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.
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.
This is an abridged version of Calcium and Vitamin D, which includes references and more details on just about every paragraph below. This should conclude my calcium-vitamin D barrage of the past few weeks!
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:
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!
(Thank you to everyone who donated and used the Amazon links over the weekend! And especially to O.P. from the Southern hemisphere whose email address wasn’t working.)
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.
One can hope that more studies will not come out to contradict these findings!
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.
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
I’m going through my backlog of research on bones in order to write a reader-friendly version of the tome that is Bones, Vitamin D, and Calcium on VeganHealth.org.
In January 2012, a report from China was released of a randomized clinical trial comparing the effects of cow’s milk and soymilk on bone mineral density (BMD) in postmenopausal women (1).
The women were divided into three groups: soy, cow’s, and control. The women knew which treatment they were receiving, while the control group got nothing. The milk and soymilk had 250 mg of calcium and they drank one serving per day.
BMD was measured in the spine, hip, and femur at 6, 12, and 18 months.
In the cow’s milk group, BMD increased in the hip and femur. In the soymilk group, BMD did not change significantly, but showed a downward trend in all three locations. In the control group, there was a downward trend in all three locations that only reached significance in the femur at 18 months.
It should be strongly noted that the participants were asked to avoid calcium from other milks and supplements during the trial which means their total calcium intake was probably quite low and I’m somewhat amazed that their BMD didn’t decrease more or in all three groups. Total calcium intake during the study period was not reported.
Compliance was 93.1% in the cow’s milk group and 82.5% in the soymilk group. This might explain a small amount of the differences between those groups. Other possibilities are that calcium in fortified soymilk is known to quickly settle to the bottom of the milk where it might not be ingested but left in the container, and that milk contains phosphorus and growth factors that might increase BMD.
This is just one small study and more work needs to be done before any conclusions should be drawn.
Reference
1. Gui JC, Brašić JR, Liu XD, Gong GY, Zhang GM, Liu CJ, Gao GQ. Bone mineral density in postmenopausal Chinese women treated with calcium fortification in soymilk and cow’s milk. Osteoporos Int. 2012 May;23(5):1563-70. Epub 2012 Jan 27. | link
In 2010, I wrote about a meta-analysis on calcium supplements and cardiovascular disease, Calcium Supplements: Are They Safe? The association with heart disease was limited to people who started out with a dietary calcium intake of 700 mg/day or more (not including the supplements). Then in 2011, I noted a study on supplement use in older women that found a link between calcium supplements and a lower risk of mortality (Supplement Safety).
Since I recommend that vegans get their calcium levels up to at least 700 mg and preferably the DRI (1,000 mg for adults under 50; 1,200 mg for adults over 50) by whatever means necessary (greens, fortified foods, or supplements), I try to keep track of this research as closely as I can. In February, results from two different studies looking at calcium supplements and cardiovascular disease were reported.
One study was from the USA and followed people aged 50 to 71 at baseline for 12 years (1). No association between cardiovascular disease deaths and calcium intake was found for women. For men, calcium supplements of 400 to 1,000 mg/day was associated with an increased risk of cardiovascular death, but was just barely statistically significant. But supplements of more than 1,000 mg/day were associated with a highly significant increase in cardiovascular mortality:
(mg/day)
None
1.00
< 400
.99 (.94-1.04)
400–1,000
1.09 (1.01-1.18)
> 1,000
1.20 (1.05-1.36)
When the numbers were stratified for smoking, there was a strong trend towards the risk being mainly in current smokers. The average user of supplements for men had a dietary calcium intake (not including supplements) of 815 mg. So once you figure in another 400 to 1,000+ mg of supplemental calcium, their intakes were anywhere from the DRI to about 50% higher than the DRI.
The second study was from Sweden, on older women (2). All-cause mortality for dietary calcium (not including supplements) was a U-shaped curve, with both low calcium and high calcium associated with an increase in mortality:
(mg/day)
< 600
1.38 (1.27, 1.51)
600-999
1.00
1000-1399
1.00 (.96-1.04)
≥ 1,400
1.40 (1.17-1.67)
The findings were similar, but even stronger for cardiovascular disease, and were also very similar for dietary plus supplemental calcium.
One thing to consider for this Swedish study is that 1,400 mg of non-supplemental calcium would indicate a pretty high dairy intake. If you assume 300 mg per serving of dairy, that’s at least 3 servings of dairy per day (on top of the calcium they might be getting from other foods). The results did not adjust for dairy product intake so it’s possible that dairy of 3 servings (or more) per day could have caused the increase in cardiovascular deaths.
While it’s not yet clear what is going on here, my conclusion remains that vegans should aim for at least 700 to 1,000 mg/d (or 700 to 1,200 mg/d if over 50) from foods or supplements, but that you should not go much above that.
References
1. Xiao Q, Murphy RA, Houston DK, Harris TB, Chow W, Park Y. Dietary and Supplemental Calcium Intake and Cardiovascular Disease Mortality: The National Institutes of Health–AARP Diet and Health Study. JAMA Intern Med. 2013;():1-8. | link
2. Michaëlsson K, Melhus H, Warensjö Lemming E, Wolk A, Byberg L. Long term
calcium intake and rates of all cause and cardiovascular mortality: community
based prospective longitudinal cohort study. BMJ. 2013 Feb 12;346:f228. | link
[Thank you for all the responses to my request for information on increasing bone mineral density! I received a lot of responses and am still working my way through them.]
Because I’m planning to write a more reader-friendly version of VeganHealth.org’s Bones, Vitamin D, and Calcium, I decided to check in on the research on protein and bone health. In so doing, I found a 2012 review from a group of researchers in France who declared having no conflicts of interest (1).
There has been an enormous amount of research on protein and bone health and their review had almost 4 pages of references. I will hit the highlights of what they found:
– Many clinical trials show that adding purified proteins to the diet increases calcium excretion through the urine.
– Phosphorus, in which meat and dairy are rich, counteracts the increase of calcium in the urine between 40 and 65%.
– Findings that older people in Western countries have higher hip fracture rates are confounded by the fact that people in Western countries live longer, protein intakes were not estimated for individuals, and there are ethnic differences in bone structure and lifestyles.
– High protein diets increase acid excretion in the urine, but this can be handled by the body’s acid buffer system without the need for calcium.
– Studies measuring whole-body calcium balance (as distinct from excretion) in relation to high protein diets have been mixed, but this might partly be due to the difficulty in measuring calcium balance and because high protein diets might reduce calcium balance when calcium intakes are particularly low.
– In low-calcium, but not high-calcium diets, higher protein intakes probably increase calcium absorption from the digestive tract causing an increase in calcium excretion in the urine.
– Fruits and vegetables are beneficial to bone health, probably due to their high potassium and magnesium content. This could cause confounding in protein studies because diets high in protein are often low in fruits and vegetables.
– As I describe in my post Protein Intake and Bone Health, Darling et al. (2009) found that a large majority of the cross-sectional surveys and cohort studies have reported either no association or a beneficial association between protein and bone mineral density.
– There is some evidence that a beneficial effect of protein on bones is only seen when calcium intake and vitamin D status is adequate.
– Maintenance of adequate bone strength and density with aging is dependent on adequate muscle mass which is dependent on adequate intake of protein.
– An increase in IGF-1 is most likely the mechanism for increased bone health with higher protein intakes.
They conclude, “Although HP [high protein] diets induce an increase in net acid and urinary calcium excretion, they do not seem to be linked to impaired calcium balance and no clinical data support the hypothesis of a detrimental effect of HP diet on bone health, except in the context of inadequate calcium supply.”
Reference
1. Calvez J, Poupin N, Chesneau C, Lassale C, Tomé D. Protein intake, calcium balance and health consequences. Eur J Clin Nutr. 2012 Mar;66(3):281-95. | link
I noticed that the new USDA nutrient database seemed to have changed the amounts of calcium in some of the greens they had listed. I have updated Table 5 in Bones, Vitamin D, and Calcium at VeganHealth.org.
The USDA database lists a number of different versions for foods – for each type of greens, for example, there are a half dozen to a dozen entries. In the past, I’ve tried to take the most usual or average them out. This time, in updating Table 5, I used the exact entry and I included a number of entries for some of the foods.
Unfortunately, the amount of calcium in broccoli was lowered from 50 to 31 mg per serving. Other greens seemed to stay about the same.
I was wondering if you saw this study [showing that increased vitamin D intake, but not increased dairy and calcium, protected adolescent girls against stress fractures] that went around yesterday, and saw PCRM’s release on it. I only read the abstract, but didn’t see that higher intakes of calcium was correlated with higher risk of bone fracture. I was wondering what you thought about this, because I remember you referencing some studies showing that vegans have higher rates of bone fracture, and that the difference went away when the vegans had high enough intakes of calcium. Was that because they were getting the calcium from plant sources, you reckon?
Answer:
It is only one study (EPIC-Oxford, 2007) showing vegans to have a higher fracture rate, the only study measuring fracture rates in Western vegans. It showed that the category of vegans getting less than 525 mg/day of calcium had a higher fracture rate than other diet groups, but that vegans getting more calcium had the same rate.
I did see PCRM’s press release on this study and have since obtained a copy of the paper. Although not mentioned in the abstract, the study found a trend towards increased risk of stress fracture with increased calcium intakes, among girls in the high impact activity category, though the finding was not statistically significant.
These results have little bearing, one way or the other, on my recommendations that vegans get more than 525 mg/day of calcium (and preferably 700 – 1,000 mg/day). The lowest category of calcium intake was 541 mg/day. The second lowest was 825 mg/day and that category didn’t have a practically different risk compared to the lowest category. It wasn’t until the middle category of calcium intake, an average of 1,111 mg per day, that there was a strong trend towards higher risk of stress fracture (though, again, it wasn’t statistically significant).
Here are some excerpts from the paper’s discussion:
“Our findings are not consistent with those reported in a prospective study of 125 young adult female competitive distance runners, which found that higher intakes of calcium and dairy products predicted lower rates of stress fracture and that higher intakes of vitamin D, calcium, and dairy foods were all associated with significant gains in hip bone mineral density during the 2 years of follow-up.
“Our findings are supported by several studies that have found no association between dairy intake and bone health in children and adolescents. While 2 randomized trials reported a positive relationship between dairy product consumption and measures of bone health, most cross-sectional, retrospective, and prospective studies did not. A review of calcium intake, dairy product intake, and bone health found that the vast majority of controlled studies of dairy supplementation or total dietary calcium intake show that, although very low calcium intake may be harmful to bone development, increases in dairy or total dietary calcium intakes higher than 400 to 500 mg/d are not correlated with nor represent a predictor of bone mineral density or fracture rate in children or adolescents.”
The evidence appears to be mixed as to whether calcium intakes higher than 400 to 500 mg in children and adolescents is protective, harmful, or neutral. EPIC-Oxford remains the most important finding for vegans.
Reference
Sonneville KR, Gordon CM, Kocher MS, Pierce LM, Ramappa A, Field AE. Vitamin D, Calcium, and Dairy Intakes and Stress Fractures Among Female Adolescents. Arch Pediatr Adolesc Med. 2012 Mar 5. [Epub ahead of print] | link
