OSTEOPOROSIS
by Michael Klaper
Dear Dr. Klaper,
What are your thoughts on osteoporosis? What is it and what can we do to prevent it? Can it be reversed and bone strength improved?
-- J.K.
Dear J.K.:
Good - and timely - questions. Everyone has an image of her in their mind - the little, old woman, bent over with a C-shaped spine. She is the embodiment of a process that does to the skeleton what Alzheimer’s disease does to the brain. In osteoporosis, for which she has become the symbol, the bones become so weakened and crumbly they have the tensile strength of styrofoam. Daily body movements and the relentless force of gravity have compressed the vertebral bones of her spine, collapsing them, and bending her permanently forward. Most of her skeleton is equally as fragile. A cough, a hug, or a minor fall, can snap a rib, an arm, a thigh - and a fractured hip in one’s seventies or eighties can be a death sentence.
The specter of the elderly woman with the collapsing spine described above is a common one, but far from complete picture. The young, lean, female long-distance runner or a 60-year old apparently healthy male would not seem to be candidates for osteoporosis – yet they too can be victims. In industrialized nations, osteoporosis is a devastating, but silent, epidemic. One out of four Americans will suffer an osteoporosis-related fracture during their lifetime - at least 1.2 million fractures in the U.S. resulting in medical and social costs of at least 6.1 billion dollars every year.
If you believe the many advertisements, osteoporosis results from not swallowing enough calcium in our daily diets. Yet, medical studies2 show that merely consuming more dairy products or calcium tablets is not sufficient to prevent nor reverse this devastating disease. So, let’s consider some of the underlying causes of osteoporosis, as well as strategies for preserving and even strengthening our bones.
To understand osteoporosis, we must first realize that our bones are alive. Rather than dead, chalky rods that support us as we walk, sit, and stand, our bones are living tissue, with a rich blood supply and a high level of metabolic activity. Bones are constantly being built up by busy cells called “osteoblasts,” as well as being dismantled and re-shaped by the bone-dissolving cells called "osteoclasts." The balance of bone build-up versus bone break-down determines the strength of our skeletons. When bone dissolution and breakdown exceeds the rate of bone construction, our skeleton becomes weakened and susceptible to fracture - the disease of osteoporosis.
Diagnosing Osteoporosis
The loss of calcium from the bones is painless. Osteoporosis gives no warning symptoms until it is detected on a test or, worse, announces itself with a painful fracture. If a person has the risk factors for osteoporosis - Caucasian race, sedentary lifestyle, cigarette smoking, etc. - she or he should consider having her bone density measured. Contrary to popular belief, an x-ray is not effective in diagnosing early osteoporosis. By the time decreased bone density can be diagnosed on an x-ray film, the osteoporotic process is already far advanced. Long before reaching this point, anyone suspected of developing osteoporosis should have their skeletal density assessed with a non-invasive test called bone densitometry. This painless examination uses a light ray to measure the density of the bones, usually at the wrist and lower spine. Any family doctor can order this test.
Osteoporosis is not an inevitable part of growing older. Nature would not supply us with a heart and blood vessel system made to function for over 100 years, while giving us bones destined to fall apart at age 60! Bones are supposed to last as long as all the rest of our organs, at least to the hundred year mark - and beyond. Rather than being a normal part of aging, osteoporosis is a disease state – characterized by excessive loss of calcium from the bones with eventual dissolution of the bone structure. This is an important concept. Osteoporosis is not so much a disease of deficient calcium intake, but rather excessive calcium loss from the bones. Where is the calcium going? It's going out through the kidneys into the urine - and down the toilet!
“Calcium Thieves”
Why does this happen? In our daily lives, we encounter a number of "calcium thieves" that can rob our bones of this vital mineral. Interestingly, with one exception, all the “calcium thieves” have something in common - they are things that we put in our mouths. We will examine them in a moment, but first we must consider the one "thief" that we do not ingest - in fact, the one that we do not have to do anything to invite to weaken our skeleton. Actually, this rascal is the number one cause of calcium flowing from the bones of modern women and men - simply the lack of physically using our bones, especially against the force of gravity.
Like muscle, nerve, and all the other tissues of the body, the more we use our bones, the stronger they become and the better they function. Every step you take sends pulses of electrical energy up and down the lengths of your leg bones. These pulsating currents of bio-electricity help to keep the calcium atoms firmly anchored in the substance of the skeleton. Thus, every movement of our body - especially movements against resistance such as gravity, elastic exercise bands, etc. - helps to keep the bones calcified, healthy, and fracture-resistant.
Unfortunately, today most of us do very little manual labor - machines carry our loads, and even carry most of us everywhere - so we are free to sit for most of our day. This is a very effective way to let the calcium drain out of our bones. As we look around the globe, we see that in countries where people spend their entire long lives physically active, their bones stay strong. In these nations, the disease of osteoporosis is rare.
A dramatic demonstration of the opposite situation is seen in the astronauts, who spend relatively few days in gravity-free environments, and yet who suffer severe loss of calcium from their bones. Fortunately, the calcium is restored to the skeleton in a relatively short time when the astronaut is back in a normal-gravity environment. This is an important, and hopeful, clue for the rest of us - evidence that the osteoporotic process can be reversed.
To keep your bones healthy and to prevent osteoporosis, the most important thing you can do is to stay as physically active as you can throughout your life. Since calcium is always being laid down in the skeleton, it is never to late to begin to strengthen the bones. Medical studies by Dr. Aloia and others have shown that, even in elderly people, osteoporotic bones can be made stronger by gentle but steady exercise, like walking up stairs or squeezing rubber balls.3 Such is the power of using our muscles - it actually helps pull calcium into the bones and keep it there, keeping our skeleton strong.
Any exercise that places a mild, repeated stress on the bones, causes the bones to become thicker, stronger, and more calcified. Never miss a chance to walk up stairs or to carry packages. Never stop walking - try to take a brisk, 30 to 60-minute walk at least every other day - and more frequently is even better.
Although exercises against gravity are especially potent in helping bones stay strong, muscle contraction of any kind will help generate electrical currents that help pull calcium into the bones. Elastic, stretchable bands that can be used in resistance training, even while a person is sitting, are also excellent tools to provide muscular exercise that will help keep bones strong.
Now that we understand that our ever-more-sedentary desk jobs and lifestyles are the chief cause of the osteoporosis epidemic that is ravaging virtually all industrialized societies, we’ll look at the other major calcium thieves that attack our bones - namely, those hiding in things that we ingest. Let’s see how a moment of pleasure to entertain the tongue can rob precious calcium from the bones and weaken our very skeleton.
The “calcium thieves” that gain “oral entrance” into our bodies commonly include:
a. Concentrated animal protein.
Chicken, fish, and other meat-based products (burgers, hot dogs, fish fillets, etc.) all contain concentrated protein whose acidic nature dissolves calcium out of the bones. The dissolved calcium is washed through the bloodstream and is excreted by the kidneys into the urine. This phenomenon is well known to nutritional scientists and is called “protein-induced hypercalciuria”4. This means that diets high in meats and other animal products produce a sustained loss of calcium from the body.
It has been known for years that the ethnic group with some of the most severe osteoporosis on the planet are the Native American Inuit living in the Arctic. This is due in significant part to their ingestion of large quantities of high-protein fish and seal meat. This high-protein diet apparently results in high losses of calcium from their bones and leads to advanced osteoporosis among their women.5
What this effect means to your bones is that most every time you have a meal based upon a large piece of chicken, fish, or red meat, for the following several hours, precious calcium is leached from your skeleton into your urine - destined for the sewer system. Therefore, it is wise to minimize the portions of animal protein on your plate and look for more skeleton-friendly foods in the plant kingdom. Fortunately, most proteins of plant origin, especially those in whole grains, potatoes, fruits, seeds, and green and yellow vegetables, are significantly less acidic than animal-based proteins - and thus they have far less tendency to steal calcium from the bones. It's been observed for many years that osteoporosis is less of a problem among vegetarians than among omnivores.6
So, to reduce your loss of bone calcium from your food choices, stop seeing chicken, fish, and lean beef as "health foods." Begin to base more of your meals on whole, plant-based foods, like Oriental vegetable stir-fries over rice, bean burritos, whole grain casseroles, potato-based entrees, as well as other high-fiber meals which can be found in the recipe books listed in the “Resources” section. If you are trying to decrease the amount of carbohydrates in your diet, increase your proportion of vegetable-based entrees on your plate (stews, soups, salads, stir-fries, etc.) and reduce the proportion of pastas or other high-carbohydrate foods.
Although animal proteins are among the most pervasive of “calcium thieves” in the Western diet, there are other common culprits that we ingest that cause our bones to age and weaken prematurely. These include:
b. Sugar (as in cakes and candies), which makes the kidneys urinate out calcium.7
c. Phosphoric acid, a common ingredient in cola drinks that gives the cola its “bite,” is a potent calcium thief8, as is
d. Caffeine in coffee, tea, or cola drinks.9
e. Cigarette smoke10, and
f. Alcohol both leach calcium out of the bones11, (alcoholics and cigarette smokers both suffer high rates of osteoporosis).
g. Finally, excessive amounts of salt12 (actually, the element sodium) in some people can cause excessive urinary calcium loss. People at risk for osteoporosis should avoid pickled foods, preserved meats, chips, and other high-salt foods.
Well, there you have the recipe for osteoporosis: Be a woman (women start with less calcium in their bones than men), work at a sedentary desk job, eat your tuna fish or chicken breast for lunch, sip all day on your diet cola, smoke your cigarettes, have a glass of wine or beer after work, and do as little physical exercise as you possibly can. This is a sure way to waste away the very element needed to keep your bones strong, and to hasten your trip to a fractured hip - a predictable, but fortunately avoidable, course.
Dairy Reconsidered
For people who dutifully drink milk and swallow cheese, ice cream and yogurt, believing that the magic of cow’s milk will ward off fractures in old age, be advised that there is very little evidence that dairy products prevent osteoporosis - in fact, just the opposite may be true. Surprisingly, the nations who consume the most dairy products - the United States, Israel, the Netherlands and Scandinavian countries - suffer the highest incidences of osteoporosis13. If dairy products actually prevented osteoporosis, it would be rare in America and these other countries - yet, it is actually more rampant in these nations than in less developed countries.
Conversely, most humans on our planet, in Asia, South America, and Africa, virtually never consume cow's milk products - the milk, transportation, and refrigeration simply are not available. Yet, osteoporosis is not a common condition in these countries. Most of these people (barring starvation or parasitic diseases) enjoy strong bones throughout their physically active lives, deriving essentially all their calcium from green vegetables, seeds, grains, and from their drinking water.
Incidentally, seeing cow's milk and dairy products as far from essential for bone health can be advantageous for the rest of your body. Cow's milk contains proteins and other substances that are thought to play a major role in many serious diseases, like asthma, rheumatoid arthritis, recurring ear infections, eczema, colitis, and various autoimmune diseases. Don't be surprised if, after a few weeks without dairy products, your body feels and functions better in many ways - less swallowed phlegm, intestinal gas, runny nasal secretions, and other common, milk-related symptoms. Fortunately, these days, going dairy free is no great hardship. It is easy to find non-dairy replacements for milk, yogurt, ice cream, cheese, and other cow's milk-based products - just check in the refrigerator and freezer cases of your local natural food store or supermarket.
Supplements and Other Strategies
Although calcium intake alone is not to be relied upon as the total osteoporosis prevention or reversal program, an abundant calcium intake should be part of everyone’s diet. Aiming for a calcium intake of 1000 mg. to 1200 mg. a day is a good idea. Until the last fifty years, our diets contained far more whole fruits and vegetables - and thus significantly more calcium - than we consume today. Unless you eat several helpings of dark green leafy vegetables and a cup of nuts or seeds daily – not impossible, just uncommon - one would be wise to consider including in the daily diet calcium-fortified orange juice from the supermarket, or beverages such as calcium-fortified soy milk and rice milk from the natural food store. You can also take a calcium supplement, as a tablet, liquid or powder - 500 to 1000 milligrams per day. (This amount of supplemental calcium should be sufficient, since the calcium found in other foods and drinking water predictably provides at least 500 mg. - 700 mg. of calcium per day.) Preferably, supplemental calcium is always balanced with approximately equal amounts of magnesium, as magnesium is essential for retaining calcium in the skeletal structure.
Remember, however, that you cannot prevent or reverse osteoporosis just by swallowing large amounts of calcium supplements. Excessive amounts of calcium can lead to precipitation of calcium-containing kidney stones as well as calcium deposits in muscles, tendons, and other vital tissues. Osteoporosis is a disease of the active dissolution of bone structure - calcium first, and then the structural collagen protein – and the entire process must be reversed.
As important as it is for us to avoid “calcium thieves,” there are several additional nutritional components to bone health that must be consumed in order to prevent or reverse osteoporosis. These nutrients include: Vitamin K, Vitamin B‑6, and the earth elements, manganese, copper, zinc, boron, and silicon. These nutrients are all present in whole, plant-based foods, such as dark green leafy vegetables, root vegetables, nuts, seeds, grains, sea vegetables (nori, arame, wakame, etc.), and fruits.
Vitamin D is essential for us to absorb calcium from our food into our bloodstream. Vitamin D is made naturally in our skin as sunlight falls upon it (15 minutes per day of gentle sunlight on the skin of the arms is all that is required. If such sun exposure unavailable, an oral Vitamin D supplement should be taken).
In view of the foregoing, if you are taking a multivitamin/mineral supplement, be sure it contains the following nutrients in approximately the indicated amounts. To gain the most benefit, try to consume the supplements twice daily, with or shortly after meals:
Calcium 250-500 mg., Magnesium 250-500 mg., Zinc 15 mg., Copper 1-2 mg. 5-10 mg. Boron 1-3 mg. Silicon 1-2 mg. Vitamin B-6 5-25 mg. Folic Acid .08 - 5 mg. Vitamin C 100-1000 mg. Vitamin D 100-200 I.U. Vitamin K 100-500 mcg.
[A person who is being medicated with the anticoagulant drug, warfarin, should not take supplements with Vitamin K, as that vitamin can counteract the effects of their “blood thinner.”]
The above nutrient recommendations, along with a full discussion of the diagnosis and management of osteoporosis, are presented in the excellent book, Preventing and Reversing Osteoporosis, by physician and educator, Alan Gaby, M.D. (See “Resources” section.)
Hormone Replacement Therapy
It is true that the hormones estrogen and progesterone play a significant role in keeping bones well calcified. After a woman reaches menopause, and her ovaries produce less of these essential hormones, bone strength may suffer. Hormone replacement has been seen as a major answer to the osteoporosis problem; however, it has now become evident that swallowing oral estrogen tablets alone is not the answer.
Although possibly offering benefits for the skin and other tissues in the body, in the skeleton estrogen replacement therapy inhibits the action of osteoclasts. Thus, estrogens act by retarding normal bone breakdown. In this way, estrogens stop the breakdown of bone, but they do not increase the rate of bone formation by the osteoblasts. This is important because inhibiting the action of osteoclasts does not make for stronger bones. Osteoclasts have an important function, namely removing old bone spicules that have been micro-fractured through the shocks of daily living. It is essential that the osteoclasts remove these weakened bone struts to make way for new bone construction by the osteoblasts. In this light, it can be seen that the action of estrogens may ultimately not decrease the rate of fractures. In other words, estrogen-like drugs may slow down the removal of old bone - and thus create denser-appearing bones on x-rays and scans - but it is far from proven that estrogens actually make the bones stronger and (the ultimate test) reduce the incidence of osteoporosis-related fractures.
On the negative side, estrogen therapy can produce adverse effects, such as enlarging breast lumps and making menstrual bleeding heavier and more painful. They may even put a woman at higher risk for several types of cancers, including of the breast and uterus. Should a woman and her doctor decide upon estrogen therapy, some of these problems may be avoided through the use of a “balanced estrogen” containing appropriate amounts of the three most abundant estrogens in the body, estrone, estradiol, and estriol. (See Natural Hormone Replacement in “Resources.”) Balanced estrogen patches, tablets, and vaginal creams/suppositories are available through compounding pharmacies.
A woman may also want to talk to her doctor about a new class of drugs, the so-called “selective estrogen receptor modifiers” like raloxifene.
These drugs may slow down bone loss– although they are not free of side effects and are certainly not the entire solution to the osteoporosis puzzle. Again, the woman and the physician are the best people to make the decision as to the appropriateness of this therapy.
Incidentally, just because a woman is past the age of menopause and does not produce large amounts of estrogen from her ovaries, it does not mean her body is completely incapable of producing estrogen. Her adrenal glands, as well as the subcutaneous fat stores under her skin, are two tissues still capable of producing estrogen - if the woman consumes the appropriate essential fats in her diet. Adequate essential fat intake can be assured through ingesting a teaspoon or two of flaxseed oil or hempseed oil daily (along with 200-400 I.U. of Vitamin E to prevent oxidation in the body). A handful (one-half cup) of green, organic pumpkin seeds or raw walnuts will also help provide these essential omega-3 fats, as will the soybean oil in one-half cup tofu. The judicious use of these omega-3-containing oils will not only help maintain normal hormone balance and stronger bones, but also help create a more moisturized, youthful-looking skin.
If estrogen replacement therapy is decided upon, it is also wise to consider including natural progesterone as part of the hormone replacement program. Natural progesterone is also produced by the ovaries and is capable of stimulating new bone growth, thus actually helping bones grow stronger. There are advantages to specifying the form of progesterone to be “natural progesterone.” “Progestins” like the commonly-prescribed medroxyprogesterone (sold under the name, “Provera” and other brands) are chemically modified and can cause headaches, mood swings, and other adverse side effects. Natural progesterone is available, currently without prescription, at natural food stores and pharmacies. With medical guidance, natural progesterone can be used with good effect in conjunction with or in place of estrogen-based therapy.
When using powerful hormones like progesterone, more than “just enough” is not better. Usually, just one-half teaspoon of progesterone cream rubbed into the skin of the forearm will produce the desired effect. If the woman is still having menstrual periods, the progesterone cream should be used during the last two weeks of her monthly cycle. If she is past the age of menopause, the small amount of progesterone cream can be applied daily. It is important to work with the physician to check the progesterone levels in the saliva to determine the best dose of cream. Both the woman and her doctor can learn the fundamentals of using natural progesterone in the prevention or treatment of osteoporosis in the excellent monograph, Natural Progesterone, by John R. Lee, M.D. (See “Resources.”) Research is also beginning to accumulate that men with low bone density can benefit from small doses of progesterone cream, as well. Men do make progesterone naturally and it is an important hormone in maintaining healthy bones and tissues in both sexes. (See “Resources” section.)
Biphosphonates
A philosophy similar to that for estrogen replacement therapy in the prevention of osteoporosis can be applied to the “biphosphonate” drugs such as alendronate and etidronate. In other words, “biphosphonate” drugs may slow down the removal of old bone, and thus create denser-appearing bones on x-rays and scans, but whether they actually create stronger bones that will resist fracture for many years is far from clear.
The studies done to date on the action of biphosphonates on bones have only been carried out to a total of five years of treatment. We may well see an increase in bone fractures in biphosphonate drug users after five or more years of use. At this time, these drugs should be viewed as a “stop gap” measure that may “plug the leak” of calcium from the body. However, they should not be viewed as the long-term “cure” of the problem – that goal has been presented in the previous pages and is summarized below.
Reversing Bone Loss
If a diagnosis of osteoporosis has already been made on a bone density study, then increasing your bone density should become priority number one. Yes, osteoporosis can be reversed. Even into old age, the osteoblasts still retain the ability to deposit calcium in the bone structure - and indeed they do so on a daily basis. Because bone building is constantly in progress, bones – even osteoporotic ones - can be helped to make themselves stronger. A basic bone-building plan should utilize all of the modalities below:
- Eliminate all “calcium thieves” – especially excess animal protein, sugar, salt, cigarette smoke, alcohol, and phosphoric acid-containing cola drinks.
- Be sure your intake of calcium and magnesium exceed 1000 mg. of each daily.
- Assure an adequate intake of other trace minerals, especially boron, manganese, chromium, copper, zinc and silicon in the dosages previously given.
- Assure adequate vitamin intake, especially vitamin B-6, folic acid, vitamin C, and vitamin K at the dosages given previously.
- Consult with your physician about the role of hormone replacement, especially natural progesterone for women and testosterone for men. For the lean, athletic woman whose menstrual periods have stopped, she is at risk for osteoporosis due to excessively low hormone levels. In her pursuit of a low-fat diet, she may be ingesting so little fat that she cannot make adequate levels of progesterone in other bone-protecting hormones. (For that reason, she would be wise to increase the amount of fat in her diet via ingesting two to three teaspoons daily of an omega 3-rich oil such as flax seed oil or hemp seed oil, available in the refrigerator case of natural food stores.) Such a small amount of fat will not result in weight gain, but can be instrumental in maintaining healthy bones and other hormone-dependent organs.
- Institute a regular program of weight-bearing activity, possibly including exercise with elastic-resistance bands.
Conclusion
If this common sense approach to building and maintaining bone strength is diligently practiced, you can look forward to enjoying strong bones that will serve you well throughout a long, active, and healthy life.
RESOURCES
Preventing and Reversing Osteoporosis
by Alan Gaby, M.D.
Prima Publishing
P.O. Box 1260BK
Rocklin, CA 95677
Natural Progesterone
by John R. Lee, M.D.
BLL Publishing
P.O. Box #2068
Sebastopol, CA 95473
The John R. Lee Medical Letter
c/o Publisher’s Mgmt. Corp.
P. O. Box 84900
Phoenix, AZ 85071
Phone: 1-800-528-0559
URL: www.johnleemd.com
Natural Hormone Replacement
by Jonathan V. Wright, M.D. and John Morgenthaler
Smart Publications
P. O. Box 4667
Petaluma, CA 94955
Phone: 1-800-543-3873
URL: www.smart-publications.com
Delicious, low-fat meals made with calcium-sparing, moderate-protein, whole-foods ingredients can be found in:
Food for Life
by Neal Barnard, M.D.
Harmony Books
CalciYum!
by David and Rachelle Bronfman
Bromedia Inc.
Box 778, 181 Bay Street
Toronto, Ontario, Canada M5J 2T3
The Peaceful Palate
by Jennifer M. Raymond, M.S.
1418 Cedar Street
Calistoga, CA 94515
REFERENCES
1. Riggs, B.L., and L. J. Melton, III. 1986. Involutional osteoporosis. N England Journal of Medicine 314:1676-1686.
2. a) Riggs, B.L., et al. 1987. Dietary calcium intake and rates of bone loss in women. J Clin Invest 80:979-982.
b) Riis, B., et al. 1987. Does calcium supplementation prevent postmenopausal bone loss? A double-blind, controlled clinical study. New England Journal of Medicine 316:173-177.
c) Barger-Lux, MJ, et al. The role of calcium intake in preventing bone fragility, hypertension, and certain cancers. Journal of Nutrition 1994;124:1406S-1411S.
3. a) Aloia, J., Exercise and skeletal health. Journal of American Geriatric Society 29:104, 1981.
b) Smith, E., Physical activity and calcium modalities for bone mineral increase in aged women. Med Sci, Sports Exercise 13:60, 1981.
c) Smith, E.L., 1982. Exercise for prevention of osteoporosis: A review. The Physician and Sportsmedicine 10(3):72-82.
d) DeBenedette, V., 1987. Study: Swimming may increase bone density. The Physician and Sportsmedicine 15(12):49.
4. a) Licata, A. Acute effects of dietary protein on calcium metabolism in patients with osteoporosis. J Gerontol 36:14, 1982.
b) Kerstetter, J.E., et al. Dietary protein increases urinary calcium. J Nutr. 1990;120:134-136.
c) Linkswiler, H.M., et al. Protein-induced hypercalciuria. Fed Proc. 1981;40:2429-2433.
5. Mazess, R., Bone mineral content of North Alaskan Eskimos. Am J Clin Nutr 27: 916,1974.
6. a) Ellis, R.R., et al., Osteoporosis in British vegetarians and omnivores. Am J Clin Nutr. 1974;27:769-770.
b) Sanchez, T.V., et al. Bone mineral density in elderly vegetarian and omnivorous females. In: Mazeness R.B., ed. Proceedings of the 4th International Conference on Bone Mineral Measurements. Bethesda, MD: National Institute of Arthritis, Metabolism, and Digestive Diseases; 1980:94-98.
7. Lemann, J., Jr., et al. 1969. Possible role of carbohydrate-induced calciuria in calcium oxalate kidney-stone formation. New England Journal of Medicine 280:232-237.
8. Mazarlegos-Ramos E., et al. Consumption of soft drinks with phosphoric acid as a risk factor for the development of hypocalcemia in children: A case-control study. J Pediatr. 1995;126:940-942.
9. a) Heaney, R.P., et al. Effects of nitrogen, phosphorus, and caffeine on calcium balance in women. J Lab Clin Med. 1982;99:46-55.
b) Hernandez-Avila, M., et al. 1991. Caffeine, moderate alcohol intake, and risk of fractures of the hip and forearm in middle-aged women. American Journal Clinical Nutrition 54:157-163.
10. Daniell, H. Osteoporosis of the slender smoker; vertebral compression fractures and loss of metacarpal cortex in relation to postmenopausal cigarette smoking and lack of obesity. Arch Intern Med 136:298, 1976.
11. a) Bikle, D. Bone disease in alcohol abuse.ann Intern Med 103:42, 1985.
b) Spencer, H., et al. 1985. Alcohol-osteoporosis. American Journal Clinical Nutrition 41:847.
12. a) Define, A., et al. A longitudinal study of the effect of sodium and calcium intakes on regional bone density in postmenopausal women. American Journal Clinical Nutrition 1995;62:740-745.
b) Matkovic, V., et al. Urinary calcium, sodium, and bone mass of young females. American Journal Clinical Nutrition 1995;62:417-425.
13. a) Abelow, BlJ., et al. Cross-cultural association between dietary animal protein and hip fracture: A hypothesis. Calcif Tissue Int. 1992;50:14-18.
b) Ju J-F, et al. Dietary calcium and bone density among middle-aged and elderly women in China. American Journal Clinical Nutrition 1993;58:219-227.
c) Kin K., et al. Bone density and body composition on the Pacific Rim. A comparison between Japan-born and U.S. born Japanese-American women. J Bone Miner Res. 1993;8:861-869.
d) Russell-aulet, M., et al. Bone mineral density and mass in a cross-sectional study of white and Asian women. J Bone Miner Res. 1993;8:575-582.