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Glyphosate's chelating action can have profound effects on iron in plants Eker et al. Glyphosate interferes with iron assimilation in both glyphosate-resistant and glyphosate-sensitive soybean crops Bellaloui et al. It is therefore conceivable that glyphosate's chelation of iron is responsible for the refractory iron deficiency present in celiac disease.

Erythropoietin EPO , also called hematopoietin, is a cytokine produced by interstitial fibroblasts in the kidney that regulates red blood cell production. Low EPO levels, leading to a low turnover rate of red blood cells, is a feature of celiac disease Bergamaschi et al. This can lead to megaloblastic anemia, where red blood cells are large macrocytic and reduced in number due to impaired DNA synthesis.

A recent hematological study on mice exposed to Roundup at subacute levels for just 15 days revealed an anemic syndrome in both male and female mice, with a significant reduction in the number of erythrocytes and in hemoglobin, reduced hematocrit and increased mean corpuscular volume, indicative of macrocytic anemia Jasper et al. Molybdenum deficiency is rarely considered in diagnoses, as it is only needed in trace amounts. However, molybdenum is essential for at least two very important enzymes: sulfite oxidase and xanthine oxidase.

Sulfite oxidase converts sulfite, a highly reactive anion, to sulfate, which is much more stable. Sulfite is often present in foods such as wine and dried fruits as a preservative. Sulfate plays an essential role in the sulfated proteoglycans that populate the extracellular matrices of nearly all cell types Turnbull et al. So, impaired sulfite oxidase activity leads to both oxidative damage and impaired sulfate supplies to the tissues, such as the enterocytes in the small intestine.

The excess presence of sulfur-reducing bacteria such as Desulfovibrio in the gut in association with celiac disease Collado et al. These distal sites could reoxidize the H 2 S through an alternative pathway that does not require molybdenum for sulfur oxidation Ingenbleek and Kimura, Xanthine oxidase XO produces uric acid from xanthine and hypoxanthine, which are derived from purines. It is activated by iron, which, as we have seen, is often intractably deficient in association with celiac disease.

Impaired XO activity would be expected to drive purines towards other degradation pathways. Adenosine deaminase ADA , a cytoplasmic enzyme that is involved in the catabolism of purine bases, is elevated in celiac disease, and is therefore a useful diagnostic marker Cakal et al.

In fact, elevation of ADA is correlated with an increase in several inflammatory conditions. Impaired purine synthesis is expected in the context of cobalamin deficiency as well, because methyl melonlyl CoA mutase depends on catalytic action by cobalamin Allen et al. Decreased purine synthesis results in impaired DNA synthesis, which then leads to megaloblastic anemia Boss, , due to slowed renewal of RBC's from multipotent progenitors, a problem that is compounded by suppressed EPO activity Bergamaschi et al. A remarkable recent case of a three-month old infant suffering from molybdenum deficiency links several aspects of glyphosate toxicity together, although glyphosate exposure was not considered as a possible cause in this case Boles et al.

This child presented with microcephaly, developmental delay, severe irritability, and lactic acidosis. Lactic acidosis is a striking feature of intentional glyphosate poisoning induced by drinking Roundup Zouaoui et al. In vitro studies of glyphosate in the formulation Roundup have demonstrated an ability to disrupt oxidative respiration by inducing mitochondrial swelling and inhibiting mitochondrial complexes II and III Peixoto, This would explain a massive build-up of lactic acid following ingestion of Roundup, due to a switch to anaerobic metabolism.

Glyphosate has also been shown to uncouple mitochondrial phosphorylation in plants Haderly et al. As has been stated previously, microcephaly is a feature of excess RA, which could be induced by glyphosate due to its inhibitory action on CYP enzymes. In the case study on molybdenum deficiency Boles et al. Serum hypouricemia was also present, indicative of impaired XO activity.

So, the induction of excess RA, depletion of molybdenum, and lactic acidosis by glyphosate provide a plausible environmental factor in this case. One final aspect of molybdenum deficiency involves nitrate metabolism. As a source of nitric oxide, inorganic nitrite regulates tissue responses to ischemia. While nitrate reductase activity has been known to be a capability of microbes for many years, it has only recently been realized that mammals also possess a functioning nitrate reductase capability, utilizing a molybdenum-dependent enzyme to produce nitrite from nitrate Jansson et al.

Molybdenum deficiency would impair this capability, likely contributing to the higher risk to venous thrombosis observed in celiac disease Zenjari et al.

Autoimmune thyroid disease is associated with celiac disease Collin et al. In Valentino et al. Selenium, whose deficiency is associated with celiac disease Hinks et al. Twenty five specific selenoproteins are derived from this amino acid. Selenium deficiency can lead to an impairment in immune function and spermatogenesis in addition to thyroid function Papp et al. One very important selenoprotein is glutathione peroxidase, which protects cell membranes and cellular components against oxidative damage by both hydrogen peroxide and peroxynitrite ONOO — Prabhakar et al.

Wheat can be a good source of selenoproteins. However, the content of selenium in wheat can range from sufficient to very low, depending upon soil physical conditions.

Since glyphosate has been shown to deplete sulfur in plants Saes Zobiole et al. A gluten-free diet will guarantee, however, that no selenium is available from wheat, inducing further depletion of selenoproteins, and therefore increasing the risk to immune system, thyroid and infertility problems in treated celiac patients.

The gut bacterium Lactobacillus, which is negatively impacted by glyphosate Shehata et al.

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Selenocysteine is present in the catalytic center of enzymes that protect the thyroid from free radical damage Triggiani et al. Free radical damage would lead to apoptosis and an autoimmune response Tsatsoulis, Glyphosate's disruption of these bacteria would lead to a depletion in the supply of selenomethionine and selenocysteine.

Methionine depletion by glyphosate Nafziger et al. Thus, there are a variety of ways in which glyphosate would be expected to interfere with the supply of selenoproteins to the body, including its effects on Lactobacillus, its depletion of methionine, the no-till farming methods that are possible because weeds are killed chemically, and the likely interference with plant uptake of inorganic selenium.

This aligns well with the observed higher risk of thyroid problems in association with celiac disease, in addition to infertility problems and immune issues, which are discussed elsewhere in this paper. Further support for an association between glyphosate and thyroid disease comes from plots over time of the usage of glyphosate in the U.

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Thyroid cancer incidence rate plotted against glyphosate applied to U. The prevalence of kidney disease and resulting dialysis is increasing worldwide, and kidney disease is often associated with increased levels of celiac disease autoantibodies. A population-based study in Sweden involving nearly 30, people with diagnosed celiac disease determined that there was nearly a three-fold increased risk for kidney failure in this population group Welander et al.

Inflammation plays a crucial role in kidney disease progression Tonelli et al. Chronic kidney disease develops as a consequence of assaults on the kidney from inflammatory agents, brought on by the induction of pro-inflammatory cytokines and chemokines in the kidney. The toxic phenol p-Cresol sulfate, as well as indoxyl sulfate, a molecule that is chemically similar to p-Cresol, have been shown to induce activation of many of these cytokines and chemokines Sun et al.

The aromatic amino acid tryptophan contains an indole ring, and therefore disruption of tryptophan synthesis might be expected to generate indole as a by-product.

1 Introduction

Indeed, glyphosate has been shown to induce a significant increase in the production of indoleacetic acid in yellow nutsedge plants Caal et al. Indole is produced by coliform microorganisms such as E.

Glyphosate induces a switch in E. Besides, E. Feeding indole to rats deprived of sulfur metabolites leads to macrocytic anemia Roe, Indole acetic acid inhibits the growth of cobalamin-dependent microorganisms, which then causes macrocytic pernicious anemia in the host due to cobalamin deficiency Drexler, Experiments on exposure of mouse fetuses to indoleacetic acid have shown that it dramatically induces microcephaly in developing fetuses exposed at critical times in development Furukawa et al.

A case study found celiac disease associated with microcephaly and developmental delay in a month-old girl Bostwick et al. A gluten-free diet restored head growth.

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The authors suggested that poor head growth might precede other manifestations of celiac disease in infants. A study on plants demonstrated a concentration gradient of indoleacetic acid in the plant embryo, similar to the gradient in retinoic acid that controls fetal development in mammals Uggla et al. This alternative may be another way in which glyphosate would promote microcephaly.

Thus, solely through its effect on indole production and indole catabolism in gut bacteria, chronic glyphosate exposure would be expected to lead to cobalamin deficiency, pernicious anemia, microcephaly in a fetus during pregnancy, and kidney failure. The damaged villi associated with celiac disease are impaired in their ability to absorb a number of important nutrients, including vitamins B6, B12 cobalamin and folate, as well as iron, calcium and vitamins D and K Hallert et al.

Thus, long-term celiac disease leads to major deficiencies in these micronutrients. Cobalamin deficiency has been well addressed previously. We have also already mentioned the chelation of trace minerals by phytates and by glyphosate. However, other factors may be at play as well, as discussed here. Glyphosate disrupts the synthesis of tryptophan and tyrosine in plants and in gut bacteria, due to its interference with the shikimate pathway Lu et al. Glyphosate also depletes methionine in plants and microbes. The authors suggested a metabolic disturbance in tryptophan synthesis rather than impaired absorption, as other similar amino acids were not deficient in the serum.

Dyspepsia, a clinical symptom of celiac disease, is likely mediated by excess serotonin synthesis following ingested tryptophan-containing foods Manocha et al. Serotonin 5-hydroxytryptamine or 5-HT is produced by enterochromaffin EC cells in the gut and is an important signaling molecule for the enteric mucosa Kim et al. EC cells are the most numerous neuroendocrine cell type in the intestinal lumen, and they regulate gut secretion, motility, pain and nausea by activating primary afferent pathways in the nervous system Chin et al.

Serotonin plays an important role in activating the immune response and inflammation in the gut, and also induces nausea and diarrhea when it is overexpressed. Anaerobic bacteria in the colon convert sugars into short-chain fatty acids, which can stimulate 5-HT release from EC cells Fukumoto et al. This is likely an important source of fats to the body in the case of a low-fat diet induced by impaired fatty acid metabolism due to insufficient bile acids.