20–forty ng of Vitamin B12, is not sufficient to meet the RDA of two.four μg/day for developed humans.
4.3. Edible Mushrooms
Several wild edible mushroom species are popular among vegetarians in European countries. Nil or trace levels (approximately 0.09 μg/100 g dry weight) of Vitamin B12 were measured in the dried fruiting bodies of porcini mushrooms (Boletus sp.), parasol mushrooms (Macrolepiota procera), oyster mushrooms (Pleurotus ostreatus), and black morels (Morchella conica). In contrast, the fruiting bodies of black trumpet (Craterellus cornucopioides) and golden chanterelle (Cantharellus cibarius) independent higher levels of Vitamin B12 (1.09–2.65 μg/100 1000 dry weight) than the abovementioned mushrooms [49]. To determine whether the fruiting bodies of dried black trumpet and gold chanterelle incorporate Vitamin B12 or other corrinoid compounds that are inactive in humans, we purified the corrinoid compound using an immunoaffinity column and identified it as Vitamin B12 by liquid chromatography-electrospray ionization tandem mass spectrometry [49]. In addition, high levels of Vitamin B12 were detected in the commercially bachelor stale shiitake mushroom fruiting bodies (Lentinula edodes), which are used in various vegetarian dishes. The Vitamin B12 contents of stale shiitake mushroom fruiting bodies (100 1000 dry weight) significantly varied and the average Vitamin B12 value was approximately 5.61 μg [50]. Stale shiitake mushroom fruiting bodies rarely contained the inactive corrinoid, Vitamin B12[c-lactone] as well as Vitamin B12 [50]. Lion's mane mushroom (Hericium erinaceus) fruiting bodies besides incorporate considerable amounts of Vitamin B12[c-lactone] [51]. Stabler et al. [52] demonstrated that Vitamin B12[c-lactone] binds very weakly to the most specific Vitamin B12-binding protein, i.eastward., the intrinsic factor involved in the gastrointestinal absorption of Vitamin B12, and it strongly inhibits Vitamin B12-dependent enzymes, methylmalonyl-CoA mutase and methionine synthase.
The consumption of approximately fifty g of dried shiitake mushroom fruiting bodies could meet the RDA for adults (2.4 μg/twenty-four hour period), although the ingestion of such large amounts of these mushroom fruiting bodies would not be possible on a daily ground.
4.4. Edible Algae
Diverse types of edible algae are consumed worldwide every bit food sources. Dried green laver (Enteromorpha sp.) and regal laver (Porphyra sp.) are the most widely consumed edible algae, and they contain substantial amounts of Vitamin B12 (approximately 63.6 μg/100 thou dry weight and 32.3 μg/100 g dry weight, respectively) [53] (Figure 2). However, excluding these 2 genera, other edible algae contain aught or only traces of Vitamin B12 [54]. To make up one's mind whether dried majestic and green lavers contain Vitamin B12 or inactive corrinoids, the algal corrinoid compounds were purified and confirmed as Vitamin B12 [55,56]. A substantial amount (133.eight μg/100 1000 dry weight) of Vitamin B12 was constitute in dried Korean purple laver (Porphyra sp.), simply seasoned and toasted laver products incorporate lower amounts of Vitamin B12 (approximately 51.vii μg/100 g dry weight) [57]. In particular, when the stale purple laver was treated by toasting until the laver's color changed from purple to greenish, the decreases in the Vitamin B12 contents of the seasoned and toasted laver products were not due to the loss or destruction of Vitamin B12 during the toasting process [57]. In vitro gastrointestinal digestion experiments indicated that the estimated digestion rate of Vitamin B12 from stale regal laver was approximately 50% at pH ii.0 (as a model of normal gastric office). The release of gratuitous Vitamin B12 from the imperial laver significantly decreased to approximately 2.5% at pH 7.0 (equally a model of severe atrophic gastritis) [57]. Edible purple laver predominantly contains coenzyme forms (5′-deoxyadenosylcoblamin and methylcobalamin) of Vitamin B12 or hydroxocobalamin (or both) [57,58,59].
Various types of dried green and purple lavers are Vitamin B12 sources: (i) a Japanese green laver, (Suji-aonori, Entromopha prolifera); (ii) ordinary purple lavers (Porphyra sp.; nori, which has been formed into a canvas and dried); (3) Taiwan purple laver (Hong-mao-tai, Bangia atropurpurea); and (4) New Zealand purple laver (Karengo, a mixture of Porphyra cinnamomea and Porphyra virididentata).
To measure the biological action of Vitamin B12 in lyophilized royal laver (Porphyra yezoensis), the effects of laver feeding were investigated in Vitamin B12-deficient rats [58]. Urinary methylmalonic acid excretion was undetectable inside xx days of initiating a diet supplemented with dried majestic laver (10 μg of Vitamin B12/kg diet), and the hepatic Vitamin B12 (especially coenzyme Vitamin B12) levels significantly increased. These results indicate that Vitamin B12 obtained from purple laver is bioavailable in rats. A nutritional analysis of 6 vegan children who had consumed vegan diets including brownish rice and dried purple laver (nori) for four–10 years suggested that the consumption of nori may prevent Vitamin B12 deficiency in vegans [sixty]. Our preliminary study indicated that similar dried majestic laver products that are available in local markets in Taiwan (Hong-mao-tai, Bangia atropurpurea) and New Zealand (Karengo, a mixture of P. cinnamonea and P. virididentata) contained 28.v ± 3.ix and 12.iii ± 1.9 μg of Vitamin B12 per 100 g weight, respectively (Figure 2).
For a long time, it was unclear whether algae have an absolute requirement for Vitamin B12 for growth, and why algae that lack a requirement of Vitamin B12 for growth incorporate substantial amounts of Vitamin B12. However, recent biochemical and bioinformatics studies take accurately defined the Vitamin B12 requirements of various algae (half of all algal species absolutely require Vitamin B12 for their growth), and they accept suggested possible physiological functions for Vitamin B12 in algae [61,62].
Furthermore, the standard tables of food composition in Japan [63] indicate that dried royal laver (per 100 thou) contains various other nutrients that are defective in vegetarian diets, such every bit Vitamin A (3600 μg of Vitamin A equivalent every bit provitamin A), iron (10.7 mg), and n-3 polyunsaturated fat acids (1.19 g), besides as Vitamin B12 (77.vi μg). Regal laver as well contains a large amount of a pigment protein, phycoerythrin, which is digested in the intestine to release the covalently linked chromophore moiety, a phycoerthrobilin compound (a stiff antioxidant) [64].
Chlorella tablets (eukaryotic microalgae Chlorella sp.) used in human nutrient supplements contain biologically active Vitamin B12 [65]. Nevertheless, our unpublished study indicates that the Vitamin B12 contents significantly differ amidst various commercially bachelor Chlorella tablets (from zero to several hundred μg of Vitamin B12 per 100 g dry out weight); nosotros do not have any information on why such a huge variation occurs. Thus, vegetarians who consume Chlorella tablets every bit a source of Vitamin B12 should check the nutrition labeling of Chlorella products to ostend their Vitamin B12 contents. High levels of Vitamin B12 are described in the nutritional labels of dietary supplements that contain edible blue-green alga such as Spirulina, Aphanizomenon, and Nostoc. Withal, although substantial amounts of Vitamin B12 were detected in these commercially available supplements using a microbiological Vitamin B12 analysis method, these supplements often contained large amounts of pseudovitamin B12 [66,67,68,69,seventy,71] (Figure 3), which is biologically inactive in humans. Therefore, edible cyanobacteria and their products are not suitable for use as sources of Vitamin B12 for vegetarians.
Structural formulae of Vitamin B12 and pseudovitamin B12. (1) Vitamin B12 and (2) pseudovitamin B12 (7-adeninyl cyanocobamide).
5. Conclusions
A survey of naturally occurring and high Vitamin B12-containing plant-derived food sources showed that nori, which is formed into a canvass and dried, is the most suitable Vitamin B12 source for vegetarians presently bachelor. Consumption of approximately 4 g of dried regal laver (Vitamin B12 content: 77.vi μg /100 g dry out weight) supplies the RDA of ii.4 μg/day. In Japan, several sheets of nori (9 × iii cm2; approximately 0.three grand each) are often served for breakfast. A large amount of nori can be consumed as certain forms of sushi (vinegared rice rolled in nori). In particular, hand-rolled sushi made by wrapping rice and fillings with nori is easy to set up and facilitates the consumption of a big corporeality of nori. When dried royal laver was treated past toasting until the laver's colour inverse from purple to green, the toasting treatment did non affect the Vitamin B12 contents [57]. Dried purple lavers could also be a suitable nutrient item for integration in Italian, French, and other forms of western cuisine. Dried imperial laver is also a rich source of iron and n-three polyunsaturated fatty acids (Figure 4). Dried purple laver is a natural plant product; therefore, information technology is suitable for most vegetarian groups. Among edible mushrooms, relatively high levels of Vitamin B12 were detected in the commercially available shiitake mushroom fruiting bodies, but the Vitamin B12 content significantly varies (1.3–12.7 μg/100 g dry weight), which is significantly lower than that found in dried majestic laver. Notwithstanding, the stale shiitake mushroom fruiting bodies (per 100 g) contain 18.ix mg of Vitamin D2 (ergocalciferol) and 2.0 mg of iron [63], which are too nutrients that vegetarian diets tend to lack. Thus, the apply of these plant-based food sources can significantly improve the nutrient imbalance in vegetarian diets to reduce the incidence of Vitamin B12 deficiency in vegetarians.
Proposed method for improving nutrient imbalance in vegetarian diets using stale regal laver as a Vitamin B12 source in addition to other plant-based food sources.
Author Contributions
All authors equally contributed to the grooming of the manuscript and have canonical the final version.
Conflicts of Interest
The authors declare no conflict of interest.
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