Vitamin B12 - A Nutrition Guide for Vegetarians & Vegans: From Nori to Mushrooms, Omnivores Can Benefit, Too!

With 77µg per 100g of the Nori leaves in the wrapping sushi makes an excellent B12 source, even if you stick to the vegan, no tuna version ;-)

If this is not your first visit to the SuppVersity you will be aware that I am not a exactly a proponent of vegetarianism let alone vegan dieting. Just like any other severely restrictive diet people who don't eat animal products are at an increased risk of nutrient deficiencies.

For vegetarians and even more so for vegans, it is not exactly easy to cover their daily requirements of vitamin A, vitamin D3, iron, cholesterol (yes, cholesterol is an essential nutrient!), n-3 polyunsaturated fatty acids and saturated fats. The most urgently needed nutrient for the average vegetarian / vegan dieter, however is vitamin B12, or cobalamin, as scientists say.

Actually dairy happens to be an excellent B12 source. Why not become lacto-vegetarian?

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Vitamin B12 is a water-soluble vitamin with a key role in the normal functioning of the brain and nervous system, and for the formation of blood. It is one of the eight B vitamins. It is normally involved in the metabolism of every cell of the human body, especially affecting DNA synthesis and regulation, but also fatty acid metabolism and amino acid metabolism. Neither fungi, plants, nor animals - including humans - are capable of producing vitamin B12. Therefore a sufficient intake of vitamin B12 is essential for optimal health.

Even in omnivorous humans, vitamin B12 deficiencies are frequent (Stabler. 2004). Among vegetarians and specifically vegans, it is yet rampant (Pawlak. 2013; Pawlak. 2014).

Figure 1: Reliable data on B12 levels is scarce. Based on surrogate markers and B12 deficiency symptoms scientists are still certain that "B12 deficiency as a worldwide problem." (Stabler. 2004) - one vegetarians are particularly susceptible to.

In the latest review by Pawlak et al. who included only studies that assessed serum vitamin B12 an reported actual percentages of vitamin B12 deficiency (40 studies total)...

• the deficiency prevalence among infants reaches 45%,
• the deficiency among the children and adolescents ranged from 0 to 33.3%, and 
• the deficiency among pregnant women ranges from 17 to 39%, dependent on the trimester

Adults and elderly individuals who follow a vegetarian lifestyle had a deficiency range from 0–86.5%. In general, higher deficiency prevalence was reported in vegans than in other vegetarians.  Accordingly, Pawlak et al. conclude that...

"[...]with few exceptions, the reviewed studies documented relatively high deficiency prevalence among vegetarians. Vegans who do not ingest vitamin B12 supplements were found to be at especially high risk." (Pawlak. 2014)

For vegans, specifically, the scientists recommend the routine use of vitamin B12 supplements to ensure adequate vitamin B12 intake and point out that "[v]egetarians, regardless of the type of vegetarian diet they adhere to, should be screened for vitamin B12 deficiency." (Pawlak. 2014)

Why is it so difficult for vegetarians and vegans to meet their requirements?

The Institute of Medicine’s recommended dietary allowance (RDA) of B12 needed to meet an adult’s requirement as 2.4mg per day. B12 is synthesized only by microorganisms, and this is why natural food sources of B12 are limited to meats and foods of animal origin.

 "Clams and beef liver are the highest sources of B12, containing about 84 and 71mg of B12 in a 3 oz serving (USDA. 2011). The amount of B12 found in a chicken varies from about 3.3mg in the entire chicken liver to 0.03mg in achicken’s neck. Pork contains between 0.3mg of B12 in each sausage patty to about 11.4mg in pork liver. 6 The content of B12 in fish ranges from about 9mg in one half of a fillet of sockeye salmon to about 0.5mg in a 3 oz serving of yellow fin tuna." (Pawlak. 2013)

Needless to say that a vegetarian or vegan person mustn't eat any of the aforementioned "good" B12 sources. The question is thus: Where can a vegan or vegetarian get his B12 from?

Diagnosis of low B12 levels is tricky! The most commonly used cobalamin essay has a sensitivity of "only" 62.6% and produces 22%+ false positives. An often-used alternative, the holotranscobalamin essay is a tad better, but with a sensitivity of 64.7% and 18.4% false positives, not exactly accurate, either (Carmel. 2013). Until now no 100% reliable test is available and studies like Salomon (2005) show that patients with "normal" plasma cobalamin levels, but symptoms vitamin B12 deficiency improve after treatment with the vitamin.

In view of the fact that the name of this website contains the word "supplement", the most obvious and probably safest source are supplements. In that, it's important to point out that not all supplements that promise to solve the vegetarian B12 problems will actually deliver.

Fourteen years ago, Micheal S. Donson tested the efficacy of sublingual cobalamine tablets, nutritional yeast, and probiotic supplements in a group of Hallelujah dieters and other raw-food vegetarians and found that only the former two, i.e. the sublingual cobalamine tablets and the nutritional yeast that contained 5µg of cyanocobalamin per tablespoon brought his subjects' depleted B12 levels back into the normal range. The probiotic supplement, on the other hand, was useless (Donaldson. 2000).

For patients with insufficient intrinsic factor production oral supplements are not suitable, though. For them, only injectable vitamin B12 will reliably bring their levels back up (Katz. 1972). People with low stomach acid, which often occurs with aging, as well, and people with gastric bypass (Smith. 1993) have similar, but less pronounced problems to cover their B12 requirements from oral sources (dietary and supplemental).

Now, supplementation and injections are nice, but isn't is possible to get your B12 from foods without having to eat meat and animal products?

In general, it is possible, but there is one major problem: The total content and bioavailability of vitamin B12 in food sources vegetarians and vegans can eat is comparably low.

Table 1: Content and bioavailability of selected "good" dietary sources of vitamin B12 (Watanabe. 2007)

If you take a look at the data in Table 1 you will see that the only source that can keep up with fish and meat are algae. Chloeralla in particular is an excellent source of dietary B12 for both vegetarians and, if I didn't miss yet another stupid dogma, vegans, as well (Watanabe. 2007).

In a previous study, Watanabe et al. (2002) have found that chlorella tablets, but not spirulina, which contains mostly pseudy vitamin B12 is a suitable source of vitamin B12 for man (and woman ;-).

In a more recent overview of vegetarian and vegan B12 sources, the researchers from the United Graduate School of Agricultural Sciences at the Tottori University in Japan (Watanabe. 2014) compiled a comprehensive overview of suitable B12 sources which includes...

• 

  Are "organic" vegetables worth it? Find out in a previous article.

  Vitamin B12-Enriched Beans and Vegetables Produced Using Organic Fertilizers or Hydroponics -- Previous research has shown that you can significantly increase the B12 content of spinach by adding an organic fertilizer such as cow manure. Practically speaking this is an increase to to approximately 0.14 μg/100 g fresh weight - that's huge considering the fact that "regular" spinach contains < 0.01µg/100g vitamin B12.
  
  In view of the fact that the RDA for B12 is 2.4 μg/day that's still too little to be able to cover your B12 needs from spinach alone. Still, in the future we may be seeing other "high B12" vegetables on the market even non-vegetarian dieters may benefit from.
• Fermented Beans and Vegetables -- The Vitamin B12 content of soybeans is low or undetectable. In the course of the fermentation process soybean products are yet loaded with B12, so that fermented soybeans (Tempe, a traditional Indonesian food that's made of fermented soybeans) can contain up to 8.0 μg B12 per 100g (Nout. 1990)
  
  Comparable increases in B12 content have been observed in vegetables that have been fermented with certain lactic acid or propionic bacteria (up to 10µg/100g; Gupta. 1998).
  
  

  

  "Pesticide pollution: Chinese tea may not be safe to drink," this is what you could read on the website of Greenpeace in 2012, already and obviously this has not changed over the last 2 years | read more

  Tea, of which most people forget that it is fermented (not green tea, though), as well can also contain significant amounts of vitamin B12. For black tea (Batabata-cha), scientists have shown that drinking 50 mL/day, equivalent to a daily dose of 1 ng Vitamin B12, for 6 weeks, compensated the B12 deficiency of B12 deficient rodents (Kittaka-Katsura. 2004). As Watanabe et al. point out, results like these "indicate that Vitamin B12 found in fermented black tea is bioavailable in rats." Unfortunately, the same cannot be said for human beings, where the consumption of 1–2 L of the fermented tea drink, which is equivalent to 20–40 ng of Vitamin B12, is not sufficient to meet the RDA of 2.4 μg/day for adult humans.
• Edible Mushrooms --  Zero or trace levels (approximately 0.09 μg/100 g dry weight) of Vitamin B12 were measured in the dried fruiting bodies of porcini mushrooms (Boletussp.), parasol mushrooms (Macrolepiota procera), oyster mushrooms (Pleurotus ostreatus), and black morels (Morchella conica).
  
  

  

  Figure 2: The micronutrients in nori and dried shiitake mushrooms complement each other perfectly (see bottom line for explanation)

  In contrast, the fruiting bodies of black trumpet (Craterellus cornucopioides) and golden chanterelle (Cantharellus cibarius) contained higher levels of Vitamin B12 (1.09–2.65 μg/100 g dry weight) than the above mentioned mushrooms (Watanabe. 2012).
  
  In addition, high levels of Vitamin B12 were detected in the commercially available dried shiitake mushroom fruiting bodies (Lentinula edodes), which are used in various vegetarian dishes. The Vitamin B12 contents of dried shiitake mushroom fruiting bodies (100 g dry weight) significantly varied and the average Vitamin B12 value is approximately 5.61 μg (Bito. 2014). 

In conjunction with algae and algae supplements the aforementioned vegetarian sources of B12 may in fact be sufficient to cover the daily requirements of 2.4µg of vitamin B12.

Milk has a built-in B12 absorption enhancer (learn more). Now you tell me: Who would ever doubt that nature knows best?

Bottom line: Of all vegetarian B12 sources, nori is the one marine source of vitamin B12, Watanabe et al. highlight in particular. The consumption of only 4g of dried purple laver (Vitamin B12 content: 77.6 μg /100 g dry weight) supplies the RDA of 2.4 μg/day. Moreover, nori can be easily consumed as a wrapping for rice and fillings and retains most of its precious B12 content upon heating (Miyamoto. 2009).

In conjunction with dried shiitake mushroom fruiting bodies that contain 18.9 mg of Vitamin D2 (ergocalciferol) and 2.0 mg of iron, both likewise micronturients vegetarians usually don't get enough of in their diets, the dried purple lavers that are rich sources of n-3 polysaturated fatty acids and can be easily integrated in Italian, French, and other forms of Western cuisine, are thus probably the best non-supplemental source of B12 vegetarians can get | Comment on Facebook!

References:

• Bito, Tomohiro, et al. "Characterization of vitamin B< sub> 12</sub> compounds in the fruiting bodies of shiitake mushroom (< i> Lentinula edodes</i>) and bed logs after fruiting of the mushroom." Mycoscience (2014). 
• Carmel, Ralph. "Diagnosis and management of clinical and subclinical cobalamin deficiencies: Why controversies persist in the age of sensitive metabolic testing." Biochimie 95.5 (2013): 1047-1055.
• Gupta, Uma, E. R. Rati, and R. Joseph. "Nutritional quality of lactic fermented bitter gourd and fenugreek leaves." International journal of food sciences and nutrition 49.2 (1998): 101-108. 
• Katz, Max, Sook K. Lee, and Bernard A. Cooper. "Vitamin B12 malabsorption due to a biologically inert intrinsic factor." New England Journal of Medicine 287.9 (1972): 425-429.
• Kittaka-Katsura, Hiromi, et al. "Characterization of corrinoid compounds from a Japanese black tea (Batabata-cha) fermented by bacteria." Journal of agricultural and food chemistry 52.4 (2004): 909-911.
• Miyamoto, Emi, et al. "Characterization of vitamin B12 compounds from Korean purple laver (Porphyra sp.) products." Journal of agricultural and food chemistry 57.7 (2009): 2793-2796.
• Nout, M. J. R., and F. M. Rombouts. "Recent developments in tempe research." Journal of Applied Bacteriology 69.5 (1990): 609-633.
• Pawlak, Roman, et al. "How prevalent is vitamin B12 deficiency among vegetarians?." Nutrition reviews 71.2 (2013): 110-117.
• Pawlak, R., S. E. Lester, and T. Babatunde. "The prevalence of cobalamin deficiency among vegetarians assessed by serum vitamin B12: a review of literature." European journal of clinical nutrition 68.5 (2014): 541-548. 
• Smith, C. Daniel, et al. "Gastric acid secretion and vitamin B12 absorption after vertical Roux-en-Y gastric bypass for morbid obesity." Annals of surgery 218.1 (1993): 91.
• Solomon, Lawrence R. "Cobalamin-responsive disorders in the ambulatory care setting: unreliability of cobalamin, methylmalonic acid, and homocysteine testing." Blood 105.3 (2005): 978-985.
• Stabler, Sally P., and Robert H. Allen. "Vitamin B12 deficiency as a worldwide problem." Annu. Rev. Nutr. 24 (2004): 299-326.
• USDA National Nutrient Database for Standard Reference, Release 18.Vitamin B12 (mg) Content of Selected Foods Per Common Vitamin B-12 Measure, Sorted by Nutrient Content. 2005; Available at: http://www.nal.usda.gov/fnic/foodcomp/Data/SR18/nutrlist/sr18w418.pdf. Accessed 27 November 2011. 
• Watanabe, Fumio, et al. "Characterization and bioavailability of vitamin B12-compounds from edible algae." Journal of nutritional science and vitaminology 48.5 (2002): 325-331.
• Watanabe, Fumio. "Vitamin B12 sources and bioavailability." Experimental Biology and Medicine 232.10 (2007): 1266-1274.
• Watanabe, Fumio, et al. "Characterization of vitamin B 12 compounds in the wild edible mushrooms black trumpet (Craterellus cornucopioides) and golden chanterelle (Cantharellus cibarius)." Journal of nutritional science and vitaminology 58.6 (2012): 438-441.
• Watanabe, Fumio, et al. "Vitamin B12-Containing Plant Food Sources for Vegetarians." Nutrients 6.5 (2014): 1861-1873.