Warning: Lots of biochemistry discussed below. Hopefully the general ideas of the article will make sense even if you skim over the more technical parts.

A study just came out with a scary title, “Vegetarianism produces subclinical malnutrition, hyperhomocysteinemia and atherogenesis.” The abstract shows that the cross-sectional study measured homocysteine levels (among other disease markers) of a rural population of men living in Chad who were supposedly vegetarian (1). They found homocysteine levels to be elevated and therefore concluded that the men might be at risk for cardiovascular disease. Except for the provocative title, there was nothing particularly interesting in the abstract, and I decided not to pursue it further as there is a steady flow of cross-sectional studies on semi-vegetarians from developed countries and their cardiovascular disease markers.

But a number of people contacted me about it and so I changed my mind. I’m glad I did, as the paper was much more interesting than the abstract, though still not very relevant to vegetarians in developed countries.

Here is a summary. Twenty-four apparently healthy men from a rural part of Chad, a country in Africa, were compared to 15 men from a nearby urban part of Chad. The rural men ate very little animal products and less than their urban counterparts. There is no indication that this was due to any sort of “vegetarianism,” but rather simply because of the food available to them in their area.

Protein intakes for the rural men were an average of 50 g per day compared to 63 g per day for the urban men. The RDA for meat-eating men of that height would be 51 g and the recommended protein intake for vegan men that height would be 57 g. That would put these rural men at a “probably adequate” protein level, in my opinion. However, their average intake of the sulfur amino acids methionine and cysteine was only 10.4 mg/kg while the RDA is 19 mg/kg.

The rural men were marginally suffering from an indicator of protein malnutrition, known as prealbumin (aka as transthyretin), which was at an average level of 176 mg/l (compared to 292 mg/l for the urban men). The lower limit of a healthy prealbumin is listed by most sources as 180 mg/l, while the upper limit of healthy is listed as anywhere from 300 to 400 mg/l.

The B12 levels of the rural vs. urban men were 174 vs. 269 pmol/l. Homocysteine levels of the rural vs. urban men were 19 vs. 11 µmol/l.

Some background: Homocysteine is a byproduct of methionine metabolism and is considered to be a risk factor for heart disease and stroke (among other diseases). Generally, homocysteine is raised by either vitamin B12, folate, or vitamin B6 deficiency. Vegetarians and vegans who do not supplement with vitamin B12 typically have elevated homocysteine levels. A level of 8 µmol/l or below is ideal, whereas greater than about 12 µmol/l is associated with increased risk of disease.

In the past, some people have thought that elevated homocysteine was caused by high levels of methionine in the diet, although this was put to rest some years ago.

Now, here is the interesting part of this study (if you happen to find the folate/methionine cycle interesting). Because the rural men were not technically deficient in vitamin B12, but were marginally protein malnourished, the researchers thought it was not vitamin B12 deficiency that was causing the elevated homocysteine but rather marginal intakes of the amino acid methionine. Their theory is that when you are deficient in methionine, the body produces excess homocysteine from cysteine so that it can then create methionine and, in turn, s-adenosylmethionine (SAMe) which is an important methyl donor for many reactions throughout the body.

My take on this is somewhat different. Although the vitamin B12 levels in the rural men were technically not in the deficiency range, they were not ideal for homocysteine levels. Selhub (2) suggests a minimum vitamin B12 level of 300 pmol/l for minimizing homocysteine levels and this is born out in the current study in that even the urban men with a B12 level of 269 pmol/l had a slightly elevated homocysteine of 10.8 µmol/l while getting plenty of protein.

Despite the title of the study saying that vegetarianism produces atherogenesis, there was no mention of this in the paper. In fact, the cholesterol levels of the rural and urban men were at relatively low levels of 154 and 166 mg/dl respectively (which is not a direct measure of atherogenesis, but low cholesterol levels are often associated with low atherogenesis).

A press release published in SFGate.com did a write-up on the study (which is what caught some people’s attention): Vegetarian Diet Might Increase the Risk of Cardiovascular Diseases, According to a Recent Study, Says Nutri-Med Logic Corp. While I would not describe their release as terribly inaccurate, they fail to mention that the study was of semi-vegetarians in Chad who were arguably malnourished. Their suggestion of supplementing with alpha-lipoic acid to combat what is either B12 or protein malnutrition is a stretch.

The take home message from this study is: People who limit animal product consumption need a regular source of vitamin B12. People who follow a vegetarian diet due to a lack of food in an area with low amounts of available plant protein could become protein malnourished and this could possibly exacerbate elevated homocysteine levels. Vegans in developed countries can easily avoid these problems by supplementing with vitamin B12 and getting enough protein.

References

1. Ingenbleek Y, McCully KS. Vegetarianism produces subclinical malnutrition, hyperhomocysteinemia and atherogenesis. Nutrition. 2011 Aug 26. [Epub ahead of print] Link

2. Selhub J, Jacques PF, Dallal G, Choumenkovitch S, Rogers G. The use of blood concentrations of vitamins and their respective functional indicators to define folate and vitamin B12 status. Food Nutr Bull. 2008 Jun;29(2 Suppl):S67-73. Review. Link

I’ve been reviewing the scientific literature on protein and bone health. As many readers know, there has been a theory that animal protein, by way of increased sulfur amino acids, causes calcium excretion leading to osteoporosis. This theory was always on shaky ground and more recent evidence has contradicted the theory. I just read a meta-analysis on the subject and added the following to the article, Bones, Vitamin D, and Calcium, on VeganHealth.org:

“Another 2009 meta-analysis found that among five well-designed studies measuring calcium balance, net acid excretion was not associated with either decreased calcium balance or a marker of bone deterioration (48).”

The paper had an interesting list of cohort studies in the discussion:

“First, during 8 yr of follow-up, fracture risk was not reduced among a cohort of 36,217 postmenopausal women who consumed either lower protein or lower NAE [net acid excretion] diets (37). Second, wrist fracture risk was highest among 1865 peri- and postmenopausal women who consumed the lowest protein intakes over 25 yr of follow-up (38). As well, a recent 2-yr trial in 276 postmenopausal women either supplemented with potassium citrate (expected to neutralize the acid of the Western diet) or encouraged to consume increased fruit and vegetables showed that these interventions did not reduce bone turnover or decrease bone loss (36).”

The take home message, which I’ve written about before, is that not eating animal protein does not protect you from osteoporosis. Make sure you get enough calcium, vitamin D, and even (plant) protein.

References

36. Macdonald HM, Black AJ, Aucott L, Duthie G, Duthie S, Sandison R, Hardcastle AC, Lanham New SA, Fraser WD, Reid DM. Effect of potassium citrate supplementation or increased fruit and vegetable intake on bone metabolism in healthy postmenopausal women: a randomized controlled trial. Am J Clin Nutr. 2008 Aug;88(2):465-74. (Link) Free article available.

37. Dargent-Molina P, Sabia S, Touvier M, Kesse E, Bréart G, Clavel Chapelon F, Boutron-Ruault MC. Proteins, dietary acid load, and calcium and risk of postmenopausal fractures in the E3N French women prospective study. J Bone Miner Res. 2008 Dec;23(12):1915-22. (Link) Free article available.

38. Thorpe DL, Knutsen SF, Beeson WL, Rajaram S, Fraser GE. Effects of meat consumption and vegetarian diet on risk of wrist fracture over 25 years in a cohort of peri- and postmenopausal women. Public Health Nutr. 2008 Jun;11(6):564-72. Epub 2007 Aug 9. (Link) Free article available.

48. Fenton TR, Lyon AW, Eliasziw M, Tough SC, Hanley DA. Meta-analysis of the effect of the acid-ash hypothesis of osteoporosis on calcium balance. J Bone Miner Res. 2009 Nov;24(11):1835-40. (Link)

A study was published in the Journal of the American Dietetic Association’s August issue doing an analysis of protein and weight gain. The odd thing about it was that they used data from a cohort of male employees of the Chicago Western Electric Company — from the 1950s!

In any case, they found that, after 7 years of follow-up, animal protein intake was associated with being overweight and obese, but vegetable protein was the opposite — inversely associated with being overweight. This would be a no-brainer except that they found this independent of calories, fat, and carbohydrate. The findings were highly significant.

The researchers theorized that the different amino acid composition of the animal vs. vegetable protein could account for the difference.

It would have been interesting to see a cohort study done like this in which fat-free mass was included as a variable. In other words, did the people eating more animal protein have a higher muscle mass leading to a higher body mass index (the measure of overweight and obesity)? But even if it did, I’d be surprised if it could make up for the high level of statistical significance. Further research is needed!

Citation

Bujnowski D, Xun P, Daviglus ML, Van Horn L, He K, Stamler J. Longitudinal Association between Animal and Vegetable Protein Intake and Obesity among Men in the United States: The Chicago Western Electric Study. J Am Diet Assoc. 2011 Aug;111(8):1150-1155. (Abstract)

Good news from Germany:

Germany’s Strongest Man Is A Vegetarian

Excerpt:

Now I have proven finally, that being vegetarian makes you a better athlete!

It certainly proves that being vegetarian does not prevent someone from being extremely strong.

I’ve often heard the argument that since breast milk is only 6% protein (by calories), and since infancy is the time of most rapid growth, adults should need even less than 6% of their calories to be from protein.

Ginny Messina just wrote an interesting artice on why that is not the case:

Link

The reason I have not yet commented on the vitamin D news of yesterday is because I have been working for a couple weeks on updating the VeganHealth protein page. In the midst of doing that, Voracious Vegan became a voracious omnivore, which distracted me. But, it made the subject of protein even more relevant because I have a sneaking suspicion some vegans are not eating an ideal amount.

In particular:

• Legumes, quinoa, and pistachios are the only plants foods high in the amino acid lysine. If you are not eating them every day, you might be falling short of lysine needs.
• There is evidence that people over 60 should be eating well above the RDA for protein to prevent muscle and bone loss.

I encourage everyone to give it a read, at least through Lysine: The Limiting Amino Acid in Vegan Diets, and the next section, Protein Needs for People Over 60, if you happen to be over 60. The rest of the text is technical details that are not necessary for everyone to read, although if you are skeptical that vegans need as much protein as I’m suggesting, you might want to read the entire page.

Link

Dear Jack,

I recently got into a debate with a friend who insisted that quinoa, hemp, amaranth, buckwheat, and spirulina are all complete proteins. When I told him soy is the only complete vegetarian protein, he told me he avoids all soy due to its negative effect on men’s health. I wondered where this guy learned this and a quick google search on vegetarian complete proteins got me here. I checked out your page on protein. That chart listing the essential amino acids in so many plant foods made me realize that in fact many plant foods do contain all the essential amino acids but at such low levels it’s hard to list them as ‘complete proteins’ in the true meaning intended. So my take is that the only vegetarian protein that comes close to really being a complete protein (meaning it has essential amino acid levels similar to those of animal proteins) is soy. Would you agree?

Answer:

[As an aside, the research to date indicates that moderate amounts of soy do not harm men’s health.]

Because this question about complete proteins comes up on a regular basis, I decided to do some number crunching to get to the bottom of it. Mind you, there are many more numbers to crunch if someone wanted to take the time, but I think I’ve covered enough to draw some conclusions.

I see two ways of looking at the question of whether a food has complete protein:

If you look at Table 3 of Where Do You Get Your Protein?, you will see what it takes to meet the RDA for each EAA for a variety of foods.

I have taken some of the data from Table 3 and constructed the table below to look more closely at what foods might contain a “complete protein”. In the table below, the numbers in the right-hand column represent the following equation:

Where:

From the chart above, it appears that tuna is the most complete protein with a range of only .4 servings and only 1.7 servings required to meet the RDA for all the EAA. Chicken, beef, edamame (whole, cooked soybeans), lentils, and pinto beans all do quite well. I think it’s fair to consider all of them a “complete protein”. Tofu, milk, quinoa, soy milk, and eggs do significantly better than most grains and nuts which have a much wider range.

As for spirulina…not so much.

One thing to note about this is that all the numbers depend on the serving size. I tried to pick what I thought were reasonable (or common) serving sizes for each food (you can see what they are in Table 3).

The USDA database has a lot of specific entries for some of the food categories above (like ground beef). I chose what looked like a common version of the food, but I did not average the data across more than one version.

As for the remaining, supposed complete proteins mentioned in the original question above, here is what I found:

Amaranth
The USDA lists 9 g of protein per cup of cooked amaranth. That’s a good amount when compared to other grains, but I’m not sure if it’s as easy to eat a cup of amaranth as a cup of, say, rice or corn. The USDA had no amino acid info.

Hemp
There was no info in the USDA database. I found many sources saying that it is a complete protein but none that I know to be reliable.

Nutritional yeast
No info in the USDA database. According to this site, it has 9 g of protein per 3 tbsp serving. That’s a decent amount, but I’m not sure if we can trust that info.

In conclusion, edamame, lentils, and pinto beans fared pretty well with chicken and beef for being a complete protein. Tofu, soymilk, and quinoa were on par with eggs and milk.

I am happy to report that we have updated and added a feature to the protein page at VeganHealth.org. If you scroll down to Table 3, you can now type in your ideal body weight, click Submit, and the table will show you how many servings of the listed foods it would take to meet the RDA for protein and the essential amino acids.

Of course, you shouldn’t get all your protein from just one food, but it can give people an idea of what might be required from various food combinations. It’s also not important for everyone to meet the RDA for protein; some people need less.

I’d like to thank Vegan Outreach’s volunteer, Jean B., for all the work she has done to make VeganHealth.org look nicer! She has been redoing the pages one at a time and I really appreciate all her help!

The Fall 2009 issue of Vegetarian Voice magazine, the newsletter of the North American Vegetarian Society, has an article by Amy Joy Lanou and Michael Castleman, “A Whole Diet Approach to Building Better Bones.”

I will quote from the article to sum up their arguments:

“[W]e have known for at least 20 years that fracture rates are highest in areas where dairy and calcium consumption are also the highest.”

“Research shows that a low-acid diet, one that is high in fruits and vegetables and devoid of (or low in) animal protein (meats, poultry, fish, milk, eggs and cheese) helps keep calcium in bones.”

“[Osteoporosis is] actually a disease of calcium imbalance. Drinking milk and eating dairy foods provides calcium – but these foods are so high in protein that they draw more calcium out of bone then they replace.”

“We do need some calcium. The World Health Organization recommends 400 to 500 mg/day for people in countries at high risk of osteoporosis.”

“The best approach to osteoporosis prevention – the only one that makes scientific sense – is a diet very low in or devoid of animal foods and high in fruits and vegetables, combined with walking or equivalent exercise for 30 to 60 minutes a day, every day.”

If you have been following vegan nutrition advocacy for the past two decades, nothing above should be new to you. And here are the major problems I have with it:

1. Most non-vegans in Western countries get around 800 to 1200 mg of calcium per day. At this level of intake, I agree that there is little evidence that to prevent osteoporosis one needs even more calcium. However, Lanou and Castleman imply that all you need is a vegan diet containing 400 – 500 mg of calcium per day and walking for 30 to 60 minutes for strong bones. And they leave out the most important study published to date on bone health and vegans, a 2007 report from the EPIC-Oxford study which showed that vegans had a 30% higher rate of bone fractures than did meat-eaters and lacto-ovo vegetarians!

In that study, the vegans who got more than 525 mg of calcium had the same rate of bone fractures as the meat-eaters and lacto-ovo vegetarians, showing that vegans need more than 525 mg of calcium. (In the study, 32% of vegans had calcium intakes between 525 and 699 mg per day, and 24% had greater than 699 mg per day.)

This is the only study looking at the bone fracture rates of vegans.

2. Lanou and Castleman base most of their argument on the idea that animal protein leeches calcium from the bones. As I posted a few weeks ago, a meta-analysis looking at bone health and fractures found that “Overall, the weight of the evidence shows that the effect of dietary protein [including animal protein] on the skeleton appears to be favorable to a small extent or, at least, is not detrimental.”

In my opinion, the argument that a primary cause of osteoporosis is animal protein has always been on shaky ground.

3. Lanou and Castleman leave vitamin D out of their final recommendations (they briefly mention you can get it from the sun earlier in the article). Vitamin D can be a significant problem for many vegans and needs to be addressed in discussions of bone health.

4. I do not see why it is necessary to make an argument that people only need 400 to 500 mg of calcium per day, when the evidence is so lacking (and actually points in the other direction). What harm could come from encouraging vegans to get at least the low end of what is a normal amount of calcium (like 700 to 800 mg/day) in Western countries? None. But what harm could come from vegans not getting that much? Only osteoporosis!

In summary, there is no direct evidence that a vegan diet with only 400 to 500 mg of calcium per day prevents osteoporosis. The direct evidence is just the opposite.

More info on vegan diets and bone health.

A meta-analysis looking at protein intake and bone health was published this month in the American Journal of Clinical Nutrition (1).

In terms of bone mineral density (BMD), the authors reported:

“Overall, there was very little evidence of a deleterious influence of protein intake on BMD, with most cross-sectional surveys and cohort studies reporting either no influence or a positive influence. Thus, 15 cross-sectional surveys found a statistically significant positive relation between protein intake and at least one BMD site. However, 18 studies found no significant correlation between protein intake and at least one BMD site.

“The cohort studies also identified little evidence of any deleterious influence of protein intake on bone. … [N]o studies showed a significant increase in BMD loss with increased protein intake, and only one study showed a significant decrease in BMD loss with increased animal and total protein intakes.”

In terms of bone fracture rates, the authors reported:

“Overall, the [seven] cohort studies indicated either a benefit or no effect of protein intake on hip fracture relative risk, with only one study reporting a significant increase in risk with increasing animal protein intake and increasing animal to vegetable protein ratio. Three studies found a decreased relative risk of hip fracture with increasing animal, total, and vegetable protein intakes. Two studies found no significant association of animal protein with fracture risk, whereas 2 studies found no association of total protein with fracture risk. Last, 2 studies found no relation between fracture risk and vegetable protein.”

In summary:

“Overall, the weight of the evidence shows that the effect of dietary protein on the skeleton appears to be favorable to a small extent or, at least, is not detrimental. However, the long-term clinical importance of the effect is unclear, and a reduction in fracture risk was not seen. More research is required to resolve the protein debate. In the meantime the protein intakes and balance of different protein sources as indicated in the current healthy eating guidelines represent appropriate dietary advice.”

Reference

1. Darling AL, Millward DJ, Torgerson DJ, Hewitt CE, Lanham-New SA. Dietary protein and bone health: a systematic review and meta-analysis. Am J Clin Nutr. 2009 Dec;90(6):1674-92. Epub 2009 Nov 4.