Calcium Deficiency

What Is Calcium?

[dropcap]C[/dropcap]alcium is the most abundant mineral in the body, with 99% residing in teeth and bones where it constitutes 40% of skeletal bone weight along with 45% phosphorus.

As a component of hard tissues, calcium fulfills a structural role to maintain body size and acts as attachments for musculoskeletal tissues.

Q: What does the non-skeleton calcium do in the body?

A: The remaining 1% of calcium is present in blood and soft tissues. Calcium levels in the blood are maintained within very strict limits by dietary intake, hormonal regulation and a rapidly exchangeable pool in bone tissue. The many important functions are described below.

What Is Calcium Deficiency In Celiac Disease and/or Gluten Sensitivity?

• Relationship between calcium deficiency and celiac disease. Calcium deficiency is a symptom of celiac disease that results when the level within cells is too low to meet metabolic needs of the body for this mineral.
• Relationship between calcium deficiency and effects. Deficiency is characterized by bone and tooth demineralization causing weak teeth and fragile bones and impaired nerve conduction, muscle contraction, blood clotting, blood pressure regulation, glycogen to glucose conversion, many hormone actions, many enzyme activities, and acetylcholine production.
• Relationship between calcium deficiency and vitamin D in celiac disease. Research demonstrates that calcium malabsorption in celiac disease does not result from the absence of vitamin D receptors, but rather from reduction of vitamin D regulated proteins and functions essential for active calcium absorption that are located in the enterocytes of the villi.¹
• Relationship between calcium deficiency and  diet in celiac disease. A study investigating life-long gluten-free diet in celiac disease patients shows that inadequate intake of calcium is common (more than 10% of patients) and may relate to habitual poor food choices in addition to inherent deficiencies in the gluten free diet. “Dietary education should also address the achievement of adequate micronutrient intake.”²

How Prevalent Is Calcium Deficiency In Celiac Disease and/or Gluten Sensitivity?

Calcium deficiency affects 100% of study subjects with untreated celiac disease.³ There was a significantly lower mean blood calcium in children with dental enamel defects who were found to have celiac disease (7.9 mg/dL compared to nonceliacs 9.6mg/dl).⁴

What Are The Symptoms Of Calcium Deficiency?

• Anxiety.
• Bone pain.
• Change in saliva composition to inadequate calcium for replenishment for tooth enamel.
• Dental caries (cavities).
• Dental enamel defects.
• Elevated blood pressure.
• Eye Floaters.
• Excessive bleeding from injury.
• Fat stores around organs is increased.
• Fatigue.
• Impaired blood clotting.
• Insomnia.
• Irritability.
• Mental dullness.
• Muscle cramps advancing to tetany and/or seizures.
• Muscle spasms or twitches.
• Muscle weakness.
• Osteomalacia.
• Osteopenia advancing to Osteoporosis.
• In children, rickets occur.
• Cataracts occur in chronic deficiency.
• Seizures and laryngospasm occur when deficiency is severe.

How Does The Body Get Calcium?

• Calcium must be obtained from the diet since the body cannot make it. Calcium absorption requires ionization. Calcium mineral becomes ionized (receives a positive electrical charge) in the acidic environment of stomach juice.
• Ionized calcium is absorbed by active transport in the duodenum where an acid medium prevails and by passive transfer throughout the remainder of the small bowel where the pH is alkaline, providing there is adequate absorptive surface area.
• Active transport is controlled through the action of vitamin D. Vitamin D increases calcium absorption at the brush border (microscopic structures) that cover absorbing villi and stimulates production of calcium binding protein.⁵ Villi are tiny, multitudinous strucures that form the small intestinal mucosa lining.
• The parathyroid glands play a major role in maintaining calcium balance in the blood by the production and activity of parathyroid hormone.
• EPA increases calcium levels in the body, preventing bone loss.
• Albumin, a major blood protein, is needed to carry calcium in blood.

What Does Calcium Do In The Body?

1. Essential for enzyme activation;
2. Second messenger roles (transmitting hormonal information);
3. Essential for blood clotting;
4. Opposes phosphorus as a buffer to maintain acid-alkaline balance of the blood;
5. Required for neuromuscular transmission;
6. Required for muscle activity: contraction and normal muscle tone and muscle irritability;
7. Maintains cell permeability for the activation of body enzymes;
8. Essential for cell and cell organelle membrane function (stabilization and transport); and
9. Required for milk production in the nursing of infants.

How Does Calcium Deficiency Develop?

Calcium deficiency results from malabsorption in celiac disease. That is, calcium is rendered unabsorbable due to these mechanisms:

• Deficiency results primarily from malabsorption of this mineral due to inflammation of intestinal lining as an immune response to gluten that results in inadequate absorbing surface area.
• Malabsorption can occur as a consequence of low stomach acid. Sufficient acid is required to ionize calcium (receives a positive electric charge) which is required for absorption later in the small intestine. That is, no electric charge, no absorption.
• Malabsorption can occur as a consequence of insufficient carrier proteins needed to transport ionized into the bloodstream from the absorbing cells of the small intestine.
• Binding with unabsorbed fatty acids present because of fat malabsorption, Calcium readily binds with fat to form soaps which cannot be absorbed but rather pass into the colon and out of the body.
• Reduction of vitamin D regulated proteins needed for active transport from the gut to the bloodstream.
• Insufficient albumin in the blood needed to carry calcium.
• Insufficient EPA to maintain calcium levels in the body.

Does Calcium Deficiency Respond To A Gluten-Free Diet?

Yes. Calcium deficiency responds to gluten free diet. Patients with decreased axial bone density (Dexa scan) should obtain 1200 mg calcium and 400 mg of vitamin D daily.⁶

Adding vinegar, such as rice (not white distilled), to meals helps to dissolve calcium in food and enhances absorption of calcium from the small intestine.⁷

6 Steps To Correct Calcium Deficiency In Celiac Disease and/or Gluten Sensitivity:

• [dropcap]1[/dropcap]Meet, or Exceed the RDA (Recommended Dietary Allowances) for Calcium in milligrams (mg) per day:

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200 mg for infants birth-6 months; 260 mg for infants 7-12 months;

700 mg for children 1-3 years; 1,000 mg for children 4-8 years;

1300 mg for children 9-12 years; 1,300 mg for teens 14-18 years;

1,000 mg for adults 19-50 years;

1000 mg for males 51-70 years; 1,200 mg for females 51-70 years:

1200 mg for males and females over 71 years;

1,000 mg for pregnancy; 1,000 mg for breastfeeding women.⁸[/box]

• [dropcap]2[/dropcap]Diet – Include Food Sources Richest in Calcium: 

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Animal Milk Sources:

Food Sources of calcium ranked by milligrams of calcium per standard amount; also calories in the standard amount.

Food, Standard Amount	Calcium (mg)	Calories
Plain yogurt, non-fat (13 g protein/8 oz), 8-oz container	452	127
Romano cheese, 1.5 oz	452	165
Pasteurized process Swiss cheese, 2 oz	438	190
Plain yogurt, low-fat (12 g protein/8 oz), 8-oz container	415	143
Fruit yogurt, low-fat (10 g protein/8 oz), 8-oz container	345	232
Swiss cheese, 1.5 oz	336	162
Ricotta cheese, part skim, ½ cup	335	170
Pasteurized goat milk with added vitamin D, 1 cup	328	140
Pasteurized process American cheese food, 2 oz	323	188
Provolone cheese, 1.5 oz	321	150
Mozzarella cheese, part-skim, 1.5 oz	311	129
Cheddar cheese, 1.5 oz	307	171
Fat-free (skim) milk, 1 cup	306	83
Muenster cheese, 1.5 oz	305	156
1% low-fat milk, 1 cup	290	102
Low-fat chocolate milk (1%), 1 cup	288	158
2% reduced fat milk, 1 cup	285	122
Reduced fat chocolate milk (2%), 1 cup	285	180
Buttermilk, low-fat, 1 cup	284	98
Chocolate milk, 1 cup	280	208
Whole milk, 1 cup	276	146
Yogurt, plain, whole milk (8 g protein/8 oz), 8-oz container	275	138
Ricotta cheese, whole milk, ½ cup	255	214
Gluten-Free Blue cheese, 1.5 oz	225	150
Mozzarella cheese, whole milk, 1.5 oz	215	128
Feta cheese, 1.5 oz	210	113

Source: Nutrient values from Agricultural Research Service (ARS) Nutrient Database for Standard Reference, Release 17. Foods are from ARS single nutrient reports, sorted in descending order by nutrient content in terms of common household measures.

Plant Sources and Non-Milk Sources Have Lesser Amounts:

Non-Dairy Food Sources of calcium ranked by milligrams of calcium per standard amount; also calories in the standard amount. The bioavailability may vary…see explanation below.

Food, Standard Amount	Calcium (mg)	Calories
Soy beverage, calcium fortified, 1 cup	368	98
Sardines, Atlantic, in oil, drained, 3 oz	325	177
Tofu, firm, prepared with nigarib , ½ cup	253	88
Pink salmon, canned, with bone, 3 oz	181	118
Collards, cooked from frozen, ½ cup	178	31
Molasses, blackstrap, 1 Tbsp	172	47
Spinach, cooked from frozen, ½ cup	146	30
Soybeans, green, cooked, ½ cup	130	127
Turnip greens, cooked from frozen, ½ cup	124	24
Ocean perch, Atlantic, cooked, 3 oz	116	103
Cowpeas, cooked, ½ cup	106	80
White beans, canned, ½ cup	96	153
Kale, cooked from frozen, ½ cup	90	20
Okra, cooked from frozen, ½ cup	88	26
Soybeans, mature, cooked, ½ cup	88	149
Blue crab, canned, 3 oz	86	84
Beet greens, cooked from fresh, ½ cup	82	19
Pak-choi, Chinese cabbage, cooked from fresh, ½ cup	79	10
Clams, canned, 3 oz	78	126
Dandelion greens, cooked from fresh, ½ cup	74	17
Rainbow trout, farmed, cooked, 3 oz	73	144

Both calcium content and bioavailability should be considered when selecting dietary sources of calcium. Some plant foods have calcium that is well absorbed, but the large quantity of plant foods that would be needed to provide as much calcium as in a glass of milk may be unachievable for many. Many other calcium-fortified foods are available, but the percentage of calcium that can be absorbed is unavailable for many of them.

Note: Vinegar, such as rice (not white distilled), consumed with calcium-containing food has been shown to improve the ability of calcium to dissolve out of food and to enhance the absorption of calcium from the small intestine.⁹[/box]

• [dropcap]3[/dropcap] Diet – Avoid  or Limit These Foods That Deplete or Interfere With Absorption:

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• High fat meals bind calcium in the intestines, causing what is bound to be passed out of the body with stool.
• High oxalate-containing food like rhubarb, spinach, chard and beet greens bind calcium in the intestines, causing what is bound to be passed out of the body with stool.
• High phytic acid-containing foods like whole grains and seeds bind calcium in the intestines, causing what is bound to be passed out of the body with stool.
• High fiber foods interfere with absorption of calcium in the intestines, causing loss with stool.

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• [dropcap]4[/dropcap]Monitor Medications That Deplete or Interfere With Absorption:

[box type=”shadow” ]Here are common medications that deplete calcium. Ask your doctor or pharmacist about possible interactions between calcium supplements and medications you’re taking to make sure you time the doses correctly. Do not stop prescribed medications without supervision.

• Antacids/Ulcer Medications – Pepcid®, Tagamet®, Zantac®.
• Magnesium and Aluminum Antacid preparations (Gaviscon®, Maalox®, Mylanta®).
• Tetracyclines.
• Anticonvulsants – Phenobarbital and Barbituates; and Dilantin®, Tegretol®, Mysoline®, Depakane/Depacon®.
• Aspirin and Salicylates.
• Corticosteroids (Prednisone, Medrol®, Aristocort®, Decadron®).
• Foscanet (anti-viral).
• Potassium Sparing Diuretics (Midamor®, Aldactone®, Dyrenium® and others).
• Loop Diuretics (Lasix®, Bume®x, Edecrin®).

You may need to take calcium supplements several hours before or after taking your medications.[/box]

• [dropcap]5[/dropcap]Manage Nutritional Supplements to Obtain Calcium:

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• Calcium is available in tablet and chewable forms and as part of multivitamin/ mineral supplements.
• In general, daily calcium intakes of 2,000 mg or less are safe.
• Calcium intakes greater than 2,000-4,000 mg daily may depress absorption of magnesium, zinc, iron, manganese and other minerals, and are associated with depressed reflexes, muscle weakness, ataxia and anorexia.

Caution:

• Individuals with tendency to form kidney stones should consult a physician before increasing calcium intake.
• Milk-alkali syndrome (calcium deposition in soft tissues and kidney stones) is possible after consumption of 2 or more quarts of milk daily along with large amounts of carbonate antacids.[/box]

• [dropcap]6[/dropcap]Other Supplements That Deplete or Interfere With Absorption:

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• Calcium interferes with selenium, magnesium and other minerals, therefore it should be taken separately 2 hours before or after.
• Phosphorus interferes with the balance of calcium. [/box]

What Do Medical Research Studies Tell About Calcium Deficiency In Celiac Disease and/or Gluten Sensitivity?

RESEARCH STUDY SUMMARIES

“Nutritional inadequacies of the gluten-free diet in both recently-diagnosed and long-term patients with celiac disease.” This study investigating life-long gluten-free diet (GFD) in celiac disease patients aimed to determine the nutritional adequacy of the ‘no detectable gluten’ diet. Results show that inadequate intake of calcium is common (more than 10%) and may relate to habitual poor food choices in addition to inherent deficiencies in the GFD. “Dietary education should also address the achievement of adequate micronutrient intake.”

A seven-day prospective food intake was assessed in 55 patients who were adherent to a GFD for more than 2 years and in 50 newly-diagnosed age- and sex-matched patients (18-71 years, 24% male) studied prospectively over 12 months on GFD. Historical pre-celiac intake was also assessed in the latter group. Intake was compared with Australian Nutritional Recommendations and the Australian population data.

RESULTS: Nutritional intake was similar between groups. Of macronutrients, only starch intake fell over 12 months (26% to 23%). Fibre intake was inadequate for all except in diet-experienced men. More than one in 10 of both newly-diagnosed and experienced women had inadequate thiamin, folate, vitamin A, magnesium, calcium and iron intakes. More than one in 10 newly-diagnosed men had inadequate thiamin, folate, magnesium, calcium and zinc intakes. Inadequate intake did not relate to nutrient density of the GFD. Inadequacies of folate, calcium, iron and zinc occurred more frequently than in the Australian population. The frequency of inadequacies was similar pre- and post-diagnosis, except for thiamin and vitamin A, where inadequacies were more common after GFD implementation.  Because dietary intake patterns at 12 months on a GFD are similar to longer-term intake, researchers stress that fortification of GF foods also need to be considered.”²

“Screening for celiac disease in children with dental enamel defects.” Study investigating prevalence of celiac disease in 140 children with dental enamel defects compared to a group of 720 children free from any dental enamel defects recruited as controls demonstrated that celiac disease is more prevalent among children with dental enamel defects than in the general population and that lower serum calcium significantly predicted celiac disease in this cohort. (17.86%) compared to controls (0.97%) Importantly, There was a significantly lower mean blood calcium and phosphorous and a higher mean serum alkaline phosphatase among cases compared to controls.¹⁰ than in the control group (-1.3 ± 13.6 cm(2)). In the lite orange juice trial, the reduction of VAT was significantly greater in the CaD group (-13.1 ± 18.4 cm(2)) than in the control group (-6.4 ± 17.5 cm(2)) after control for baseline VAT. The effect of calcium and vitamin D on VAT remained highly significant when the results of the 2 trials were combined.¹¹

“Calcium plus vitamin D3 supplementation facilitated fat loss in overweight and obese college students with very-low calcium consumption: a randomized controlled trial.” This study investigating the effect of calcium plus vitamin D3 (calcium+D) supplementation on anthropometric and metabolic profiles during energy restriction in healthy, overweight and obese adults with very-low calcium consumption found that calcium plus vitamin D3 supplementation for 12 weeks augmented body fat and visceral fat loss in very-low calcium consumers during energy restriction.

Fifty-three subjects were randomly assigned in an open-label, randomized controlled trial to receive either an energy-restricted diet (about 500 kcal/d) supplemented with 600 mg elemental calcium and 125 IU vitamin D3 or energy restriction alone for 12 weeks. Repeated measurements of variance were performed to evaluate the differences between groups for changes in body weight, BMI, body composition, waist circumference, and blood pressures, as well as in plasma TG, TC, HDL, LDL, glucose and insulin concentrations.

Eighty-one percent of participants completed the trial (85% from the calcium + D group; 78% from the control group). A significantly greater decrease in fat mass loss was observed in the calcium + D group (-2.8±1.3 vs.-1.8±1.3 kg; P=0.02) than in the control group, although there was no significant difference in body weight change between groups. The calcium + D group also exhibited greater decrease in visceral fat mass and visceral fat area. No significant difference was detected for changes in metabolic variables.¹²

“Enhancing effect of dietary vinegar on the intestinal absorption of calcium in ovariectomized rats.” This animal study investigating the effects of dietary vinegar on the absorption of calcium from food suggests that dietary vinegar enhanced intestinal calcium absorption by improving calcium solubility (dissolved) and by the trophic effect of the acetic acid contained in vinegar, which would reduce bone turnover and be helpful in preventing osteoporosis.

Researchers first removed the ovaries (ovariectomy) from rat subjects to induce bone loss such as seen in osteoporosis. The apparent absorption of calcium was higher when the rats were fed on a diet containing 1.6% vinegar for 32 days than when fed on a diet without vinegar. The calcium content in the femur (thigh bones) of the rats given diets containing 0.4% and 1.6% vinegar were also higher. The serum parathyroid hormone level was lower and the crypt depth of the duodenum thicker in the rats fed on a diet containing 1.6% vinegar.⁹

“Intestinal calcium absorption is shown by stable strontium test in celiac disease before and after gluten-free diet.” This study investigating calcium at diagnosis and after one year of gluten fee diet demonstrated significantly abnormal levels of calcium in all women with untreated celiac disease.³

“Localization of vitamin D receptor in normal human duodenum and in patients with celiac disease.” Study investigating receptors for calcitrol, the active metabolite of vitamin D, demonstrated that calcium malabsorption in celiac disease does not result from the absence of vitamin D receptors, but rather from reduction of vitamin D regulated proteins and functions essential for active calcium absorption that are located in the enterocytes of the villi.¹³

CASE REPORT SUMMARIES

“Celiac disease causing symptomatic hypocalcaemia, osteomalacia and coagulopathy.” This case report describes diagnosing celiac disease in a 36-year-old gentleman who presented with 6 months of poor energy, tingling in fingers and weight loss with a change in bowel habit. He appeared cachectic and had clubbing, demineralisation of teeth, pectus carinatus, kyphosis, spinal tenderness, proximal muscle weakness and generalised muscle wasting (atrophy).

Chvostek’s and Trosseau’s signs were positive. His hemoglobin (Hb) was 8.7 g/dl, MCV 64.7 fl with low iron. Calcium corrected was 1.30 nmol/l, parathyroid hormone 440.4 ng/l, vitamin D <12.5 nmol/l; INR was 2.7 with coagulation inhibitor studies negative. Radiographs of spine and pelvis commented on osteopenia with thoracic kyphosis and mild anterior wedging of thoracic vertebrae. Antitissue transglutaminase was 145 U/ml, and antiendomysial antibodies were positive. An esophagogastroduodenoscopy was consistent with celiac disease. A diagnosis of osteomalacia and coagulopathy secondary to celiac disease was made.

The hypocalcaemia was treated with calcium gluconate infusions with symptomatic relief. Coagulopathy was treated with vitamin K intravenously with normalization of INR (international normalised ratio), a lab measurement to determine coagulation.¹⁴

“Disabling osteomalacic myopathy as the only presenting feature of coeliac disease.” This case report describes diagnosing celiac disease in a 59-year-old woman who presented with a 3-month history of bilateral, proximal lower-limb weakness associated with disabling pain that rendered her wheelchair-bound. There were no gastrointestinal symptoms. Clinical examination showed evidence of bilateral, proximal muscle atrophy and weakness in the lower limbs. Low serum calcium and raised serum alkaline phosphatase, coupled with radiological findings, led to the diagnosis of osteomalacia. Subsequent gastroscopy and duodenal biopsy confirmed a diagnosis of coeliac disease.

With adherence to a gluten-free diet, the patient’s condition remarkably improved within 3 months and she could walk pain-free using a stick. Osteomalacia and myopathy may rarely be the initial and primary presentations of coeliac disease. There are very few reports of osteomalacia as the only presentation of coeliac disease and no reports that describe such a dramatic recovery 3 months after commencing a gluten-free diet.¹⁵

Sources:

1. Colston KW, Mackay AG, Finlayson C, Wu CJ, Maxwell JD. Localization of vitamin D receptor in normal human duodenum and in patients with celiac disease. Gut. Sep 1994; 35(9):1219-25. [↩]
2. Shepherd SJ1, Gibson PR. Nutritional inadequacies of the gluten-free diet in both recently-diagnosed and long-term patients with coeliac disease. J Hum Nutr Diet. 2013 Aug;26(4):349-58. doi: 10.1111/jhn.12018. [↩] [↩]
3. Molteni N, Bardella MT, Vezolli G, Pozzoli E, Bianchi P. Intestinal calcium absorption is shown by stable strontium test in celiac disease before and after gluten-free diet. American Journal of Gastroenterology. Nov. 1995;90(11):2025-8. [↩] [↩]
4. El-Hodhod MA, El-Agouza IA, Abdel-Al H, Kabil NS, Bayomi KA. Screening for celiac disease in children with dental enamel defects. ISRN Pediatr. 2012;2012:763783. Epub 2012 Jun 7. [↩]
5. Kathleen Mahan and Sylvia Escott-Stump, ed. Krause’s Food, Nutrition & Diet Therapy, 10th Edition. Philadelphia, PA. USA: W.B. Saunders Company, 2000. [↩]
6. Murray JA, the widening spectrum of celiac disease. American Journal of Clinical Nutrition. Mar 1999; 69(3):354-365. [↩]
7. Kishi M, Fukaya M, Tsukamoto Y, Nagasawa T, Takehana K, Nishizawa N. Enhancing effect of dietary vinegar on the intestinal absorption of calcium in ovariectomized rats. Biosci Biotechnol Biochem. 1999 May;63(5):905-10. [↩]
8. https://ods.od.nih.gov/factsheets/Calcium-Consumer/ [↩]
9. Kishi M, Fukaya M, Tsukamoto Y, Nagasawa T, Takehana K, Nishizawa N. Enhancing effect of dietary vinegar on the intestinal absorption of calcium in ovariectomized rats. Biosci Biotechnol Biochem. 1999 May;63(5):905-10. [↩] [↩]
10. El-Hodhod MA, El-Agouza IA, Abdel-Al H, Kabil NS, Bayomi KA. Screening for celiac disease in children with dental enamel defects. ISRN Pediatr. 2012;2012:763783.)

    “Calcium and vitamin D supplementation is associated with decreased abdominal visceral adipose tissue in overweight and obese adults.” This study  investigating the effect of  calcium and vitamin D on obesity showed findings that suggest calcium and/or vitamin D supplementation contributes to a beneficial reduction of visceral abdominal fat (VAT).

    Two parallel double-blind, placebo-controlled trials were conducted in which 171 people were given either orange juice fortified with 350mg of calcium and 100 IU of vitamin D (CaD) or non-fortified orange calcium and vitamin D juice. After four months, the average weight loss in both groups was the same – about 5.5 pounds. Scans revealed that in the group supplemented with calcium and vitamin D, the loss of visceral (abdominal) fat was significantly greater than the loss of subcutaneous fat, which is fat under the skin.

    After 16 wk, the average weight loss (about 2.45 kg) did not differ significantly between groups. In the regular orange juice trial, the reduction of VAT was significantly greater in the CaD group (-12.7 ± 25.0 cm(2 [↩]

11. Rosenblum JL, Castro VM, Moore CE, Kaplan LM. Calcium and vitamin D supplementation is associated with decreased abdominal visceral adipose tissue in overweight and obese adults.Am J Clin Nutr. 2012 Jan;95(1):101-8. doi: 10.3945/ajcn.111.019489. [↩]
12. Zhu W, Cai D, Wang Y, Lin N, Hu Q, Qi Y, Ma S, Amarasekara S. Calcium plus vitamin D3 supplementation facilitated fat loss in overweight and obese college students with very-low calcium consumption: a randomized controlled trial. Nutr J. 2013 Jan 8;12:8. doi: 10.1186/1475-2891-12-8. [↩]
13. Colston KW, Mackay AG, Finlayson C, Wu CJ, Maxwell JD. Localization of vitamin D receptor in normal human duodenum and in patients with celiac disease. Gut. Sep 1994; 35(9):1219-25. [↩]
14. McNicholas BA, Bell M. Coeliac disease causing symptomatic hypocalcaemia, osteomalacia and coagulapathy. BMJ Case Rep. 2010 Dec 1;2010. pii: bcr0920092262. doi: 10.1136/bcr.09.2009.2262. [↩]
15. Byrne MF, Razak AR, Leader MB, Sheehan KM, Patchett SE. Disabling osteomalacic myopathy as the only presenting feature of coeliac disease. Eur J Gastroenterol Hepatol. 2002 Nov;14(11):1271-4. [↩]