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B12 in Tempeh, Seaweeds, Organic Produce, and Other Plant Foods

Summary: The only plant foods which have been tested for B12 activity using the gold standard of lowering MMA levels in humans are dried and raw nori from Japan. Dried nori made MMA status worse, indicating that it can reduce B12 status and can possibly harm people who are B12-deficient. Raw nori kept MMA levels about the same, indicating that it didn't harm B12 status, but it did not help either.

No food in Europe or the U.S. has been tested for lowering MMA levels. Thus, the discussion about whether Western vegans can get B12 from plant foods can, and probably should, end here (until proper research is conducted). Because so many plant foods have failed other tests that do not measure up to the MMA lowering test, and because there are so many false rumors being passed around, the studies of B12 in plant foods are examined in detail below.

Of all the foods studied below, only tempeh in Indonesia or Thailand, dulse, Chlorella, raw nori, Aphanizomenon flos-aquae, and coccolithophorid algae warrant much further attention for providing B12. Unless these foods are shown consistently to correct B12 deficiency, vegans should not rely on them as a B12 source.

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Contents of B12 in Tempeh, Seaweeds, Organic Produce, and Other Plant Foods

Introduction

It would be great to find a reliable plant source of B12 for vegans. One might get the opposite impression given my level of critique of some of these studies. My skepticism is only due to the potential harm from relying on a food that contains inactive B12 analogues which can make a B12 deficiency even worse.

There has been a long history of misconceptions about which, if any, plant foods are sources of B12. Much of this stems from the methods of measuring B12 analogues. Other confusion stems from bacterial contamination that occurs in some foods but not others. Please see Measuring B12 in Plant Foods: Why the Confusion? for an explanation of the methods for for measuring B12 analogues in plant foods.

Unlike animals, most, if not all, plants have no B12 requirement for any function, and therefore have no active mechanisms to produce or store B12. Many seaweeds have been shown to have B12 analogues.

Most seaweeds are macroalgae, which are technically not plants. Some microalgae contain an enzyme that can use cobalamin, but also have an enzyme with the same function that does not require cobalamin in case it is not present. These macroalgae do not make their own cobalamin, but rather have a symbiotic relationship with cobalamin-producing bacteria.1 Note that I am purposefully using the term "cobalamin" rather than "vitamin B12" because it is not clear if these cobalamins are active vitamin B12 in humans.

During the 1970s, two enzymes in plants (potatoes and bean seedlings) were found to respond to the addition of adenosylcobalamin2,3 (a co-enzyme form of B12). One explanation is that adenosylcobalamin provides some factor that is usable by these enzymes, but that adenosylcobalamin is not required by these plants for growth. Thus far, these plants have not been shown to counteract B12 deficiency symptoms (though I am not aware of any well-designed attempts as it is assumed that they do not contain B12). It is probably safe to assume that many vegans who have developed severe B12 deficiency ate potatoes and beans.

There are some rumors, though no evidence of which I am aware, that if you let organic produce, such as carrots, sit at room temperature for a few hours, bacteria on the surface of the carrots will produce B12. For this to happen, specific species of bacteria would be required, as would cobalt. Until there is research showing that such a method can lower MMA levels, such produce should not be considered to provide B12.

Notes for Introduction
1. Smith AG, Croft MT, Moulin M, Webb ME. Plants need their vitamins too. Curr Opin Plant Biol. 2007 Jun;10(3):266-75. Epub 2007 Apr 16. Review.
2. Poston JM. Coenzyme B12-dependent enzymes in potatoes: leucine 2,3-aminomutase and methylmalonyl-coa mutase. Phytochemistry. 1978;17:401-402.
3. Poston JM. Leucine 2,3-aminomutase: a cobalamin-dependent enzyme present in bean seedlings. Science. 1977;195:301-302.

Plant Foods with Practically No Detectable B12 Analogue

Various studies have tested the foods in the table below for B12 analogues and found none. To my knowledge, other than in Mozafar's studies (below) in which B12 and cow dung were carefully added to the soil of potted plants, no published study has shown any B12 analogues in any of these foods.

Foods with No Detectable B12 Analogue
amesake rice1 barley miso1 miso2 natto2
rice miso1 shoyu1 tamari1 umeboshi prunes1
various fruits, vegetables, nuts,
seeds, & grains2 		 

The following table shows the B12 analogue content of various plant foods:

B12 Analogue Content (µg/30 g) of Various Foods
Country Netherlands1 Thailand2,3
Assay IF IF or R-proteinA
fermented soybean   0.15
barley malt syrup
sourdough bread
parsley
shiitake mushrooms		 .006-0.1
Only info given 		 
dried fermented soybean   0.01
tofu ND 0.02
soybean paste   0.03
soy sauce   .01B
A - Used an assay method by Lau et al.57 (1965) which uses R-protein or IF
B - µg/30 ml
IF - Intrinsic Factory Assay
ND - None Detected

As you can see, there are very small amounts, if any. Since the amounts are so small, any inactive analogues should not significantly interfere with an individual's active B12 from other sources, and if the analogue is active B12, it will not provide much. Thus, these foods should neither add to, nor detract from, a vegan's B12 status.

Notes for Plant Foods with Practically No Detectable B12 Analogue
1. van den Berg H, Dagnelie PC, van Staveren WA. Vitamin B12 and Seaweed. Lancet Jan 30, 1988.
2. Areekul S, Churdchu K, Pungpapong V. Serum folate, vitamin B12 and vitamin B12 binding protein in vegetarians. J Med Assoc Thai 1988 May;71(5):253-7.
3.Areekul S, Pattanamatum S, Cheeramakara C, Churdchue K, Nitayapabskoon S, Chongsanguan M. The source and content of vitamin B12 in the tempehs. J Med Assoc Thai 1990 Mar;73(3):152-6.

Tempeh

For a long time, tempeh has been said to contain B12. Table A.3 shows the results of measuring B12 analogue in various tempehs.

B12 Analogue Content (µg/30 g) of Tempehs
Country Netherlands1 USA2 Indonesia3,4
Assay IF IF IF or R-proteinA
tempeh ND .02C .054-1.2B
A - Used an assay method by Lau et al.57 (1965) which uses R-protein or IF
B - 10 commercial tempeh samples purchased from various markets in Jakarta, Indonesia
C - Cooked for 60 minutes
IF - Intrinsic Factory
ND - None Detected

The studies in the USA and in The Netherlands showed little to no B12 analogue.

In contrast, Areekul et al.4 (1990, Indonesia/Thailand) found more significant amounts of B12 analogue. Tempeh production requires molds belonging to the genus Rhizopus. These were found not to produce B12 analogues in Areekul et al's study. Rather, a bacterium, identified as Klebsiella pneumoniae, was isolated from the commercial tempeh starter and determined to be the B12 analogue source. This confirmed Albert et al.'s5 (1980) finding that the Klebsiella genera could produce B12 analogues. In Albert's study, the analogue was thought to be active B12. Whether the analogues found by Areekul et al. were the same as in Albert's study is not known. Given that K. pneumoniae is not required for tempeh production, we can conclude that the B12 analogue found in the tempeh's in Indonesia were due to bacterial contamination (though apparently common there). Tempeh in Europe and the U.S. cannot be relied on as a source of B12. Until tempeh in Indonesia are shown to reduce MMA levels, it should not be relied upon there, either.

Notes for Tempeh
1. van den Berg H, Dagnelie PC, van Staveren WA. Vitamin B12 and Seaweed. Lancet Jan 30, 1988.
2. Specker BL, Miller D, Norman EJ, Greene H, Hayes KC. Increased urinary methylmalonic acid excretion in breast-fed infants of vegetarian mothers and identification of an acceptable dietary source of vitamin B-12. Am J Clin Nutr 1988 Jan;47(1):89-92.
3. Areekul S, Churdchu K, Pungpapong V. Serum folate, vitamin B12 and vitamin B12 binding protein in vegetarians. J Med Assoc Thai 1988 May;71(5):253-7.
4. Areekul S, Pattanamatum S, Cheeramakara C, Churdchue K, Nitayapabskoon S, Chongsanguan M. The source and content of vitamin B12 in the tempehs. J Med Assoc Thai 1990 Mar;73(3):152-6.
5. Albert MJ, Mathan VI, Baker SJ. Vitamin B12 synthesis by human small intestinal bacteria. Nature 1980;283(Feb 21):781-2.

Blue-Green Algae

Blue-green algae are also known as cyanobacteria, blue-green bacteria, and cyanophyta. They are not actually algae, but rather organisms with characteristics of both bacteria and algae. They can peform photosynthesis and are thought to be the ancestors to chloroplasts in algae and plants.

    Aphanizomenon Flos-aquae

    Cell Tech and some other companies market algae from Klamanth Lake in Oregon. Cell Tech markets a species, Aphanizomenon flos-aquae, they call Super Blue Green Algae (SBGA). On April 16, 2003, Cell Tech's site stated:

    "Is the vitamin B12 in SBGA bioavailable and bioactive? Yes. The Super Blue Green Algae (SBGA) strain, Aphanizomenon flos-aquae, has been tested by Lancaster Labs for B12 analog levels using microbiological testing methods that are comparable to methods 952.20 and 960.46 of the Association of Analytical Chemists (AOAC). Unlike other plant foods such as Spirulina, which contain corrinoids with virtually no vitamin B12 activity, Aphanizomenon flos-aquae is a reliable source for vegetarians seeking to supplement their diets with a bioactive form of this important nutrient."

    However, test methods 952.20 and 960.46 use Lactobacillus leichmannii,1 which can measure non-B12 corrinoids.2 See the table Test Organisms for B12 Microbiological Assays in Measuring B12: Why the Confusion? Thus, it can only be concluded that Cell Tech's SBGA contains B12 analogues whose activity is yet to be determined.

    2010 Update: It appears that Cell Tech is now the company, Simplexity Health, and is no longer touting SBGA as a source of vitamin B12.

    In a 2009 study from Italy3, researchers gave Aphanizomenon flos-aquae to 15 vegans. First there was a washout period in which the vegans took no supplemental B12 for 3 months. They were then given 6 capsules of Klamanth Algae from Nutratec (which also contained digestive enzymes to help absorption).

    Here are the results:

    Supplementation with Aphanizomenon flos-aquae
    MarkerBaseline3 mosA6 mosB
    Homocysteine (µmol/l)13.715.2^12.0*
    Serum B12 (pg/ml)259196^237
    Folate (ng/ml)11.010.912.5
    ^Statistically significant difference from baseline.
    *Statistically significant difference from 3 months.

    The results show that the average homocysteine level went down. The authors believe tihs is an indication that Aphanizomenon flos-aquae is a source of active vitamin B12, and that it "warrants further larger, and longer-term randomized trials to confirm such preliminary conclusions."

    Here are some problems with the study:

    1. The authors state in the paper that homocysteine is the most reliable marker for B12 activity, but it is not. Homocysteine levels can be affected by folate intake and, to a lesser extent, vitamin B6. Methylmalonic acid levels are the most reliable marker for B12 activity. This is well known and uncontroversial, so it is odd that the researchers did not know this.
    2. The authors noted that vitamin B6 could not have reduced the homocysteine levels because the algae has very little. They also said that folate levels could not have affected them, but in looking at the results, folate levels did increase (even thought the difference was not statistically signifcant).
    3. The homocysteine levels of these vegans started out pretty high, and when the study ended they were still much too high. A safer level is closer to 6 - 8 µmol/l.
    4. One subject's homocysteine level increased, and one subject's homocyesteine level that was about 10 µmol/l did not respond to the aglae supplementation.
    5. The researchers obtained the algae directly from a company that produces it. It would be more reassuring if the algae was purchased in a store where the company didn't realize it was going to be tested.

    In another study from Italy (2002)4, vegetarians had really high homocysteine levels (25 µmol/l). This is much higher than almost all other studies, which makes one wonder what's going on in Italy.

    In conclusion, it appears that Aphanizomenon flos-aquae might provide some vitamin B12 activity in humans. On the other hand, it did not succeed in lowering homocysteine to an ideal level whereas vitamin B12 supplements do succeed at doing so. At this time, it would be prudent not to rely on it for optimal health.

    Notes for Aphanizomenon Flos-aquae
    1. Helrich K, ed. Official Methods of Analysis, Volume 2: Food Composition; Additives; Natural Contaminants, 15th Edition. Arlington, VA: Association of Official Analytical Chemists, Inc; 1990.
    2. Schneider Z, Stroinski A. Comprehensive B12. New York: Walter de Gruyter, 1987.
    3. Baroni L, Scoglio S, Benedetti S, Bonetto C, Pagliarani S, Benedetti Y, Rocchi M, Canestrari F. Effect of a Klamath algae product ("AFA-B12") on blood levels of vitamin B12 and homocysteine in vegan subjects: a pilot study. Int J Vitam Nutr Res. 2009 Mar;79(2):117-23.
    4. Bissoli L, Di Francesco V, Ballarin A, Mandragona R, Trespidi R, Brocco G, Caruso B, Bosello O, Zamboni M. Effect of vegetarian diet on homocysteine levels. Ann Nutr Metab. 2002;46(2):73-9.

    Spirulina

    The following table shows the B12 analogue content (µg/30 g) of various spirulina batches:

    B12 Analogue Content (µg/30 g) of Spirulina
    Country Netherlands1 USA2 Japan3
    Assay IF L. leich. IF L. leich. L. leich. IF PC
    spirulina 14.5 67 36.7 193.1 73 2.5 0.44
    spirulina     6 35.3 38 1.9 0.32
    spirulina     1.67 8.7 44 5.2 0.88
    IF - Intrinsic Factory Assay
    PC - Paper Chromotography Assay

    The wide range of B12 analogues from one measurement method to another indicates that spirulina has a wide variety of different analogues, many of which are inactive. Some may interfere with B12 activity in humans.

    Notes for Spirulina
    1. van den Berg H, Dagnelie PC, van Staveren WA. Vitamin B12 and Seaweed. Lancet. Jan 30, 1988.
    2. Herbert V, Drivas G. Spirulina and Vitamin B12. JAMA. 1982;248(23):3096-7.
    3. Watanabe F, Katsura H, Takenaka S, Fujita T, Abe K, Tamura Y, Nakatsuka T, Nakano Y. Pseudovitamin B(12) is the predominant cobamide of an algal health food, spirulina tablets. J Agric Food Chem. 1999 Nov;47(11):4736-41.

Seaweeds (Macroalgae)

Soil and Organic Produce as a B12 Source for Vegans

It is common in vegan circles to hear that if your produce has soil on it and you do not wash the produce before eating it, bacteria that lives in the soil and on the produce will provide B12. It is also claimed that in today's world, our food supply is very sanitized whereas in the past, vegan humans would have received plenty of B12 from the unsanitized produce. What is the evidence for these claims?


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