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Difference between revisions of "Choline"

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This draft has been assigned to [[User:Bethany.Chester]] and will be moved to the main namespace when completed.
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== Fact Sheet ==
  
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<--
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=== Summary ===
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* There appear to be no studies showing that those on a vegan diet are more prone to the risks associated with choline deficiency than those not on a vegan diet. There is evidence, shown below, that vegan diets are protective against risks associated with excess choline.
  
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see [[Help:Writing Fact Sheets]]  and  the articles in [[Fact Sheets Listing]]
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=== Context ===
  
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Note that we want only enough information to convincingly support the assertion and counter inaccurate information. When making a point, it is important to find those sources that will result in the most convincing arguments, and to summarize findings in the most convincing manner, all without misrepresenting or exaggerating those sources.  
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* Choline is an essential nutrient, important for brain health and a number of other physiological functions.<ref>Zeisel, Steven H., and Kerry-Ann da Costa. “Choline: An Essential Nutrient for Public Health.” Nutrition Reviews 67, no. 11 (November 2009): 615–23. Accessed January 23, 2020. https://doi.org/10.1111/j.1753-4887.2009.00246.x.</ref> It is sometimes referred to as a form of vitamin B4, but B4 is no longer considered a vitamin.
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* Although choline is readily available in plant foods.<ref name=":0">Patterson, Kristine Y. et al. “USDA Database for the Choline Content of Common Foods.” USDA, January 2008. Accessed January 21, 2020. https://data.nal.usda.gov/system/files/Choln02.pdf.</ref>, the fact that choline is most highly concentrated in animal-derived foods such as eggs and meat<ref name="nih">“Office of Dietary Supplements - Choline.” Accessed January 20, 2020. https://ods.od.nih.gov/factsheets/Choline-HealthProfessional/.</ref> has led to claims that vegans are at risk of becoming deficient in choline.
  
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Places to start for research:
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=== Evidence ===
  
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* https://veganhealth.org/choline/
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* A study in the New England Journal of Medicine recommends a high-fiber or meatless diet to avoid excess choline, which can increase the likelihood of stroke, heart disease, and mortality.<ref name=":1">Tang, W.H. Wilson, Zeneng Wang, Bruce S. Levison, Robert A. Koeth, Earl B. Britt, Xiaoming Fu, Yuping Wu, and Stanley L. Hazen. “Intestinal Microbial Metabolism of Phosphatidylcholine and Cardiovascular Risk.” New England Journal of Medicine 368, no. 17 (April 25, 2013): 1575–84. Accessed January 20, 2020. https://doi.org/10.1056/NEJMoa1109400.</ref>
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* Another study found that vegans and vegetarians are protected from the risk of heart disease that accrues to high choline intake.<ref>Zhu, Weifei, Zeneng Wang, W. H. Wilson Tang, and Stanley L. Hazen. “Gut Microbe-Generated Trimethylamine N -Oxide From Dietary Choline Is Prothrombotic in Subjects.” Circulation 135, no. 17 (April 25, 2017): 1671–73. Accessed January 20, 2020. https://doi.org/10.1161/CIRCULATIONAHA.116.025338.</ref>
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* https://www.pcrm.org/news/blog/clearing-choline-confusion
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* Other research shows that since vegans have different gut flora to omnivores, they produce very little TMAO,<ref>Koeth, Robert A., Zeneng Wang, Bruce S. Levison, Jennifer A. Buffa, Elin Org, Brendan T. Sheehy, Earl B. Britt, et al. “Intestinal Microbiota Metabolism of l -Carnitine, a Nutrient in Red Meat, Promotes Atherosclerosis.” Nature Medicine 19, no. 5 (May 2013): 576–85. Accessed January 21, 2020. https://doi.org/10.1038/nm.3145.</ref> a byproduct of choline which is linked to chronic kidney disease disease,<ref>Moraes, Cristiane, Denis Fouque, Ana Claudia F. Amaral, and Denise Mafra. “Trimethylamine N-Oxide From Gut Microbiota in Chronic Kidney Disease Patients: Focus on Diet.” Journal of Renal Nutrition 25, no. 6 (November 2015): 459–65. Accessed January 20, 2020. https://doi.org/10.1053/j.jrn.2015.06.004.</ref><ref>Tang, W.H. Wilson, Zeneng Wang, David J. Kennedy, Yuping Wu, Jennifer A. Buffa, Brendan Agatisa-Boyle, Xinmin S. Li, Bruce S. Levison, and Stanley L. Hazen. “Gut Microbiota-Dependent Trimethylamine N -Oxide (TMAO) Pathway Contributes to Both Development of Renal Insufficiency and Mortality Risk in Chronic Kidney Disease.” Circulation Research 116, no. 3 (January 30, 2015): 448–55. Accessed January 20, 2020. https://doi.org/10.1161/CIRCRESAHA.116.305360.
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</ref> stroke, and heart disease.<ref name=":1" />
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* https://nutritionfacts.org/?s=choline
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* Researchers say that choline may be responsible for the increased risk of prostrate cancer associated with egg consumption.<ref>Richman, Erin L, Stacey A Kenfield, Meir J Stampfer, Edward L Giovannucci, Steven H Zeisel, Walter C Willett, and June M Chan. “Choline Intake and Risk of Lethal Prostate Cancer: Incidence and Survival.” The American Journal of Clinical Nutrition 96, no. 4 (October 1, 2012): 855–63. Accessed January 20, 2020. https://doi.org/10.3945/ajcn.112.039784.</ref><ref>Richman, E. L., S. A. Kenfield, M. J. Stampfer, E. L. Giovannucci, and J. M. Chan. “Egg, Red Meat, and Poultry Intake and Risk of Lethal Prostate Cancer in the Prostate-Specific Antigen-Era: Incidence and Survival.” Cancer Prevention Research 4, no. 12 (December 1, 2011): 2110–21. Accessed January 20, 2020. https://doi.org/10.1158/1940-6207.CAPR-11-0354.</ref><ref>Richman, Erin L, Meir J Stampfer, Alan Paciorek, Jeanette M Broering, Peter R Carroll, and June M Chan. “Intakes of Meat, Fish, Poultry, and Eggs and Risk of Prostate Cancer Progression.” The American Journal of Clinical Nutrition 91, no. 3 (March 1, 2010): 712–21. Accessed January 20, 2020. https://doi.org/10.3945/ajcn.2009.28474.</ref>
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* One of the most common symptoms of choline deficiency is the development of non-alcoholic fatty liver disease (NAFLD).<ref>Corbin, Karen, and Steven Zeisel. “Choline Metabolism Provides Novel Insights into Nonalcoholic Fatty Liver Disease and Its Progression.” Current Opinion in Gastroenterology 28, no. 2 (March 2012): 159–65. Accessed January 21, 2020. https://doi.org/10.1097/MOG.0b013e32834e7b4b.</ref> However, plant-based and vegetarian diets have been shown to reduce the risk of NAFLD, making it unlikely that these diets are deficient in choline.<ref>Chiu, Tina H., Ming-Nan Lin, Wen-Harn Pan, Yen-Ching Chen, and Chin-Lon Lin. “Vegetarian Diet, Food Substitution, and Nonalcoholic Fatty Liver.” Ci Ji Yi Xue Za Zhi = Tzu-Chi Medical Journal 30, no. 2 (June 2018): 102–9. Accessed January 21, 2020. https://doi.org/10.4103/tcmj.tcmj_109_17.</ref><ref>Mazidi, Mohsen, and Andre Pascal Kengne. “Higher Adherence to Plant-Based Diets Are Associated with Lower Likelihood of Fatty Liver.” Clinical Nutrition 38, no. 4 (August 2019): 1672–77. Accessed January 21, 2020. https://doi.org/10.1016/j.clnu.2018.08.010.</ref>
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Is there research showing that vegans are generally not deficient in choline, or that non-vegans are?
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* The Physicians' Committee for Responsible Medicine recommends choosing plant-based sources of choline because animal sources (such as eggs, which are high in choline and cholesterol) are often also very high in saturated fat, significantly increasing the risk of heart disease<ref>Zhong, Victor W., Linda Van Horn, Marilyn C. Cornelis, John T. Wilkins, Hongyan Ning, Mercedes R. Carnethon, Philip Greenland, et al. “Associations of Dietary Cholesterol or Egg Consumption With Incident Cardiovascular Disease and Mortality.” JAMA 321, no. 11 (March 19, 2019): 1081. Accessed January 21, 2020. https://doi.org/10.1001/jama.2019.1572.</ref> and increasing the risk of dementia.<ref>Physicians Committee for Responsible Medicine. “Clearing Up Choline Confusion.” Accessed January 20, 2020. https://www.pcrm.org/news/blog/clearing-choline-confusion.</ref> Also, the USDA's Dietary Guidelines recommend eating "as little dietary cholesterol as possible."<ref>“A Closer Look Inside Healthy Eating Patterns - 2015-2020 Dietary Guidelines | Health.Gov.” Accessed January 22, 2020. https://health.gov/dietaryguidelines/2015/guidelines/chapter-1/a-closer-look-inside-healthy-eating-patterns/.
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</ref>
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== Fact Sheet ==
 
  
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=== Assertion ===
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=== Conflicting Claims ===
  
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* This fact sheet supports the assertion that choline from animal sources is not necessary and may be harmful to health.
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* A 2019 article published in the journal BMJ (British Medical Journal) generated a flurry of media buzz, raising concerns about choline deficiency in those eating plant-based diets. In the media, the article was referred to as a study, but in reality it is an editorial and the author did not carry out any of her own research. Moreover, she has ties to the egg and meat industries and so the article cannot be considered unbiased.<ref name="bmj">Derbyshire, Emma. “Could We Be Overlooking a Potential Choline Crisis in the United Kingdom?” BMJ Nutrition, Prevention & Health 2, no. 2 (December 1, 2019): 86–89. Accessed January 20, 2020. https://doi.org/10.1136/bmjnph-2019-000037.</ref>
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* Studies carried out in 2004 and 2009 raised concerns that expectant mothers on a vegan diet, with its typically lower dietary choline, could increase the risk of babies being born with neural tube defects.<ref>Shaw, G. M., S. L. Carmichael, W. Yang, S. Selvin, and D. M. Schaffer. “Periconceptional Dietary Intake of Choline and Betaine and Neural Tube Defects in Offspring.” American Journal of Epidemiology 160, no. 2 (July 15, 2004): 102–9. Accessed January 21, 2020. https://doi.org/10.1093/aje/kwh187.</ref><ref>Shaw, Gary M., Richard H. Finnell, Henk J. Blom, Suzan L. Carmichael, Stein Emil Vollset, Wei Yang, and Per M. Ueland. “Choline and Risk of Neural Tube Defects in a Folate-Fortified Population:” Epidemiology 20, no. 5 (September 2009): 714–19. Accessed January 21, 2020. https://doi.org/10.1097/EDE.0b013e3181ac9fe7.</ref> However, more recent research does not support this claim.<ref>Mills, James L, Ruzong Fan, Lawrence C Brody, Aiyi Liu, Per M Ueland, Yifan Wang, Peadar N Kirke, Barry Shane, and Anne M Molloy. “Maternal Choline Concentrations during Pregnancy and Choline-Related Genetic Variants as Risk Factors for Neural Tube Defects.” The American Journal of Clinical Nutrition 100, no. 4 (October 1, 2014): 1069–74. Accessed January 21, 2020. https://doi.org/10.3945/ajcn.113.079319.</ref><ref>Carmichael, Suzan L., Wei Yang, and Gary M. Shaw. “Periconceptional Nutrient Intakes and Risks of Neural Tube Defects in California.” Birth Defects Research Part A: Clinical and Molecular Teratology 88, no. 8 (2010): 670–78. Accessed January 21, 2020. https://doi.org/10.1002/bdra.20675.</ref><ref>Chandler, Angela L., Charlotte A. Hobbs, Bridget S. Mosley, Robert J. Berry, Mark A. Canfield, Yan Ping Qi, Anna Maria Siega‐Riz, and Gary M. Shaw. “Neural Tube Defects and Maternal Intake of Micronutrients Related to One-Carbon Metabolism or Antioxidant Activity.” Birth Defects Research Part A: Clinical and Molecular Teratology 94, no. 11 (2012): 864–74. Accessed January 21, 2020. https://doi.org/10.1002/bdra.23068.</ref> Vegan diets may actually decrease the risk of neural tube defects because up to 70 percent of these defects are linked to inadequate folic acid intake,<ref>“Neural Tube Defects (NTDs) | Duke Molecular Physiology Institute.” Accessed January 21, 2020. https://dmpi.duke.edu/neural-tube-defects-ntds.</ref><ref>Berry, Robert J., Zhu Li, J. David Erickson, Song Li, Cynthia A. Moore, Hong Wang, Joseph Mulinare, et al. “Prevention of Neural-Tube Defects with Folic Acid in China.” New England Journal of Medicine 341, no. 20 (November 11, 1999): 1485–90. Accessed January 21, 2020. https://doi.org/10.1056/NEJM199911113412001.</ref><ref>Green, Nancy S. “Folic Acid Supplementation and Prevention of Birth Defects.” The Journal of Nutrition 132, no. 8 (August 1, 2002): 2356S-2360S. Accessed January 21, 2020. https://doi.org/10.1093/jn/132.8.2356S.</ref> and those eating plant-based or vegetarian diets typically have higher folate levels than omnivores.<ref>Majchrzak, D., I. Singer, M. Männer, P. Rust, D. Genser, K.-H. Wagner, and I. Elmadfa. “B-Vitamin Status and Concentrations of Homocysteine in Austrian Omnivores, Vegetarians and Vegans.” Annals of Nutrition and Metabolism 50, no. 6 (2006): 485–91. Accessed January 21, 2020. https://doi.org/10.1159/000095828.</ref><ref>Koebnick, Corinna, Ulrike A. Heins, Ingrid Hoffmann, Pieter C. Dagnelie, and Claus Leitzmann. “Folate Status during Pregnancy in Women Is Improved by Long-Term High Vegetable Intake Compared with the Average Western Diet.” The Journal of Nutrition 131, no. 3 (April 1, 2001): 733–39. Accessed January 21, 2020. https://doi.org/10.1093/jn/131.3.733.</ref>
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* Contrary to scare tactics using unsupported claims of inadequate brain development by those on a vegan diet, Tom Sanders, Professor Emeritus of Nutrition and Dietetics at King's College London, has stated that "There is no justification for suggesting that plant-based diets risk damaging brain development...My own research on vegans and those of others in Europe and USA find the growth and development of vegans and vegetarians is normal."<ref name=":2">Gilliver, Liam. “Rachel Riley Defends Plant-Based Diet Amid Concerns Around Choline.” Vegan News, Plant Based Living, Food, Health & more. Accessed January 21, 2020. https://www.plantbasednews.org/news/rachel-riley-defends-plant-based-diet.</ref>
  
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=== Context ===
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=== Sources of Choline ===
  
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* In general, the nutrient choline is most highly concentrated in animal-derived foods such as eggs and meat.<ref name="nih">
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* A USDA database shows that choline is abundant in a variety of plant foods.<ref name=":0" /> Nutrition Professor Tom Sanders (mentioned above) confirms this and points out that that the body can make some of its own choline.<ref name=":2" />
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“Office of Dietary Supplements - Choline.” Accessed January 20, 2020. https://ods.od.nih.gov/factsheets/Choline-HealthProfessional/.</ref> This has led to claims that vegans are at risk of becoming deficient in choline.
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* The National Institutes for Health (NIH) state that cruciferous vegetables and some beans are "rich in choline." They show that soybeans contain more choline than ground beef, chicken breast, or cod, while mushrooms and potatoes contain more than tuna and dairy products. Quinoa, wheat germ, and kidney beans are also good sources.<ref name="nih" />
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* A 2019 editorial published in the journal BMJ made headlines by expressing concern about choline deficiency in those eating plant-based diets.<ref name="bmj">Derbyshire, Emma. “Could We Be Overlooking a Potential Choline Crisis in the United Kingdom?” BMJ Nutrition, Prevention & Health 2, no. 2 (December 1, 2019): 86–89. Accessed January 20, 2020. https://doi.org/10.1136/bmjnph-2019-000037.</ref>
 
  
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=== Research ===
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=== Dietary Guidelines ===
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* In the USA, recommendations for the Adequate Intake (AI) of choline are based on very limited data (one study done on adult men). The AI for women and other age groups has been extrapolated from this data and so may not be accurate. Additionally, the original study was limited as it only compared intakes of 500 mg/day and 50 mg/day, finding that the latter caused deficiency. Intermediary values were not considered, so this recommended AI may be higher than true requirements.<ref>Folate, Institute of Medicine (US) Standing Committee on the Scientific Evaluation of Dietary Reference Intakes and its Panel on, Other B. Vitamins, and And Choline. Choline. National Academies Press (US), 1998. Accessed January 21, 2020. https://www.ncbi.nlm.nih.gov/books/NBK114308/.</ref><ref>Zeisel, S. H., K. A. Da Costa, P. D. Franklin, E. A. Alexander, J. T. Lamont, N. F. Sheard, and A. Beiser. “Choline, an Essential Nutrient for Humans.” FASEB Journal: Official Publication of the Federation of American Societies for Experimental Biology 5, no. 7 (April 1991): 2093–98.</ref>
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* Despite eating a diet high in animal products,<ref>Bloomfield, Hanna E., Robert Kane, Eva Koeller, Nancy Greer, Roderick MacDonald, and Timothy Wilt. ''Benefits and Harms of the Mediterranean Diet Compared to Other Diets''. VA Evidence-Based Synthesis Program Reports. Washington (DC): Department of Veterans Affairs (US), 2015. <nowiki>http://www.ncbi.nlm.nih.gov/books/NBK379574/</nowiki>.</ref> most people in the USA do not achieve the Adequate Intake (AI) for choline, yet the actual rates of choline deficiency are very low.<ref>Bloomfield, Hanna E., Robert Kane, Eva Koeller, Nancy Greer, Roderick MacDonald, and Timothy Wilt. ''Benefits and Harms of the Mediterranean Diet Compared to Other Diets''. VA Evidence-Based Synthesis Program Reports. Washington (DC): Department of Veterans Affairs (US), 2015. <nowiki>http://www.ncbi.nlm.nih.gov/books/NBK379574/</nowiki>.</ref>. This suggests the AI is not accurate.<ref name="nih" />
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* The European Food Safety Authority sets the AI for adults at a lower figure of 400 mg/day. This figure is based on the average intake of healthy populations, which is arguably a more accurate estimate than the previously described study. (Note that the AI for pregnant and breastfeeding women is higher.)<ref>“Dietary Reference Values for Choline.” EFSA Journal 14, no. 8 (2016): e04484. Accessed January 22, 2020. https://doi.org/10.2903/j.efsa.2016.4484.</ref>
 
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* Choline produces a byproduct called TMAO in the body. A study in the New England Journal of Medicine found that TMAO increases the likelihood of stroke, heart disease, and even death. The study recommends that excess choline intake should be avoided and suggests that a high-fiber or vegetarian diet is an effective way to do this.<ref>Tang, W.H. Wilson, Zeneng Wang, Bruce S. Levison, Robert A. Koeth, Earl B. Britt, Xiaoming Fu, Yuping Wu, and Stanley L. Hazen. “Intestinal Microbial Metabolism of Phosphatidylcholine and Cardiovascular Risk.” New England Journal of Medicine 368, no. 17 (April 25, 2013): 1575–84. Accessed January 20, 2020. https://doi.org/10.1056/NEJMoa1109400.</ref>
 
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* Another study also found that high choline intake is linked to heart disease, but noted that vegans and vegetarians are protected from its effects.<ref>Zhu, Weifei, Zeneng Wang, W. H. Wilson Tang, and Stanley L. Hazen. “Gut Microbe-Generated Trimethylamine N -Oxide From Dietary Choline Is Prothrombotic in Subjects.” Circulation 135, no. 17 (April 25, 2017): 1671–73. Accessed January 20, 2020. https://doi.org/10.1161/CIRCULATIONAHA.116.025338.</ref>
 
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* Other research has supported this by showing that since vegans have different gut flora to omnivores, they produce very little TMAO.<ref>Koeth, Robert A., Zeneng Wang, Bruce S. Levison, Jennifer A. Buffa, Elin Org, Brendan T. Sheehy, Earl B. Britt, et al. “Intestinal Microbiota Metabolism of l -Carnitine, a Nutrient in Red Meat, Promotes Atherosclerosis.” Nature Medicine 19, no. 5 (May 2013): 576–85. Accessed January 21, 2020. https://doi.org/10.1038/nm.3145.</ref>
 
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* Egg consumption has been linked to an increased risk of prostate cancer, and researchers suggest that choline may be the culprit.<ref>Richman, Erin L, Stacey A Kenfield, Meir J Stampfer, Edward L Giovannucci, Steven H Zeisel, Walter C Willett, and June M Chan. “Choline Intake and Risk of Lethal Prostate Cancer: Incidence and Survival.” The American Journal of Clinical Nutrition 96, no. 4 (October 1, 2012): 855–63. Accessed January 20, 2020. https://doi.org/10.3945/ajcn.112.039784.</ref><ref>Richman, E. L., S. A. Kenfield, M. J. Stampfer, E. L. Giovannucci, and J. M. Chan. “Egg, Red Meat, and Poultry Intake and Risk of Lethal Prostate Cancer in the Prostate-Specific Antigen-Era: Incidence and Survival.” Cancer Prevention Research 4, no. 12 (December 1, 2011): 2110–21. Accessed January 20, 2020. https://doi.org/10.1158/1940-6207.CAPR-11-0354.</ref><ref>Richman, Erin L, Meir J Stampfer, Alan Paciorek, Jeanette M Broering, Peter R Carroll, and June M Chan. “Intakes of Meat, Fish, Poultry, and Eggs and Risk of Prostate Cancer Progression.” The American Journal of Clinical Nutrition 91, no. 3 (March 1, 2010): 712–21. Accessed January 20, 2020. https://doi.org/10.3945/ajcn.2009.28474.</ref>
 
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* TMAO has also been linked to chronic kidney disease.<ref>Moraes, Cristiane, Denis Fouque, Ana Claudia F. Amaral, and Denise Mafra. “Trimethylamine N-Oxide From Gut Microbiota in Chronic Kidney Disease Patients: Focus on Diet.” Journal of Renal Nutrition 25, no. 6 (November 2015): 459–65. Accessed January 20, 2020. https://doi.org/10.1053/j.jrn.2015.06.004.</ref><ref>
 
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Tang, W.H. Wilson, Zeneng Wang, David J. Kennedy, Yuping Wu, Jennifer A. Buffa, Brendan Agatisa-Boyle, Xinmin S. Li, Bruce S. Levison, and Stanley L. Hazen. “Gut Microbiota-Dependent Trimethylamine N -Oxide (TMAO) Pathway Contributes to Both Development of Renal Insufficiency and Mortality Risk in Chronic Kidney Disease.” Circulation Research 116, no. 3 (January 30, 2015): 448–55. Accessed January 20, 2020. https://doi.org/10.1161/CIRCRESAHA.116.305360.
 
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</ref>
 
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* In some people, excess choline consumption causes a strong fishy body odor, including the breath, urine, and sweat.<ref>
 
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Rehman, H. U. “Fish Odour Syndrome.” Postgraduate Medical Journal 75, no. 886 (August 1, 1999): 451–52. Accessed January 20, 2020. https://doi.org/10.1136/pgmj.75.886.451.</ref>
 
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* The USDA has published a database of the choline content of various foods. It shows that eggs are extremely high in choline, containing about three times as much as meat and fish. However, wholegrains contain almost as much choline as meat and fish, and breakfast cereals are also a good source. Overall, fruits and vegetables are a better source than milk. The database also shows that some individual plant foods have a very high choline content, such as wheat germ, soy flour, quinoa, and peanut butter.<ref>Patterson, Kristine Y. et al. “USDA Database for the Choline Content of Common Foods.” USDA, January 2008. Accessed January 21, 2020. https://data.nal.usda.gov/system/files/Choln02.pdf.</ref>
 
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* One of the most common symptoms of choline deficiency is the development of non-alcoholic fatty liver disease (NAFLD).<ref>Corbin, Karen, and Steven Zeisel. “Choline Metabolism Provides Novel Insights into Nonalcoholic Fatty Liver Disease and Its Progression.” Current Opinion in Gastroenterology 28, no. 2 (March 2012): 159–65. Accessed January 21, 2020. https://doi.org/10.1097/MOG.0b013e32834e7b4b.</ref> However, plant-based and vegetarian diets have been shown to reduce the risk of NAFLD, making it unlikely that these diets are deficient in choline.<ref>Chiu, Tina H., Ming-Nan Lin, Wen-Harn Pan, Yen-Ching Chen, and Chin-Lon Lin. “Vegetarian Diet, Food Substitution, and Nonalcoholic Fatty Liver.” Ci Ji Yi Xue Za Zhi = Tzu-Chi Medical Journal 30, no. 2 (June 2018): 102–9. Accessed January 21, 2020. https://doi.org/10.4103/tcmj.tcmj_109_17.</ref><ref>Mazidi, Mohsen, and Andre Pascal Kengne. “Higher Adherence to Plant-Based Diets Are Associated with Lower Likelihood of Fatty Liver.” Clinical Nutrition 38, no. 4 (August 2019): 1672–77. Accessed January 21, 2020. https://doi.org/10.1016/j.clnu.2018.08.010.</ref>
 
  
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=== Conflicting Information ===
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* In the USA, recommendations for the Adequate Intake (AI) of choline are based on very limited data (one study done on adult men). The AI for women and other age groups has been extrapolated from this data and so may not be accurate. Additionally, the original study was limited as it only compared intakes of 500 mg/day and 50 mg/day, finding that the latter caused deficiency. Intermediary values were not considered, so the recommended AI may be higher than true requirements<ref>Folate, Institute of Medicine (US) Standing Committee on the Scientific Evaluation of Dietary Reference Intakes and its Panel on, Other B. Vitamins, and And Choline. Choline. National Academies Press (US), 1998. Accessed January 21, 2020. https://www.ncbi.nlm.nih.gov/books/NBK114308/.</ref><ref>Zeisel, S. H., K. A. Da Costa, P. D. Franklin, E. A. Alexander, J. T. Lamont, N. F. Sheard, and A. Beiser. “Choline, an Essential Nutrient for Humans.” FASEB Journal: Official Publication of the Federation of American Societies for Experimental Biology 5, no. 7 (April 1991): 2093–98.</ref> — especially as the body produces some of its own choline.<ref>''“Dietary Reference Intakes: The Essential Guide to Nutrient Requirements”''. Accessed January 22, 2020. <nowiki>https://doi.org/10.17226/11537</nowiki>.</ref><ref>Hollenbeck, Clarie B. “An Introduction to the Nutrition and Metabolism of Choline.” Central Nervous System Agents in Medicinal Chemistry 12, no. 2 (June 2012): 100–113. Accessed January 21, 2020. https://doi.org/10.2174/187152412800792689.</ref>
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* The European Food Safety Authority sets the AI for adults at a lower figure of 400 mg/day. This figure is based on the average intake of healthy populations, and is arguably more accurate than the study mentioned above. However, it still does not establish the minimum amount of choline required for good health.<ref>“Dietary Reference Values for Choline.” EFSA Journal 14, no. 8 (2016): e04484. Accessed January 22, 2020. https://doi.org/10.2903/j.efsa.2016.4484.</ref>
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* In 2019, an article was published in the journal BMJ claiming that those eating plant-based diets may be at risk of choline deficiency. In the media, the article was referred to as a study, but in reality it is an editorial and the author did not carry out any of her own research. Moreover, she has ties to the egg and meat industries and so the article cannot be considered unbiased.<ref name="bmj"/>
 
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* Two studies carried out in 2004 and 2009 appeared to show that low choline intake in pregnant women could increase the risk of babies being born with neural tube defects.<ref>Shaw, G. M., S. L. Carmichael, W. Yang, S. Selvin, and D. M. Schaffer. “Periconceptional Dietary Intake of Choline and Betaine and Neural Tube Defects in Offspring.” American Journal of Epidemiology 160, no. 2 (July 15, 2004): 102–9. Accessed January 21, 2020. https://doi.org/10.1093/aje/kwh187.</ref><ref>Shaw, Gary M., Richard H. Finnell, Henk J. Blom, Suzan L. Carmichael, Stein Emil Vollset, Wei Yang, and Per M. Ueland. “Choline and Risk of Neural Tube Defects in a Folate-Fortified Population:” Epidemiology 20, no. 5 (September 2009): 714–19. Accessed January 21, 2020. https://doi.org/10.1097/EDE.0b013e3181ac9fe7.</ref> However, more recent research does not support this claim.<ref>Mills, James L, Ruzong Fan, Lawrence C Brody, Aiyi Liu, Per M Ueland, Yifan Wang, Peadar N Kirke, Barry Shane, and Anne M Molloy. “Maternal Choline Concentrations during Pregnancy and Choline-Related Genetic Variants as Risk Factors for Neural Tube Defects.” The American Journal of Clinical Nutrition 100, no. 4 (October 1, 2014): 1069–74. Accessed January 21, 2020. https://doi.org/10.3945/ajcn.113.079319.</ref><ref>Carmichael, Suzan L., Wei Yang, and Gary M. Shaw. “Periconceptional Nutrient Intakes and Risks of Neural Tube Defects in California.” Birth Defects Research Part A: Clinical and Molecular Teratology 88, no. 8 (2010): 670–78. Accessed January 21, 2020. https://doi.org/10.1002/bdra.20675.</ref><ref>Chandler, Angela L., Charlotte A. Hobbs, Bridget S. Mosley, Robert J. Berry, Mark A. Canfield, Yan Ping Qi, Anna Maria Siega‐Riz, and Gary M. Shaw. “Neural Tube Defects and Maternal Intake of Micronutrients Related to One-Carbon Metabolism or Antioxidant Activity.” Birth Defects Research Part A: Clinical and Molecular Teratology 94, no. 11 (2012): 864–74. Accessed January 21, 2020. https://doi.org/10.1002/bdra.23068.</ref> In contrast, up to 70 percent of neural tube defects are linked to inadequate folic acid intake.<ref>“Neural Tube Defects (NTDs) | Duke Molecular Physiology Institute.” Accessed January 21, 2020. https://dmpi.duke.edu/neural-tube-defects-ntds.</ref><ref>Berry, Robert J., Zhu Li, J. David Erickson, Song Li, Cynthia A. Moore, Hong Wang, Joseph Mulinare, et al. “Prevention of Neural-Tube Defects with Folic Acid in China.” New England Journal of Medicine 341, no. 20 (November 11, 1999): 1485–90. https://doi.org/10.1056/NEJM199911113412001.</ref><ref>Green, Nancy S. “Folic Acid Supplementation and Prevention of Birth Defects.” The Journal of Nutrition 132, no. 8 (August 1, 2002): 2356S-2360S. Accessed January 21, 2020. https://doi.org/10.1093/jn/132.8.2356S.</ref> Those eating plant-based or vegetarian diets typically have higher folate levels than omnivores.<ref>Majchrzak, D., I. Singer, M. Männer, P. Rust, D. Genser, K.-H. Wagner, and I. Elmadfa. “B-Vitamin Status and Concentrations of Homocysteine in Austrian Omnivores, Vegetarians and Vegans.” Annals of Nutrition and Metabolism 50, no. 6 (2006): 485–91. Accessed January 21, 2020. https://doi.org/10.1159/000095828.</ref><ref>Koebnick, Corinna, Ulrike A. Heins, Ingrid Hoffmann, Pieter C. Dagnelie, and Claus Leitzmann. “Folate Status during Pregnancy in Women Is Improved by Long-Term High Vegetable Intake Compared with the Average Western Diet.” The Journal of Nutrition 131, no. 3 (April 1, 2001): 733–39. Accessed January 21, 2020. https://doi.org/10.1093/jn/131.3.733.</ref>
 
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=== Other Sources ===
 
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* The National Institutes for Health (NIH) state that cruciferous vegetables and some beans are "rich in choline." They show that soybeans contain more choline than ground beef, chicken breast, or cod, while mushrooms and potatoes contain more than tuna and dairy products. Quinoa, wheat germ, and kidney beans are also good sources.<ref name="nih"/>
 
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* The Physicians' Committee for Responsible Medicine recommends choosing plant-based sources of choline because animal sources (such as eggs) are often very high in saturated fat. It points out that high saturated fat consumption increases the risk of heart disease and dementia.<ref>Physicians Committee for Responsible Medicine. “Clearing Up Choline Confusion.” Accessed January 20, 2020. https://www.pcrm.org/news/blog/clearing-choline-confusion.</ref>
 
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* Tom Sanders, Professor Emeritus of Nutrition and Dietetics at King's College London, has stated that "There is no justification for suggesting that plant-based diets risk damaging brain development...My own research on vegans and those of others in Europe and USA find the growth and development of vegans and vegetarians is normal." He points out that the body can make some of its own choline and that the nutrient is "abundant" in several plant-based foods.<ref>Gilliver, Liam. “Rachel Riley Defends Plant-Based Diet Amid Concerns Around Choline.” Vegan News, Plant Based Living, Food, Health & more. Accessed January 21, 2020. https://www.plantbasednews.org/news/rachel-riley-defends-plant-based-diet.</ref>
 
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* According to the NIH, most people in the USA do not achieve the adequate intake for choline established by the Food and Nutrition Board of the Institute of Medicine. This is despite eating a diet high in animal products. However, actual rates of choline deficiency are very low,<ref name="nih"/> suggesting that the AI may not be accurate. This is likely to be because the body produces some of its own choline,<ref>Hollenbeck, Clarie B. “An Introduction to the Nutrition and Metabolism of Choline.” Central Nervous System Agents in Medicinal Chemistry 12, no. 2 (June 2012): 100–113. Accessed January 21, 2020. https://doi.org/10.2174/187152412800792689.</ref> which may not have been sufficiently accounted for.
 
  
 
== See Also ==
 
== See Also ==
 +
* [https://veganhealth.org/choline/ Choline - Vegan Health] (Article at by Jack Norris at vegan health.org)
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* [https://www.pcrm.org/news/blog/clearing-choline-confusion Clearing Up Choline Confusion] (Article at PCRM.org)
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* [https://nutritionfacts.org/?s=choline NutritionFacts.org videos on choline.]
  
 
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Latest revision as of 08:05, 4 February 2020

Fact Sheet

Summary

  • There appear to be no studies showing that those on a vegan diet are more prone to the risks associated with choline deficiency than those not on a vegan diet. There is evidence, shown below, that vegan diets are protective against risks associated with excess choline.

Context

  • Choline is an essential nutrient, important for brain health and a number of other physiological functions.[1] It is sometimes referred to as a form of vitamin B4, but B4 is no longer considered a vitamin.
  • Although choline is readily available in plant foods.[2], the fact that choline is most highly concentrated in animal-derived foods such as eggs and meat[3] has led to claims that vegans are at risk of becoming deficient in choline.

Evidence

  • A study in the New England Journal of Medicine recommends a high-fiber or meatless diet to avoid excess choline, which can increase the likelihood of stroke, heart disease, and mortality.[4]
  • Another study found that vegans and vegetarians are protected from the risk of heart disease that accrues to high choline intake.[5]
  • Other research shows that since vegans have different gut flora to omnivores, they produce very little TMAO,[6] a byproduct of choline which is linked to chronic kidney disease disease,[7][8] stroke, and heart disease.[4]
  • Researchers say that choline may be responsible for the increased risk of prostrate cancer associated with egg consumption.[9][10][11]
  • One of the most common symptoms of choline deficiency is the development of non-alcoholic fatty liver disease (NAFLD).[12] However, plant-based and vegetarian diets have been shown to reduce the risk of NAFLD, making it unlikely that these diets are deficient in choline.[13][14]
  • The Physicians' Committee for Responsible Medicine recommends choosing plant-based sources of choline because animal sources (such as eggs, which are high in choline and cholesterol) are often also very high in saturated fat, significantly increasing the risk of heart disease[15] and increasing the risk of dementia.[16] Also, the USDA's Dietary Guidelines recommend eating "as little dietary cholesterol as possible."[17]

Conflicting Claims

  • A 2019 article published in the journal BMJ (British Medical Journal) generated a flurry of media buzz, raising concerns about choline deficiency in those eating plant-based diets. In the media, the article was referred to as a study, but in reality it is an editorial and the author did not carry out any of her own research. Moreover, she has ties to the egg and meat industries and so the article cannot be considered unbiased.[18]
  • Studies carried out in 2004 and 2009 raised concerns that expectant mothers on a vegan diet, with its typically lower dietary choline, could increase the risk of babies being born with neural tube defects.[19][20] However, more recent research does not support this claim.[21][22][23] Vegan diets may actually decrease the risk of neural tube defects because up to 70 percent of these defects are linked to inadequate folic acid intake,[24][25][26] and those eating plant-based or vegetarian diets typically have higher folate levels than omnivores.[27][28]
  • Contrary to scare tactics using unsupported claims of inadequate brain development by those on a vegan diet, Tom Sanders, Professor Emeritus of Nutrition and Dietetics at King's College London, has stated that "There is no justification for suggesting that plant-based diets risk damaging brain development...My own research on vegans and those of others in Europe and USA find the growth and development of vegans and vegetarians is normal."[29]

Sources of Choline

  • A USDA database shows that choline is abundant in a variety of plant foods.[2] Nutrition Professor Tom Sanders (mentioned above) confirms this and points out that that the body can make some of its own choline.[29]
  • The National Institutes for Health (NIH) state that cruciferous vegetables and some beans are "rich in choline." They show that soybeans contain more choline than ground beef, chicken breast, or cod, while mushrooms and potatoes contain more than tuna and dairy products. Quinoa, wheat germ, and kidney beans are also good sources.[3]

Dietary Guidelines

  • Despite eating a diet high in animal products,[30] most people in the USA do not achieve the Adequate Intake (AI) for choline, yet the actual rates of choline deficiency are very low.[31]. This suggests the AI is not accurate.[3]
  • In the USA, recommendations for the Adequate Intake (AI) of choline are based on very limited data (one study done on adult men). The AI for women and other age groups has been extrapolated from this data and so may not be accurate. Additionally, the original study was limited as it only compared intakes of 500 mg/day and 50 mg/day, finding that the latter caused deficiency. Intermediary values were not considered, so the recommended AI may be higher than true requirements[32][33] — especially as the body produces some of its own choline.[34][35]
  • The European Food Safety Authority sets the AI for adults at a lower figure of 400 mg/day. This figure is based on the average intake of healthy populations, and is arguably more accurate than the study mentioned above. However, it still does not establish the minimum amount of choline required for good health.[36]

See Also

Plain Text

Footnotes

  1. ↑ Zeisel, Steven H., and Kerry-Ann da Costa. “Choline: An Essential Nutrient for Public Health.” Nutrition Reviews 67, no. 11 (November 2009): 615–23. Accessed January 23, 2020. https://doi.org/10.1111/j.1753-4887.2009.00246.x.
  2. ↑ 2.0 2.1 Patterson, Kristine Y. et al. “USDA Database for the Choline Content of Common Foods.” USDA, January 2008. Accessed January 21, 2020. https://data.nal.usda.gov/system/files/Choln02.pdf.
  3. ↑ 3.0 3.1 3.2 “Office of Dietary Supplements - Choline.” Accessed January 20, 2020. https://ods.od.nih.gov/factsheets/Choline-HealthProfessional/.
  4. ↑ 4.0 4.1 Tang, W.H. Wilson, Zeneng Wang, Bruce S. Levison, Robert A. Koeth, Earl B. Britt, Xiaoming Fu, Yuping Wu, and Stanley L. Hazen. “Intestinal Microbial Metabolism of Phosphatidylcholine and Cardiovascular Risk.” New England Journal of Medicine 368, no. 17 (April 25, 2013): 1575–84. Accessed January 20, 2020. https://doi.org/10.1056/NEJMoa1109400.
  5. ↑ Zhu, Weifei, Zeneng Wang, W. H. Wilson Tang, and Stanley L. Hazen. “Gut Microbe-Generated Trimethylamine N -Oxide From Dietary Choline Is Prothrombotic in Subjects.” Circulation 135, no. 17 (April 25, 2017): 1671–73. Accessed January 20, 2020. https://doi.org/10.1161/CIRCULATIONAHA.116.025338.
  6. ↑ Koeth, Robert A., Zeneng Wang, Bruce S. Levison, Jennifer A. Buffa, Elin Org, Brendan T. Sheehy, Earl B. Britt, et al. “Intestinal Microbiota Metabolism of l -Carnitine, a Nutrient in Red Meat, Promotes Atherosclerosis.” Nature Medicine 19, no. 5 (May 2013): 576–85. Accessed January 21, 2020. https://doi.org/10.1038/nm.3145.
  7. ↑ Moraes, Cristiane, Denis Fouque, Ana Claudia F. Amaral, and Denise Mafra. “Trimethylamine N-Oxide From Gut Microbiota in Chronic Kidney Disease Patients: Focus on Diet.” Journal of Renal Nutrition 25, no. 6 (November 2015): 459–65. Accessed January 20, 2020. https://doi.org/10.1053/j.jrn.2015.06.004.
  8. ↑ Tang, W.H. Wilson, Zeneng Wang, David J. Kennedy, Yuping Wu, Jennifer A. Buffa, Brendan Agatisa-Boyle, Xinmin S. Li, Bruce S. Levison, and Stanley L. Hazen. “Gut Microbiota-Dependent Trimethylamine N -Oxide (TMAO) Pathway Contributes to Both Development of Renal Insufficiency and Mortality Risk in Chronic Kidney Disease.” Circulation Research 116, no. 3 (January 30, 2015): 448–55. Accessed January 20, 2020. https://doi.org/10.1161/CIRCRESAHA.116.305360.
  9. ↑ Richman, Erin L, Stacey A Kenfield, Meir J Stampfer, Edward L Giovannucci, Steven H Zeisel, Walter C Willett, and June M Chan. “Choline Intake and Risk of Lethal Prostate Cancer: Incidence and Survival.” The American Journal of Clinical Nutrition 96, no. 4 (October 1, 2012): 855–63. Accessed January 20, 2020. https://doi.org/10.3945/ajcn.112.039784.
  10. ↑ Richman, E. L., S. A. Kenfield, M. J. Stampfer, E. L. Giovannucci, and J. M. Chan. “Egg, Red Meat, and Poultry Intake and Risk of Lethal Prostate Cancer in the Prostate-Specific Antigen-Era: Incidence and Survival.” Cancer Prevention Research 4, no. 12 (December 1, 2011): 2110–21. Accessed January 20, 2020. https://doi.org/10.1158/1940-6207.CAPR-11-0354.
  11. ↑ Richman, Erin L, Meir J Stampfer, Alan Paciorek, Jeanette M Broering, Peter R Carroll, and June M Chan. “Intakes of Meat, Fish, Poultry, and Eggs and Risk of Prostate Cancer Progression.” The American Journal of Clinical Nutrition 91, no. 3 (March 1, 2010): 712–21. Accessed January 20, 2020. https://doi.org/10.3945/ajcn.2009.28474.
  12. ↑ Corbin, Karen, and Steven Zeisel. “Choline Metabolism Provides Novel Insights into Nonalcoholic Fatty Liver Disease and Its Progression.” Current Opinion in Gastroenterology 28, no. 2 (March 2012): 159–65. Accessed January 21, 2020. https://doi.org/10.1097/MOG.0b013e32834e7b4b.
  13. ↑ Chiu, Tina H., Ming-Nan Lin, Wen-Harn Pan, Yen-Ching Chen, and Chin-Lon Lin. “Vegetarian Diet, Food Substitution, and Nonalcoholic Fatty Liver.” Ci Ji Yi Xue Za Zhi = Tzu-Chi Medical Journal 30, no. 2 (June 2018): 102–9. Accessed January 21, 2020. https://doi.org/10.4103/tcmj.tcmj_109_17.
  14. ↑ Mazidi, Mohsen, and Andre Pascal Kengne. “Higher Adherence to Plant-Based Diets Are Associated with Lower Likelihood of Fatty Liver.” Clinical Nutrition 38, no. 4 (August 2019): 1672–77. Accessed January 21, 2020. https://doi.org/10.1016/j.clnu.2018.08.010.
  15. ↑ Zhong, Victor W., Linda Van Horn, Marilyn C. Cornelis, John T. Wilkins, Hongyan Ning, Mercedes R. Carnethon, Philip Greenland, et al. “Associations of Dietary Cholesterol or Egg Consumption With Incident Cardiovascular Disease and Mortality.” JAMA 321, no. 11 (March 19, 2019): 1081. Accessed January 21, 2020. https://doi.org/10.1001/jama.2019.1572.
  16. ↑ Physicians Committee for Responsible Medicine. “Clearing Up Choline Confusion.” Accessed January 20, 2020. https://www.pcrm.org/news/blog/clearing-choline-confusion.
  17. ↑ “A Closer Look Inside Healthy Eating Patterns - 2015-2020 Dietary Guidelines | Health.Gov.” Accessed January 22, 2020. https://health.gov/dietaryguidelines/2015/guidelines/chapter-1/a-closer-look-inside-healthy-eating-patterns/.
  18. ↑ Derbyshire, Emma. “Could We Be Overlooking a Potential Choline Crisis in the United Kingdom?” BMJ Nutrition, Prevention & Health 2, no. 2 (December 1, 2019): 86–89. Accessed January 20, 2020. https://doi.org/10.1136/bmjnph-2019-000037.
  19. ↑ Shaw, G. M., S. L. Carmichael, W. Yang, S. Selvin, and D. M. Schaffer. “Periconceptional Dietary Intake of Choline and Betaine and Neural Tube Defects in Offspring.” American Journal of Epidemiology 160, no. 2 (July 15, 2004): 102–9. Accessed January 21, 2020. https://doi.org/10.1093/aje/kwh187.
  20. ↑ Shaw, Gary M., Richard H. Finnell, Henk J. Blom, Suzan L. Carmichael, Stein Emil Vollset, Wei Yang, and Per M. Ueland. “Choline and Risk of Neural Tube Defects in a Folate-Fortified Population:” Epidemiology 20, no. 5 (September 2009): 714–19. Accessed January 21, 2020. https://doi.org/10.1097/EDE.0b013e3181ac9fe7.
  21. ↑ Mills, James L, Ruzong Fan, Lawrence C Brody, Aiyi Liu, Per M Ueland, Yifan Wang, Peadar N Kirke, Barry Shane, and Anne M Molloy. “Maternal Choline Concentrations during Pregnancy and Choline-Related Genetic Variants as Risk Factors for Neural Tube Defects.” The American Journal of Clinical Nutrition 100, no. 4 (October 1, 2014): 1069–74. Accessed January 21, 2020. https://doi.org/10.3945/ajcn.113.079319.
  22. ↑ Carmichael, Suzan L., Wei Yang, and Gary M. Shaw. “Periconceptional Nutrient Intakes and Risks of Neural Tube Defects in California.” Birth Defects Research Part A: Clinical and Molecular Teratology 88, no. 8 (2010): 670–78. Accessed January 21, 2020. https://doi.org/10.1002/bdra.20675.
  23. ↑ Chandler, Angela L., Charlotte A. Hobbs, Bridget S. Mosley, Robert J. Berry, Mark A. Canfield, Yan Ping Qi, Anna Maria Siega‐Riz, and Gary M. Shaw. “Neural Tube Defects and Maternal Intake of Micronutrients Related to One-Carbon Metabolism or Antioxidant Activity.” Birth Defects Research Part A: Clinical and Molecular Teratology 94, no. 11 (2012): 864–74. Accessed January 21, 2020. https://doi.org/10.1002/bdra.23068.
  24. ↑ “Neural Tube Defects (NTDs) | Duke Molecular Physiology Institute.” Accessed January 21, 2020. https://dmpi.duke.edu/neural-tube-defects-ntds.
  25. ↑ Berry, Robert J., Zhu Li, J. David Erickson, Song Li, Cynthia A. Moore, Hong Wang, Joseph Mulinare, et al. “Prevention of Neural-Tube Defects with Folic Acid in China.” New England Journal of Medicine 341, no. 20 (November 11, 1999): 1485–90. Accessed January 21, 2020. https://doi.org/10.1056/NEJM199911113412001.
  26. ↑ Green, Nancy S. “Folic Acid Supplementation and Prevention of Birth Defects.” The Journal of Nutrition 132, no. 8 (August 1, 2002): 2356S-2360S. Accessed January 21, 2020. https://doi.org/10.1093/jn/132.8.2356S.
  27. ↑ Majchrzak, D., I. Singer, M. Männer, P. Rust, D. Genser, K.-H. Wagner, and I. Elmadfa. “B-Vitamin Status and Concentrations of Homocysteine in Austrian Omnivores, Vegetarians and Vegans.” Annals of Nutrition and Metabolism 50, no. 6 (2006): 485–91. Accessed January 21, 2020. https://doi.org/10.1159/000095828.
  28. ↑ Koebnick, Corinna, Ulrike A. Heins, Ingrid Hoffmann, Pieter C. Dagnelie, and Claus Leitzmann. “Folate Status during Pregnancy in Women Is Improved by Long-Term High Vegetable Intake Compared with the Average Western Diet.” The Journal of Nutrition 131, no. 3 (April 1, 2001): 733–39. Accessed January 21, 2020. https://doi.org/10.1093/jn/131.3.733.
  29. ↑ 29.0 29.1 Gilliver, Liam. “Rachel Riley Defends Plant-Based Diet Amid Concerns Around Choline.” Vegan News, Plant Based Living, Food, Health & more. Accessed January 21, 2020. https://www.plantbasednews.org/news/rachel-riley-defends-plant-based-diet.
  30. ↑ Bloomfield, Hanna E., Robert Kane, Eva Koeller, Nancy Greer, Roderick MacDonald, and Timothy Wilt. Benefits and Harms of the Mediterranean Diet Compared to Other Diets. VA Evidence-Based Synthesis Program Reports. Washington (DC): Department of Veterans Affairs (US), 2015. http://www.ncbi.nlm.nih.gov/books/NBK379574/.
  31. ↑ Bloomfield, Hanna E., Robert Kane, Eva Koeller, Nancy Greer, Roderick MacDonald, and Timothy Wilt. Benefits and Harms of the Mediterranean Diet Compared to Other Diets. VA Evidence-Based Synthesis Program Reports. Washington (DC): Department of Veterans Affairs (US), 2015. http://www.ncbi.nlm.nih.gov/books/NBK379574/.
  32. ↑ Folate, Institute of Medicine (US) Standing Committee on the Scientific Evaluation of Dietary Reference Intakes and its Panel on, Other B. Vitamins, and And Choline. Choline. National Academies Press (US), 1998. Accessed January 21, 2020. https://www.ncbi.nlm.nih.gov/books/NBK114308/.
  33. ↑ Zeisel, S. H., K. A. Da Costa, P. D. Franklin, E. A. Alexander, J. T. Lamont, N. F. Sheard, and A. Beiser. “Choline, an Essential Nutrient for Humans.” FASEB Journal: Official Publication of the Federation of American Societies for Experimental Biology 5, no. 7 (April 1991): 2093–98.
  34. ↑ “Dietary Reference Intakes: The Essential Guide to Nutrient Requirements”. Accessed January 22, 2020. https://doi.org/10.17226/11537.
  35. ↑ Hollenbeck, Clarie B. “An Introduction to the Nutrition and Metabolism of Choline.” Central Nervous System Agents in Medicinal Chemistry 12, no. 2 (June 2012): 100–113. Accessed January 21, 2020. https://doi.org/10.2174/187152412800792689.
  36. ↑ “Dietary Reference Values for Choline.” EFSA Journal 14, no. 8 (2016): e04484. Accessed January 22, 2020. https://doi.org/10.2903/j.efsa.2016.4484.

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