Miscarriage (Spontaneous Abortion)

What Is Miscarriage?

[dropcap]M[/dropcap]iscarriage, or spontaneous abortion, is a reproductive failure characterized by loss of an unborn baby before the 20th week of pregnancy.

What Is Miscarriage In Celiac Disease and/or Gluten Sensitivity?

• Relationship between miscarriage and celiac disease. Miscarriage is a classic reproductive symptom and a complication of celiac disease that may be a presenting feature of untreated celiac disease.
• Relationship between miscarriage and correct diagnosis. A better knowledge of the relationship between celiac disease and spontaneous miscarriage may lead to correctly diagnosing and treating the cause of some cases of miscarriage, previously labeled as cases of unidentified origin.¹
• Relationship between miscarriage and failed diagnosis. ‘Unexplained’ is often undiagnosed. Considering celiac disease, which is often subclinical, in the differential diagnosis increases the probabililty of conception and uncomplicated pregnancy.²
• Relationship between miscarriage and zinc. Zinc deficiency has been incriminated in abortion. Zinc proteins are crucial to the development of a baby in that zinc proteins have been shown to be involved in the transcription and translation of genetic material.³
• Relationship between miscarriage and diet. The high incidence of miscarriage is effectively corrected by gluten-free diet in women with celiac disease.⁴

• Relationship between miscarriage and gluten. In vitro studies (laboratory) have provided two main pathogenic models of placental damage at the feto-maternal interface.  These are not yet proven.

• On the embryonic side of the placenta (baby side), a direct binding of anti-transglutaminase (-TG) antibodies to trophoblast cells that nourish the beginning baby damages them, which causes their death and results in miscarriage.
• Anti-TG antibodies may also be detrimental to endometrial angiogenesis (blood vessel formation) as shown in vitro in human endometrial endothelial cells (surface cells of the uterus). The angiogenesis inhibition seems to be the final effect of damage in surface cells of the endometrium caused by anti-TG antibodies.⁵

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

• A 15% rate of miscarriage was found in undiagnosed women with celiac disease vs. 6% in controls.⁶
• Untreated women 16-62 years with celiac disease showed significant rate of repeat miscarriage.⁷
• After treatment with gluten free diet, 1.3% of patients presented spontaneous miscarriage.⁸
• The relative risk of miscarriage was found to be 8.90 times higher in untreated mothers with celiac disease compared to mothers on a gluten-free diet.⁴

What Are The Symptoms Of Miscarriage?

In the mother, the dramatic shift in hormones and sadness due to the loss of her baby subjects her to:

• Emotional upheaval.
• Depression.
• Possible complications such as bleeding and painful breasts.

How Does Miscarriage Develop In Celiac Disease and/or Gluten Sensitivity?

• Spontaneous miscarriage results from unclear etiology involving gluten.⁸ It is proposed that the direct effect of anti-tissue transglutaminase antibodies on placenta cells of the fetus and on surface cells of the mother’s uterus results in miscarriage.⁵
• Celiac disease induces malabsorption and deficiency of factors essential for organogenesis (development of organs), e.g iron, folic acid, and vitamin K. The overall evidence suggest that celiac disease patients can be a group particularly susceptible to reproductive toxicants; however, the pathogenesis still awaits clarification.⁹
• Other deficiencies that impact abortion are vitamin A, protein, and zinc.
• Nutritional deficiencies are common before treatment with gluten free diet. In 2013, a study evaluating the nutritional status of 80 Dutch patients with newly diagnosed celiac disease showed 87% to have at least one nutrient deficit. Of these patients, 7.5% showed deficient levels of vitamin A, 20% for folic acid, 67% for zinc deficiency, 46% had decreased iron storage, and 32% had anaemia.¹⁰
• Although both celiac disease and the other manifestations of a deranged immunity might be explained on the basis of a common genetic predisposition to this kind of disorders, some findings suggest that celiac disease itself is responsible for the initiation of the immunological response. Indeed, persistent stimulation by some proinflammatory cytokines, such as interferon γ and tumor necrosis factor α, could induce further processing of autoantigens and their presentation to T lymphocytes by macrophage-type immunocompetent cells.¹¹
• Antiphospholipid syndrome (an associated disorder) induces fetal loss.¹²

Does Miscarriage Respond To Gluten-Free Diet?

The possible prevention or treatment of the effect of miscarriage in celiac disease can only be achieved through a life-long maintenance of a gluten free diet.¹³

Study results comparing untreated mothers with celiac disease with treated mothers with celiac disease indicated that the gluten-free diet reduced the relative risk of miscarriage by 9.18 times.⁴

6 Steps To Improve Risk For Miscarriage In Celiac Disease and/or Gluten Sensitivity:

• [dropcap]1[/dropcap]Remove the Trigger. Maintain a Strict, Nutritious Gluten Free Diet:

[box type=”shadow” ]Treatment. This condition responds to the complete elimination of gluten, which is the required treatment that improves both fetal health and maternal gut health.

• Gut health is the foundation to restore ALL health. Restored health will enable you to maintain a strict gluten free diet, just as other life tasks will be easier.
• A strict gluten free diet means removing 100% of wheat, barley, rye and oats from the diet.
• Cutting out bread and other obvious sources of gluten is not good enough for recovery. Even 1/8th teaspoon of flour or bread crumb is enough to sustain the inflammation that is damaging your small intestine, causing increased permeability (leaky gut) and allowing undigested gluten to enter your body where it can damage structures and function, and instigate immune inflammatory responses.

Correct Your Individual Nutritional Needs.

• Eat foods that can replenish missing nutrients. Find them under NUTRIENT DEFICIENCIES.
• Take nutritional supplements as needed. Find them under NUTRIENT DEFICIENCIES.

Recovery. You should begin to feel better within a week and notice more energy as inflammation subsides and the  absorbing cells that make up the surface lining of your small intestine are better able to function.

• Intestinal lining cells are replaced every 5 days. The healing process is like sunburn where the damaged surface layer of skin sloughs off and is replaced with new normal cells.
• Leaky gut normally resolves in two month after starting a gluten free diet and brings about a big improvement in health. Improvement in intestinal permeability precedes morphometric recovery (cell appearance and structure) of the small intestine in celiac disease.¹⁴
• The intestinal lining may take up to a year to heal.[/box]

• [dropcap]2[/dropcap] Reduce Inflammation. Foods to Eat and Foods Not to Eat:

Because gluten is inflammatory, eliminate OTHER inflammatory foods from your diet to reduce an additive effect to gluten. At the same time, try to eat foods that reduce inflammation (anti-inflammatory).

[box type=”shadow” ]Here Are Major Inflammatory Food Types That Reduce Healing:

• Damaging Foods. In susceptible persons, includes corn, dairy (cow), and soy. Lactose, the sugar in any animal milk disrupts intestinal permeability causing leaky gut.¹⁵
• Allergenic Foods. Includes foods that trigger the immune sytem to produce IgE antibodies. Allergy testing is the usual way to discover these offending foods.
• Shelf Stable Processed Foods. Includes any that contain additives and preservatives. Look for them on the nutrition label of the box or package. Additives and preservatives also disrupt intestinal permeability causing leaky gut.¹⁵
• Fats. Limit deep fried foods, trans-fats, saturated fats (animal fat/butter), and EXCESSIVE omega-6 fatty acid oils like corn oil. Rancid fats, sodium caprate (a medium chain fat), and sucrose monester fatty acid (a food grade surfactant) induce significant disruption of the intestinal barrier that causes leaky gut.¹⁵.
• Excessive Refined White Flours (bran layer removed). Includes products made from them such as cookies, bread, cakes, pies. Bran contains the vitamins and minerals that metabolize grains and slows the otherwise rapid entry of sugar from their digestion into the bloodstream. Also disrupt intestinal permeability causing leaky gut.¹⁵
• Refined Sugars.  Includes white sugar, corn fructose and high fructose corn syrup.
• Certain Spices. Includes paprika and cayenne pepper which disrupt intestinal permeability causing leaky gut.¹⁵
• Alcohol and Caffeine. Disrupt intestinal permeability causing leaky gut.¹⁵[/box]

[box type=”shadow” ]Here Are Important Anti-Inflammatory Food Types to Promote Health:

• Fruits. Contain ample amounts of vitamins, minerals and phytochemicals which are naturally occuring components in plants that detoxify toxins, carcinogens (reducing the risk by 50%) and mutagens.
• Non-Starchy Vegetables. Support intestinal integrity and provide ample amounts of vitamins, minerals and phytochemicals. Includes green leafy vegetables such as lettuce and kale, also onion, broccoli, garlic, and others.
• High Quality Complex Carbohydrates. Provide vitamins, minerals, and fiber while boosting serotonin levels to help you relax and feel calm. Includes whole grains, legumes, and root vegetables such as carrots, parsnips, sweet potatoes, turnips, red beets, and others.
• Antioxidants. Protect the body from inflammatory oxidant molecules that continually occur and help us handle stress and reduce irritability. Includes vitamin C-containing foods such as lemon, grapefruit, apricot, Brussels sprouts and strawberries, and others. Also, includes vitamin E-containing foods such as nuts, seeds, avocado, olive oil, and others. Cocoa is good, too.
• Omega-3 Fatty Acids. Balance opposing omega-6 fatty acids and bad fats. Fish sources includes tuna, salmon, cod, and others. Plants sources include flax, chia seeds, canola oil, and others.
• Probiotics. Supply normal microbes needed for colon health and health of the body such as these fermented foods: yogurt, kefir, and unpasteurized apple cider vinegar.
• Prebiotics/ High Fiber Foods.  Food with fiber keeps our population of colonic microbes healthy.
• Protective Herbs and Spices.  See below #6 below for examples.[/box]

• [dropcap]3[/dropcap] Information Sheet You Can Take to Your Doctor or Other Health Professional:

Click here.

• [dropcap]4[/dropcap] Manage Your Medications Safely:

[box type=”shadow” ]

Certain medications deplete iron, folic acid, vitamin K, vitamin A, protein, and zinc that promote spontaneous miscarriage. Ask your doctor or pharmacist about this possible adverse effect if you are taking any of the drugs listed below. Do not stop prescribed medications without supervision.

This is not a complete listing.

ANTACIDS / ULCER MEDICATIONS

• Pepcid®, Tagamet®, Zantac® deplete Folic Acid, Iron, Vitamin A, Zinc.
• Magnesium and Aluminum Antacid preparations (Gaviscon®, Maalox®, Mylanta®) deplete Folic Acid, Iron, Vitamin A, Zinc.
• Alka Seltzer®, Baking Soda deplete Folic Acid, Proteins.

ANTIBIOTICS disrupt intestinal permeability which complicates celiac disease.

• Gentomycin, Neomycin, Streptomycin, Cephalosporins, Penicillins deplete B Vitamins, Vitamin K.
•  Tetracyclines deplete Calcium, Magnesium, Iron, Vitamin B6, Zinc, Probiotics, Riboflavin.
• Cipro depletes Zinc.

ANTI-INFLAMMATORIES disrupt intestinal permeability which complicates celiac disease.

• Corticosteroids (Prednisone, Medrol®, Aristocort®, Decadron) deplete Zinc, Folic Acid.
• NSAIDS (Motrin®, Aleve®, Advil®, Anaprox®, Dolobid®, Feldene®, Naprosyn® and others) deplete Folic acid.
• Aspirin and Salicylates deplete Folic acid, Iron.

ANTICONVULSANTS

• Phenobarbital and Barbituates; and Dilantin®, Tegretol®, Mysoline®, Depakane/Depacon® deplete Calcium, Vitamin D, Folic Acid, Biotin, Carnitine, Vitamin B12, Vitamin B1, Vitamin K, Copper, Selenium, Zinc.

ANTIVIRAL AGENTS

• Zidovudine (Retrovir®, AZT and other related drugs) deplete Zinc.

CARDIOVASCULAR DRUGS

• Antihypertensives (Catapres®, Aldomet) deplete Zinc.
• ACE Inhibitors (Capoten®, Vasotec®, Monopril® and others) deplete Zinc.

CHOLESTEROL DRUGS

• Colestid® and Questran® deplete Vitamin A, Vitamin K, Folic Acid, Iron.

DIABETIC DRUGS 

• Metformin® depletes Folic acid.

DIURETICS

• Thiazide Diuretics (Hydrochlorothiazide, Enduron®, Diuril®, Lozol®, Zaroxolyn®, Hygroton® and others) deplete Zinc.
• Loop Diuretics (Lasix®, Bumex®, Edecrin®) deplete Zinc.
• Potassium Sparing Diuretics (Midamor®, Aldactone®, Dyrenium® and others) deplete Folic Acid, Zinc.

FEMALE HORMONES disrupt intestinal permeability which complicate celiac disease.

• Oral Contraceptives (Norinyl®, Ortho-Novum®, Triphasil®, and others) deplete Folic Acid, Zinc.
• Oral Estrogen/Hormone Replacement (Evista®, Prempro®, Premarin®, Estratab® and others) deplete Folic Acid,Zinc.

WEIGHT LOSS DRUGS THAT BIND FAT also interfere with absorption of some nutrients.

• Zenicol (Orlistat®) depletes Vitamin A, Vitamin K, Beta-carotene.

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• [dropcap]5[/dropcap]Nutritional Supplements To Help Correct Deficiencies:

[box type=”shadow” ]

The type and quantity of nutritional supplements that may be needed depend on which nutrients are deficient.

• Multivitamin/mineral combination once a day is useful to improve overall nutrient levels. This is a safe dose, but always check with your doctor to avoid interactions with medications.
• Vitamin A as prescribed following blood test for status.
• Vitamin D3 as prescribed following blood test for status.
• Chelated zinc as prescribed following blood test for status.
• Ferrous fumarate or gluconate following blood test for iron status

Storage Note: Store container tightly sealed, away from heat, moisture and direct light to avoid loss of potency. That is, in a safe kitchen cabinet – not in the bathroom or on the kitchen table.[/box]

• [dropcap]6[/dropcap]Manage Natural Remedies: 

[box type=”shadow” ]Hydration:

• Eight glasses of water are recommended per day unless there is a contraindication such as kidney or heart disease. The Institute of Medicine recommends approximately 2.7 liters (91 ounces) of total water, from all beverages and foods, each day for women and 3.7 liters (125 ounces) daily of total water for men.
• If you are thirsty, drink water. Add fresh, squeezed lemon to water. Lemon is anti-inflammatory, alkalizing and provides vitamin C.
• Hydration Test: Urine should be pale yellow. Fingertips should be plump, without pruning but this may not be reliable when fingers are swollen with edema. Lips should be plump, without puckering. The feeling of thirst can be unreliable.
• What is wrong with soda, coffee, tea, and alcohol? These drinks are dehydrating, increase acid, and deplete nutrients.[/box]

[box type=”shadow” ]Carminatives. The following  anti-inflammatory plant sources called carminitives help heal the digestive tract. They also tone the digestive muscles which improves peristalsis, thus aiding in the expulsion of gas from the stomach and intestine to relieve digestive colic and gastric discomfort.

Carminative Food Remedies:

• Raspberry.
• Carrot is also a cleansing digestive tonic.
• Grape is also bile stimulating and a cleansing remedy for sluggish digestion and laxative.
• Redbeets also stimulate and improve digestion and are easily digested.
• Cabbage also stimulates and improves digestion and is also a liver decongestant.
• Lettuce also stimulates and improves digestion and is also an alterative, meaning it improves the function of organs involved with the digestion and excretion of waste products to bring about a gradual change.
• Potatoes are antispasmodic (due to atropine like properties) and a liver remedy.

Carminative Herb Remedies:

• Sage is also a digestive, astringent, bile stimulant and energy tonic that heals the mucosa.  Drink as tea or use in cooking.
• Chamomile, lemon balm, and fennel, (as a tea) also help relieve nervous tension.
• Parsley also relieves indigestion.
• Rosemary as a tea and in cooking also is a nervous system tonic for stress and fatigue, bile stimulant, and can relieve headaches and indigestion.
• Thyme is also soothing remedy useful for stimulating digestion of rich, fatty foods.

Carminative Spice Remedies:

• Cloves are also antispasmodic.
• Nutmeg is also useful for indigestion.
• Ginger.[/box]

[box type=”shadow” ]Exercise Helps:

Exercise improves circulation and rids the body of toxins.

• Walking is aerobic exercise that reconditions the whole body to improve stamina. Read more about Exercise and Fitness.
• Weight training builds muscle. Read more about Exercise and Fitness.
• Stretching improves flexibilty. Read more about Exercise and Fitness.

Note: Exercise is important, but the amount and type of exercise undertaken depends on your health. Your first priority is to heal. [/box]

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

RESEARCH STUDY SUMMARIES

“Celiac disease and reproductive disorders: meta-analysis of epidemiologic associations and potential pathogenic mechanisms.” This study, which was undertaken to better define the risk of celiac disease in patients with reproductive disorders, as well as, the risk in known celiac disease patients of developing obstetric complications found that patients with recurrent miscarriage were found to have a significantly higher risk of celiac disease than the general population.

An extensive literature search of Medline and Embase databases was performed. Odds ratio (OR) and relative risk (RR) with 95% confidence intervals (95% CI) were used in order to combine data from case-control and cohort studies, respectively.

The OR for celiac disease was  5.82 (95% CI 2.30-14.74) in women experiencing recurrent miscarriage.

Furthermore, researchers found that in celiac patients, the risk of miscarriage, IUGR, low birth weight (LBW) and preterm delivery is significantly higher with an RR of 1.39 (95% CI 1.15-1.67), 1.54 (95% CI 1.22-1.95), 1.75 (95% CI 1.23-2.49) and 1.37 (95% CI 1.19-1.57), respectively. These patients should therefore be made aware of the potential negative effects of active celiac disease also in terms of reproductive performances, and of the importance of a strict diet to improve their health condition and reproductive health.¹⁶

“Vitamin and mineral deficiencies are highly prevalent in newly diagnosed celiac disease patients.” This study aiming to assess the nutritional and vitamin/mineral status of current “early diagnosed” untreated adult CD-patients in the Netherlands found that vitamin/mineral deficiencies are still common in newly “early diagnosed” CD-patients, even though the prevalence of obesity at initial diagnosis is rising.. Eighty newly diagnosed adult CD-patients were included and a comparable sample of 24 healthy Dutch subjects was added to compare vitamin concentrations.

Nutritional status and serum concentrations of folic acid, vitamin A, B₆, B₁₂, and (25-hydroxy) D, zinc, haemoglobin (Hb) and ferritin were determined  (before prescribing gluten free diet). Almost all CD-patients (87%) had at least one value below the lower limit of reference. Specifically, for vitamin A, 7.5% of patients showed deficient levels, for vitamin B₆ 14.5%, folic acid 20%, and vitamin B₁₂ 19%. Likewise, zinc deficiency was observed in 67% of the CD-patients, 46% had decreased iron storage, and 32% had anaemia. Overall, 17% were malnourished (>10% undesired weight loss), 22% of the women were underweight (Body Mass Index (BMI) < 18.5), and 29% of the patients were overweight (BMI > 25). Vitamin deficiencies were barely seen in healthy controls, with the exception of vitamin B₁₂. Vitamin/mineral deficiencies were counter-intuitively not associated with a (higher) grade of histological intestinal damage or (impaired) nutritional status. Extensive nutritional assessments seem warranted to guide nutritional advices and follow-up in CD treatment.¹⁷

“Gynecologic and obstetric findings related to nutritional status and adherence to a gluten-free diet in Brazilian patients with celiac disease.” This study investigating obstetric and gynecological disturbances in untreated women with Celiac Disease in relation to their nutritional status demonstrated a higher percentage of spontaneous abortions, anemia, and hypoalbuminemia vs. controls. After treatment with a gluten-free diet, patients presented with normal pregnancies and one patient presented spontaneous abortion. Celiac Disease should be included in the screening of spontaneous abortions.⁸

“Obstetric and gynecological problems in women with untreated celiac sprue.” Study investigating the obstetric and gynecological history of 54 women age 16-62 years showed significant rate of repeat abortions.¹⁸

“Female fertility, obstetric and gynaecological history in coeliac disease: a case control study.” This case control study investigating the incidence of abortions in Celiac Disease women demonstrated significantly more conceptions ended in miscarriage prior to diagnosis than among controls. After diagnosis and treatment with a gluten-free diet, the rate of miscarriage was similiar.¹⁹

“Celiac disease and pregnancy outcome.” This study designed as a case-control study and a before-after study investigated the effect of gluten-free diet on pregnancy outcome and lactation in 125 women affected with celiac disease. It found the high incidence of abortion, of low birth weight babies, and of short breast-feeding periods is effectively corrected by gluten-free diet in women with celiac disease.

In the case-control study, comparison of 94 untreated with 31 treated celiac women indicated that the relative risk of abortion was 8.90 times higher the relative risk of low birth weight baby was 5.84 times higher, and duration of breast feeding was 2.54 times shorter in untreated mothers. Abortion, low birth weight of baby, and duration of breast feeding did not significantly relate to the severity of celiac disease among untreated women. In the before-after study, 12 pregnant celiac women in either treated or untreated condition were compared. Results indicated that the gluten-free diet reduced the relative risk of abortion by 9.18 times reduced the number of low birth weight babies from 29.4% down to zero, and increased duration of breast feeding 2.38 times.⁴

CASE REPORT SUMMARIES

“Multiple immune disorders in unrecognized celiac disease: a case report.” This case report describes the course of a 34 year old female patient with unrecognized celiac disease and two miscarriages both at 16 weeks gestation. She was found to have multiple extra intestinal manifestations, mainly related to a deranged immune function, including macroamilasemia, macrolipasemia, IgA nephropathy, thyroiditis, and anti-b2-glicoprotein-1 antibodies, that disappeared or improved after the implementation of a gluten-free diet.

After six months of controlled gluten free diet, the patient’s body weight increased 12 kg; laboratory investigations demonstrated normalization of serum amylase, serum lipase and immunoglobulin levels; antigliadin, anti-2-glicoprotein-1 and anti-thyreoglobulin antibodies were no longer detectable, but antiendomysial antibodies were still present. Endoscopy showed a normal appearance of duodenal mucosa, and duodenal biopsy revealed a partial recovery of duodenal morphology. Due to the persistence of proteinuria (2.3 g/day), microscopic hematuria and hyaline and granular casts, a kidney biopsy showed that it was IgA nephropathy.

After 18 months of gluten-free diet, antiendomysial antibodies disappeared; creatinine clearance increased, but proteinuria further worsened (2.9 g/day, Table 1), and albumin levels were still low. After 24 months of gluten-free diet, a new duodenal biopsy showed complete recovery of villous architecture. Renal function further improved and proteinuria markedly decreased. Amylase, lipase, and immunoglobulin levels were within the normal range. Anti-2-glicoprotein-1, anti-thyreoglobulin, antigliadin, antiendomysial and anti-TTG antibodies were undetectable. A coagulation study was normal.

Although both celiac disease and the other manifestations of a deranged immunity might be explained on the basis of a common genetic predisposition to this kind of disorders, some findings suggest that celiac disease itself is responsible for the initiation of the immunological response. Indeed, persistent stimulation by some proinflammatory cytokines, such as interferon γ and tumor necrosis factor α, could induce further processing of autoantigens and their presentation to T lymphocytes by macrophage-type immunocompetent cells. As a matter of fact, the prevalence of immune diseases among patients with celiac disease seems proportional to the time of exposure to gluten, and many immune alterations disappear following the recognition of celiac disease and appropriate treatment, just as it occurred in our patient.²⁰

Sources:

1. Caramaschi P, Biasi D, Carletto A, Randon M, Pacor ML, Bambara LM. Celiac disease and abortion: focusing on a possible relationship. Recenti Progressi in Medicina. Feb 2000;91(2):72-5. [↩]
2. Bradley RJ, Rosen MP. Subfertility and gastrointestinal disease: ‘unexplained’ is often undiagnosed. Obstetrical and Gynecological Survey. Feb 2004;59(2):108-17. [↩]
3. Jameson S. Zinc status in pregnancy: the effect of zinc therapy on perinatal mortality, prematurity, and placental ablation. Annals of the New York Academy of Sciences. Mar 15, 1993;678:178-92. [↩]
4. Ciacci C, Cirillo M, Auriemma G, Di Dato G, Sabbatini F, Mazzacca G. Celiac disease and pregnancy outcome. Am J Gastroenterol. 1996 Apr;91(4):718-22. [↩] [↩] [↩] [↩]
5. Tersigni C, Castellani R, de Waure C, Fattorossi A, De Spirito M, Gasbarrini A, Scambia G, Di Simone N. Celiac disease and reproductive disorders: meta-analysis of epidemiologic associations and potential pathogenic mechanisms. Hum Reprod Update. 2014 Jul-Aug;20(4):582-93. doi: 10.1093/humupd/dmu007. [↩] [↩]
6. Sher KS, Mayberry JF. Female fertility, obstetric and gynaecological history in coeliac disease: a case control study. Acta Paediatrica. Supplementum. May 1996;412:76-7. [↩]
7. Molteni N, Bardella MT, Bianchi PA. Obstetric and gynecological problems in women with untreated celiac sprue. Journal of Clinical Gastroenterology. Feb 1999;12(1)37-9. [↩]
8. Kotze LM. Gynecologic and obstetric findings related to nutritional status and adherence to a gluten-free diet in Brazilian patients with celiac disease. Journal of Clinical Gastroenterology. Aug 2004;38(7):567-74. [↩] [↩] [↩]
9. Stazi AV, Mantovani A. A risk factor for female fertility and pregnancy: celiac disease. Gynecologica endocrinology: the Official Journal of the International Society of Gynecological Endocrinology. Dec 2000;14(6):454-63. [↩]
10. Wierdsma NJ, van Bokhorst-de van der Schueren MA, Berkenpas M, Mulder CJ, van Bodegraven AA. Vitamin and mineral deficiencies are highly prevalent in newly diagnosed celiac disease patients. Nutrients. 2013 Sep 30;5(10):3975-92. doi: 10.3390/nu5103975. [↩]
11. La Villa G, Pantaleo P, Tarquini R, Cirami L, Perfetto F, Mancuso F, Laffi G. Multiple immune disorders in unrecognized celiac disease: a case report. World J Gastroenterol  2003; 9(6): 1377-1380. [↩]
12. Shamir R, Shoenfeld Y, Blank M, et al. The prevalence of coeliac disease antibodies in patients with the antiphospholipid syndrome. Lupus. 2003;32:394-9. [↩]
13. Stazi AV, Mantovani A. A risk factor for female fertility and pregnancy: celiac disease. Gynecologica endocrinology: the Official Journal of the International Society of Gynecological Endocrinology. Dec 2000;14(6):454-63. [↩]
14. Cummins AG, Thompson FM, Butler RN, et al. Improvement in intestinal permeability precedes morphometric recovery of the small intestine in coeliac disease. Clinical Science. Apr 2001;100(4):379-86. [↩]
15. Farhadi A, Banan A, Fields J, Keshavarzian A. Intestinal barrier: an interface between health and disease. Journal of Gastroenterology and Hepatology. 2003;18:479-91. [↩] [↩] [↩] [↩] [↩] [↩]
16. Tersigni C, Castellani R, de Waure C, Fattorossi A, De Spirito M, Gasbarrini A, Scambia G, Di Simone N. Celiac disease and reproductive disorders: meta-analysis of epidemiologic associations and potential pathogenic mechanisms. Hum Reprod Update. 2014 Jul-Aug;20(4):582-93. doi: 10.1093/humupd/dmu007. [↩]
17. Wierdsma NJ, van Bokhorst-de van der Schueren MA, Berkenpas M, Mulder CJ, van Bodegraven AA. Vitamin and mineral deficiencies are highly prevalent in newly diagnosed celiac disease patients. Nutrients. 2013 Sep 30;5(10):3975-92. doi: 10.3390/nu5103975. [↩]
18. Molteni N, Bardella MT, Bianchi PA. Obstetric and gynecological problems in women with untreated celiac sprue. Journal of Clinical Gastroenterology. Feb 1999;12(1)37-9. [↩]
19. Sher KS, Mayberry JF. Female fertility, obstetric and gynaecological history in coeliac disease: a case control study. Acta Paediatrica. Supplementum. May 1996;412:76-7. [↩]
20. La Villa G, Pantaleo P, Tarquini R, Cirami L, Perfetto F, Mancuso F, Laffi G. Multiple immune disorders in unrecognized celiac disease: a case report. World J Gastroenterol  2003; 9(6): 1377-1380. [↩]