Note: this article is co-authored by Jack Norris, RD and Ginny Messina, MPH, RD and appears on Ginny’s blog as well as this one.

Vegans typically have lower calcium intakes than other vegetarians and meat-eaters. But just how much does this matter?

The popular thinking has long been that it doesn’t matter much at all. According to the acid-ash hypothesis of osteoporosis, vegans experience smaller calcium losses since we don’t eat animal protein. The theory is that calcium is “leached” from bones to counter acidic conditions caused by animal protein.

It’s supported by studies that find higher levels of both calcium and acidic compounds in the urine when people are fed big doses of animal protein (1). This is also supposedly why hip fracture rates are higher in countries with high animal protein intakes (2).

But while the theory had great support several decades ago, it hasn’t held up to the scientific evidence. An article by vegan dietitian Dr. Reed Mangels, based on a presentation she gave at the Sixth International Congress on Vegetarian Nutrition sums up the more recent research very well (3). It should be required reading for all vegan and vegetarian nutrition professionals.

Unfortunately, a quick Google search of “vegan-calcium-bone-health” shows that many vegan educators, including some who are health professionals, are still promoting the idea that protein causes calcium loss from bones.

We thought it would be interesting to see where vegetarian dietitians fit into all of this. So, we created a true/false questionnaire about bone health, protein and vegan diets. We asked dietitians who subscribe to the email list for the Vegetarian Nutrition Dietetic Practice Group (VNDPG) to answer the questions.

Although this was a small, unscientific survey, the results were interesting. They showed that VNDPG members were more aware of the issues than the general vegan community and are sharing better information than what is often available on the internet and elsewhere. But in some cases, even RDs weren’t aware of the newer research on protein and bone health.

Here is the survey with our answers.

1. Protein contributes to bone structure. TRUE

Most RDs got this one right. Bone contains collagen and other proteins and you can’t build and maintain bones without protein (4).

2. Protein from animal foods causes calcium loss from bones. Probably FALSE

According to a 2009 meta-analysis of epidemiological studies, protein is not harmful to bone health and may be beneficial (5). Particularly relevant to vegetarians, in the Adventist Health Study-2, vegetarians who ate the most protein-rich foods like legumes and veggie meats, had the fewest fractures (6). It’s true that studies link higher protein intake with higher urinary calcium losses. But this is in response to eating isolated proteins, not protein-rich foods (7). The phosphorus in those higher-protein foods seems to cancel out the effect on bone loss. Protein also improves calcium absorption when calcium intakes are low (8), so it’s possible that the higher amounts of calcium in the urine simply reflect that greater amounts being absorbed from the diet.

In fact, another 2009 meta-analysis—this one looked at clinical studies—found that the amount of calcium lost in the urine didn’t correlate with calcium balance in the body or with markers of bone health (9). That is, acidic conditions didn’t produce a net loss of calcium from the bones.

The studies comparing hip fracture rates among countries have also been called into question. Since they’re ecological studies, they don’t control for anything and are only marginally useful.

Better information comes from The Hong Kong Osteoporosis Study. This research found that hip fracture rates were lower in Hong Kong than Sweden but that spinal fracture rates were higher (10). And while that seems conflicting, it’s really not. Hip fracture rates are affected less by bone health and more by the likelihood of falling. Spinal fractures, on the other hand, actually reflect bone health. In fact, the researchers said that despite lower hip fracture rates, the Hong Kong women had more osteoporosis.

3. Drinking cow’s milk promotes osteoporosis. Probably FALSE but maybe TRUE

Given the discussion above, it doesn’t seem that the protein in milk would raise risk for osteoporosis. But, research published just last week did raise questions about the effects of milk-drinking on bone health.

The Swedish researchers found that women who drank more than 3 glasses of milk per day had a much higher rate of fracture than those who drank less than a serving (11). In contrast, though, they found that cheese and yogurt were associated with lower rates of fracture. Earlier research in Adventists also found a protective effect of cheese on bone health (12).

One possible explanation, according to the Swedish researchers, is that the sugar galactose—high in milk, but low in cheese and yogurt—is the factor affecting fractures. The research supporting this is in animals, though.

Although it would be premature to say that milk raises fracture risk, there isn’t much evidence that milk-drinkers have any particular health advantage, either. Since we oppose dairy consumption on ethical grounds, it seems like it’s enough to know that nobody actually needs dairy foods in their diet.

4. Research shows that vegans have fewer bone fractures than meat-eaters. FALSE

What evidence we have for this — and admittedly, it’s very little — isn’t especially favorable for vegans. In the EPIC-Oxford study, vegans had a 30% higher risk for fracture after adjusting for numerous variables like age, smoking, alcohol consumption, and physical activity. After adjusting for calcium intake, however, there was no difference in fracture rates. Vegans who got enough calcium were no more likely to break a bone than milk-drinkers (13).

Likewise, in the Adventist Health Study-2, there was a trend toward higher fracture rates among the vegans compared to other vegetarians as well as non-vegetarians (6). (This study didn’t test for statistical significance.)

5. People eating plant-based diets have lower calcium needs than meat-eaters. Probably FALSE

If protein doesn’t have a negative effect on bone health, then there is no reason to think that vegans have lower calcium needs. The EPIC-Oxford study mentioned above suggests that the lower calcium intakes that are typical of vegans may be harmful.

6. The US RDAs for calcium are similar to the World Health Recommendations. TRUE

A common belief is that the WHO recommends just 400 to 500 milligrams of calcium per day. But, the WHO recommends 1000 mg of calcium for adults which is the same as the US RDAs.

Two last questions on our survey looked at the more holistic story of diet and bone health.

7. Weight-bearing exercise is important for bone health TRUE

8. A variety of nutrients including vitamin D, potassium, magnesium, and calcium is needed for healthy bones. TRUE

No surprise that 100% of our respondents knew that bone health is about much more than calcium. No single nutrient or food can make or break the strength of your bones. Keeping bones strong takes a whole diet and lifestyle approach. Getting enough calcium is just one part of that, but it is still an important part. Right now, there is no reason to think that vegans have any particular advantage where this is concerned.

References

1. Schuette SA, Linkswiler HM. Effects on Ca and P metabolism in humans by adding meat, meat plus milk, or purified proteins plus Ca and P to a low protein diet. J Nutr 1982;112:338-49.

2. Frassetto LA, Todd KM, Morris RC, Jr., Sebastian A. Worldwide incidence of hip fracture in elderly women: relation to consumption of animal and vegetable foods. J Gerontol A Biol Sci Med Sci 2000;55:M585-92.

3. Mangels AR. Bone nutrients for vegetarians. Am J Clin Nutr 2014;100:469S-475S.

4. Boskey AL, Coleman R. Aging and bone. J Dent Res 2010;89:1333-48.

5. 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.

6. Lousuebsakul-Matthews V, Thorpe DL, Knutsen R, Beeson WL, Fraser GE, Knutsen SF. Legumes and meat analogues consumption are associated with hip fracture risk independently of meat intake among Caucasian men and women: the Adventist Health Study-2. Public Health Nutr 2013:1-11.

7. Spencer H, Kramer L, DeBartolo M, Norris C, Osis D. Further studies of the effect of a high protein diet as meat on calcium metabolism. Am J Clin Nutr 1983;37:924-9.

8. Kerstetter JE, O’Brien KO, Insogna KL. Dietary protein affects intestinal calcium absorption. Am J Clin Nutr 1998;68:859-65.

9. 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;24:1835-40.

10. Bow CH, Cheung E, Cheung CL, Xiao SM, Loong C, Soong C, Tan KC, Luckey MM, Cauley JA, Fujiwara S, et al. Ethnic difference of clinical vertebral fracture risk. Osteoporos Int 2012;23:879-85.

11. Michaelsson K, Wolk A, Langenskiold S, Basu S, Warensjo Lemming E, Melhus H, Byberg L. Milk intake and risk of mortality and fractures in women and men: cohort studies. Bmj 2014;349:g6015.

12. Matthews VL, Knutsen SF, Beeson WL, Fraser GE. Soy milk and dairy consumption is independently associated with ultrasound attenuation of the heel bone among postmenopausal women: the Adventist Health Study-2. Nutr Res 2011;31:766-75.

13. Appleby P, Roddam A, Allen N, Key T. Comparative fracture risk in vegetarians and nonvegetarians in EPIC-Oxford. Eur J Clin Nutr 2007;61:1400-6.

On April 2, 2014, Medscape sent out a Special Report that included a link to a video and article, Calcium + Vitamin D: Surprises From Long-term Follow-up. You probably need to sign up for a free account to view the article.

Here are some excerpts from the article which was about the Women’s Health Initiative study:

“In this large trial, more than 36,000 postmenopausal women aged 50-79 years were randomly assigned to treatment with a combination of calcium carbonate at a dose of 1000 mg elemental calcium plus vitamin D3 400 IU daily, or placebo.

“We now have 3 lines of evidence of benefit for calcium plus vitamin D supplementation: the reduction in hip fracture seen among adherent women, the reduction in vertebral fracture in the intention-to-treat analyses, and the improvement or better results for bone mineral density…

“In terms of all cancers, among the women who had low baseline intake of vitamin D, there was a statistically significant 9% reduction in total cancer with supplementation, and also a marginally significant 9% reduction in all-cause mortality.”

The report also said that there was no increase in cardiovascular disease for women taking supplements.

For the last many weeks, I have been in an undisclosed location working on an article on oxalates. I think it has been my 3rd biggest project to date, the other two being the epic adventure Vitamin B12: A Love Story followed by Soy: What’s the Harm?

But before I release the article on oxalates, I am writing to let you know that upon getting a bit more information about the oxalate content of foods and re-analyzing the data, I have expanded and moved the table Calcium & Oxalate Content of Foods to a new page and also slightly modified the absorption category for some greens:

– Studies have shown that calcium in fortified soymilk, bok choy, kale, and mustard greens is absorbed well.
– Based on oxalate levels, the calcium in turnip greens, watercress, and broccoli should also be absorbed well.
– Based on oxalate levels, the calcium in collards should be absorbed moderately well.
– Studies have shown that the calcium in spinach and rhubarb is not absorbed well.
– Based on oxalate levels, the calcium in beet greens and swiss chard should not be absorbed well.

I know a lot of people have oxalate stories, but please do not send me any links to oxalate info before I publish my piece! Once it comes out, I’ll be happy to receive any info you think I have missed. Thanks!

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I have updated the VeganHealth.org page, Nutrient Intakes of Vegetarians and Vegans, with data recently released from Adventist Health Study-2 (AHS-2) (1).

Some interesting notes:

– The nutrient intakes included supplements. However, they also used median amounts (rather than averages) which means someone using a very large dose of a supplement would not skew the “average” intake.

– 45% of the AHS-2 subjects were vegetarian and approximately 8% were strict vegetarians or what I’m calling “vegan.” They eat any category of animal products (meat, fish, eggs, dairy) less than once per month.

– There were two tables of nutrient intakes given in the paper and I used the one that was not adjusted for sex, race, and age as I’m not clear what that actually means in the case of nutrient intakes.

– The lacto-ovo vegetarians ate less dairy protein than the regular meat-eaters (median intake of 7.5 vs. 11.8 g per day). I have seen people suggest that lacto-ovo vegetarians tend to eat a lot more dairy than your average meat-eater, but this shows that is, on average, not the case.

– It was great to see that the median intake of vitamin B12 for vegans was 6.3 µg per day, but there were still many vegans not getting nearly enough as the 5th percentile was at a mere .4 µg per day.

– Calcium intake for the vegans was excellent at 933 mg per day. The 5th percentile was 520 mg. This was much better than the calcium intakes in the bone fracture study from EPIC-Oxford where almost half the vegans were getting less than 525 mg per day (more info).

– Sodium wasn’t terrible at 3,066 mg per day, but would ideally not be over 2,300.

– It looks like vegans ate as many calories as the regular meat-eaters. That’s hard for me to believe and could be an error in the methodology. Or, perhaps, the vegans really did eat as many calories, but you don’t see that often.

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References

1. Rizzo NS, Jaceldo-Siegl K, Sabate J, Fraser GE. Nutrient Profiles of Vegetarian and Nonvegetarian Dietary Patterns. J Acad Nutr Diet. 2013 Aug 26. [Epub ahead of print] | link

In her latest blog post, Calcium and Protein and Bone Health in Vegans, Ginny has a good reminder about the need for vegans to make sure they’re getting enough calcium and protein. Excerpt:

“The theory is that animal protein, through its acidifying action, “leaches” calcium from bones, eventually weakening them and causing bone fractures. If that’s true, it means that those of us who eat no animal protein are likely to have better bone health. And maybe even lower calcium needs.

“Unfortunately, it’s not true. Or at the very least, the evidence in support of this relationship has fizzled over the years. I’ve written about this before, but it remains such a pervasive and potentially harmful belief that it deserves an occasional revisit.”

Read more…

After my post Calcium Absorption from Greens, I got a question from a reader that I think many people may be wondering about.

She has been told to get 1,200 mg of calcium per day. But if the calcium from greens in only absorbed at less than 50%, does that mean she needs to get a higher amount of calcium in her diet so that she absorbs a full 1,200 mg?

The answer is that dietary recommendations are made knowing that a nutrient is only partially absorbed from the diet. It depends on the nutrient and recommendations are made for each nutrient based on its typical absorption rate.

In extreme cases, such as the calcium from spinach that is absorbed at only about 5%, you would need to make modifications to rely only on spinach or foods with a similar absorption rate. But the recommendations for calcium assume that only about 1/3 is going to be absorbed from the best sources (not sure the exact number the Institute of Medicine uses).

But this is a reason why I never mention getting one’s calcium from legumes or nuts and seeds – when you combine their relatively low amounts of calcium and their low absorption rates, you cannot rely on them for the bulk of your calcium needs. They will supply some, but not nearly enough.

Focus on the greens with higher amounts of calcium that is moderate to highly absorbable, calcium-set tofu, and fortified foods or supplements.

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Based on some comments by a reader and their finding a chart of oxalate content of various greens published by the USDA (thanks, dimqua!), I decided to more rigorously document the calcium absorption from greens. What I came up with is shown in Table 5 of the (newly renamed) article on bones on VeganHealth.org, Calcium and Vitamin D.

Here is a summary of the findings:

• Studies have shown that calcium in fortified soymilk, bok choy, kale, and mustard greens is absorbed well.

• Based on oxalate levels, the calcium in turnip greens should also be absorbed well.

• Based on oxalate levels, the calcium in collards, broccoli, and watercress should be absorbed moderately well.

• Studies have shown that the calcium in spinach and rhubarb is not absorbed well.

• Based on oxalate levels, the calcium in beet greens should not be absorbed well.

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This is an abridged version of Calcium and Vitamin D, which includes references and more details on just about every paragraph below.

Calcium

Americans are regularly being urged to consume more calcium in order to prevent osteoporosis. It is practically impossible to meet the recommendations without large amounts of cows’ milk, calcium-fortified foods, or supplements.

Because vegans do not eat dairy products, without fortified foods or supplements their calcium intakes tend to be low (about 400-600 mg per day compared to the U.S. recommended intake of 1,000 mg per day).

Traditionally, the vegan community has responded to this by saying osteoporosis is a disease of calcium loss from the bones, not a lack of calcium in the diet. This was based on two ideas.

The first idea is that ecological studies have shown that the countries with the highest intake of dairy products (northern Europe and the USA) have higher rates of hip fractures than do Asian and African countries where much less milk is consumed. This in turn, can be explained by the second idea, which is that studies show that after ingesting animal protein, people urinate large amounts of calcium.

Therefore, the thinking goes, calcium intake isn’t important for preventing osteoporosis and vegans are protected due to the lack of animal protein in their diets.

Unfortunately, there is a lot of evidence to suggest that this is not correct. It turns out that hip fractures are more indicative of the risk of falling than of osteoporosis in some countries, with a recent study from Hong Kong showing that while men and women in Hong Kong had lower rates of hip fractures, they had higher rates of vertebral factures, and the women had higher rates of osteoporosis than Caucasian women.

As for protein leaching calcium from bones into the urine – it’s a lot more complicated than that. The studies that showed calcium to be urinated out were done using protein isolates whereas eating protein from whole foods does not result in a calcium imbalance. Population studies and clinical trials show that protein, including animal protein, does not have a negative effect on bones (more details here).

So where does that leave vegans?

Vegans’ bone mineral density, a measure of osteoporosis, has been shown in many studies to be slightly lower than non-vegans. More importantly, the one study on Western vegans measuring fracture rates over time found that vegans in the group who got less than 525 mg of calcium per day had a higher fracture rate than vegans in the group getting more than 525 mg. The vegans in the lower calcium group also had higher fracture rates than the meat-eaters and lacto-ovo vegetarians.

Although it is possible to meet the calcium recommendations by eating greens alone, the average vegan probably will not meet recommendations without drinking a glass of fortified drink each day, eating calcium-set tofu, or taking a 250 – 300 mg supplement (in addition to eating an otherwise balanced diet).

The greens highest in absorbable calcium are kale, mustard greens, bok choy, turnip greens, collards, and watercress (more info). In addition to calcium, greens also contain vitamin K, potassium, and magnesium, which also contribute to better bone health.

While spinach, Swiss chard, and beet greens are high in calcium, it is not well absorbed due to their also high content of oxalates, which bind calcium and prevent absorption from the digestive tract.

Research is mixed about whether calcium intakes above 1,400 mg per day can put people at risk for chronic disease. If you take a calcium supplement, it’s best not to go overboard. Most vegans taking 250-300 mg per day would not come close to 1,400 mg.

Vitamin D

Vitamin D is also important for bones, as it can increase calcium absorption when the body signals that it needs calcium. Research has shown that in populations with calcium intakes similar to omnivores in the United States, vitamin D is more important than calcium for preventing osteoporosis.

In recent years, vitamin D has also been linked to many other diseases and some researchers have suggested that the recommended vitamin D levels are too low. However, the Institute of Medicine has reviewed the research and concluded that is not the case. The controversy has resulted in many people thinking they are deficient in vitamin D when they are not.

The only significant, natural, dietary sources of vitamin D are fatty fish, eggs (if chickens have been fed vitamin D), and mushrooms (if treated with UV rays). Most Americans get their dietary vitamin D through fortified milk and fortified margarine. The vegan diet contains little, if any, vitamin D without fortified foods or supplements. On average, vegans’ vitamin D levels are adequate, but somewhat lower than non-vegans.

Most people get a significant amount of their vitamin D from the action of UV rays on their skin. While the body can store vitamin D made in the sunnier months for use during less sunny times, this does not work for everyone. In fact, some people, even those living in sunny climates, develop extremely low levels of vitamin D. This can manifest itself through fatigue and bone pain.

If your arms and face (or the equivalent amount of skin or more) is exposed to the following amounts of midday sun (10 am to 2 pm), without sunscreen, on a day when sunburn is possible (i.e., not winter or cloudy), then you should not need any dietary vitamin D that day:

• Light-skinned: 10 to 15 minutes
• Dark-skinned: 20 minutes
• Elderly: 30 minutes

On all other days, people older than one year should get 600 to 1,000 IU of vitamin D.

Due to skin cancer concerns, some dermatologists recommend getting all your vitamin D from supplements rather than the sun. The amounts of sun above for light and dark-skinned people should be safe, but I have not seen research on how much sun is safe for elderly people and recommend talking to your doctor about how to get vitamin D if you believe you are at risk for skin cancer.

600 to 1,000 IU of vitamin D is only available in supplemental form or specially treated mushrooms.

There are two forms of supplemental vitamin D: D2 and D3. Vitamin D2 is always vegan, made from exposing fungi to UV rays. Vitamin D3 normally comes from fish oil or sheep’s wool, but there is a vegan version made by Vitashine.

A great deal of research has been conducted on vitamin D2 and D3. Vitamin D2 is effective at increasing bone mineral density (when given to people who are deficient). Vitamin D2 can also increase vitamin D levels temporarily, but is not as effective as vitamin D3 at keeping vitamin D levels raised when taken only weekly. If you take vitamin D on a regular basis, D2 should be fine, whereas if you are only going to take it sporadically, without getting sun in the interim, or find that your vitamin D levels will not increase on D2, then you should opt for D3.

If you are trying to raise your vitamin D levels with D2, make sure the laboratory can detect vitamin D2, and not just vitamin D3. Also make sure that you are not trying to raise your levels beyond what the Institute of Medicine says is adequate (50 nmol/l or 20 ng/ml) as there’s no sense in worrying if you cannot seem to get your vitamin D levels twice as high as necessary!

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I have come across another recent report on calcium supplements. This time, instead of correlating calcium intake with rates of disease, the calcification of arteries was studied (1).

Researchers in the Framingham Study measured calcium intakes and then followed participants for four years at which time they measured the amount of calcification of their arteries. They found no correlation or trends with calcium intake and calcification of the arteries in amounts up to about 3,000 mg per day in either men or women. Ditto for calcium supplements of 500 mg per day or more compared to 0 or 1-500 mg per day.

The authors of the study note one other study looking at calcification of the arteries (2) which found no association in the prospective arm, though did find a cross-sectional correlation at baseline.

The article No Need to Worry About Calcium and Your Heart from the Tufts Health & Nutrition Letter (March 2013) makes it sound like the jury is in and it’s a done deal – calcium supplements are safe (in the amounts studied). Based on the other research I’ve written about, Calcium Supplements and Cardiovascular Disease in the News, I would still suggest not going over 1,400 mg per day.

One can hope that more studies will not come out to contradict these findings!

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References

1. Samelson EJ, Booth SL, Fox CS, Tucker KL, Wang TJ, Hoffmann U, Cupples LA, O’Donnell CJ, Kiel DP. Calcium intake is not associated with increased coronary artery calcification: the Framingham Study. Am J Clin Nutr. 2012 Dec;96(6):1274-80. | link

2. Wang TK, Bolland MJ, van Pelt NC, Horne AM, Mason BH, Ames RW, Grey AB, Ruygrok PN, Gamble GD, Reid IR. Relationships between vascular calcification, calcium metabolism, bone density, and fractures. J Bone Miner Res. 2010 Dec;25(12):2777-85. doi: 10.1002/jbmr.183. Epub 2010 Jul 16. Erratum in: J Bone Miner Res. 2011 Feb;26(2):439. (Abstract) | link

Yesterday, I wrote about a clinical trial comparing soy vs. cow’s milk’s impact on bone mineral density (BMD) in Chinese women (link). To sum it up, the cow’s milk fared better than soy, which fared better than nothing.

Today I found a prospective study from the Adventist Health Study-2 (2011) comparing soy vs. cow’s milk (1). They followed 337 post-menopausal, Caucasian women, who had not been previously diagnosed with osteoporosis, for two years. 61% were considered vegetarians because they ate meat less than once a month.

The authors sum up the results:

“Those drinking soy milk at least once a day or more (highest category) were 57% less likely to have osteoporosis than those who never used soy milk [.43 (.21–.89)]. Likewise, those eating dairy products at least once a day or more were 62% less likely to have osteoporosis than those consuming dairy less than twice a week [.38 (.17–.86)].”

There was not a separate soymilk group and cow’s milk group, both findings were comparing the entire group of women to each other, though the results for each milk were adjusted for intake of the other milk.

The researchers did not measure total calcium intake, but they seemed to assume that most of this soymilk was calcium-fortified. They also found no correlation between calcium or vitamin D supplement usage (amounts not measured) and better bone health.

Interestingly, cheese was the only dairy product that, when separated out, was correlated with better bone health (the other categories were “milk,” and “yogurt/ice-cream”). The authors speculated that it was due to the higher calcium and protein content of cheese.

In conclusion, it appears to be about equally beneficial for bone health for Caucasian, postmenopausal women to be drinking either soymilk or cow’s milk.

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Reference

1. Matthews VL, Knutsen SF, Beeson WL, Fraser GE. Soy milk and dairy consumption is independently associated with ultrasound attenuation of the heel bone among postmenopausal women: the Adventist Health Study-2. Nutr Res. 2011 Oct;31(10):766-75. | link