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Department of Nutrition, School of Public Health and School of Medicine, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599-7461 and * U.S. Department of Agriculture, ARS, BHNRC, Nutrient Data Laboratory, Beltsville, MD 20705
2To whom correspondence should be addressed. E-mail: steven_zeisel{at}unc.edu.
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ABSTRACT |
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 TOP ABSTRACT MATERIALS AND METHODSRESULTS AND DISCUSSIONLITERATURE CITED |
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KEY WORDS: • food composition • choline • phosphatidylcholine • sphingomyelin • betaine
Choline is required for synthesis of the phospholipids in cell membranes, methyl group metabolism and cholinergic neurotransmission (1
). Betaine, a derivative of choline, is also important because of its role in the donation of methyl groups to homocysteine to form methionine (2
,3
). Humans have a requirement for choline; the U.S. Institute of Medicine recently made recommendations for choline intake in the diet (4
). Due to insufficient data with which to assess choline and betaine intake and to derive an estimated average requirement for choline, only an Adequate Intake of 
550 mg/d for men could be estimated. Healthy men fed a choline-deficient diet, with normal folate and vitamin B-12 intake, became choline depleted and developed liver steatosis and damage (elevated plasma alanine aminotransferase) (5
). Some humans (both men and women) receiving total parenteral nutrition solutions devoid of choline developed fatty liver and liver damage that resolved when a source of dietary choline was provided (6
–11
). Animals fed a choline-deficient diet may also develop growth retardation, renal dysfunction and hemorrhage, or bone abnormalities (12
–14
). Folate and choline metabolism are highly interrelated, and epidemiologic studies indicate a strong inverse association between dietary folate intake or blood folate levels and the risk of developing colorectal adenomas or cancer (15
) and heart disease (16
). Knowledge of choline intake could well enhance these analyses.
Some humans with a defect in the flavin-containing monooxygenase 3 gene, FM03, develop fishy body odor because they accumulate trimethylamine, a breakdown product formed from choline by bacteria in the gut (17 –19 ). An 1999 NIH sponsored workshop on trimethylaminuria estimated that as much as 1% of the U.S. population may suffer from this genetic defect, but its true incidence is not known. A choline-restricted diet is useful in these patients because it diminishes body odor (20 ). These diets have heretofore been constructed without sufficient information, and clinical care could be enhanced if the choline concentration of foods were better described.
There are some data, generated using outdated methods, on the unesterified choline in foods (21 ,22 ) and there is limited information about the phosphatidylcholine (PtdCho, also called lecithin) in foods (23 ). Almost no information is available concerning the other esterified forms of choline in foods. More is known about the betaine concentration of some foods (24 –26 ). In this study, we collected representative food samples and analyzed the choline concentration of common foods using liquid chromatography-mass spectrometry. This study will provide choline data for products analyzed under the USDA National Food and Nutrition Analysis Program (NFNAP). These data will also be used to establish a special choline database to be posted on the USDA Nutrient Data Laboratory web site (http://www.nal.usda.gov/fnic/foodcomp).
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MATERIALS AND METHODS |
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TOPABSTRACTMATERIALS AND METHODSRESULTS AND DISCUSSIONLITERATURE CITED |
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Food items for this study were obtained either locally or through a nation-wide pick-up of 12 retail outlets in accordance with the national sampling plan developed for the NFNAP (27 ) and shipped to the Food Analysis Laboratory Control Center, Virginia Polytechnic Institute and State University, Blacksburg, VA, for preparation and compositing (Table 1). For each composite, the maximum amount was taken from each sample unit to be included, with a minimum subsample size of 1 serving (according to typical serving sizes) and preferably whole units (i.e., cans, fruits, bottles). Appropriate cooking methods were used. Packaged foods were prepared according to package directions. Both fresh and frozen vegetables were cooked in boiling water for 8–10 min and then drained and cooled (except mushrooms and alfalfa seed, which were processed directly without cooking). Salmon and Atlantic cod were baked at 218°C for 20 min. Grains were boiled in 2 parts water and then simmered for 20 min. Brown rice was boiled in 1 part water then simmered for 20 min. Whole chicken was roasted in a preheated oven at 218°C for at least 25–30 min or until an internal temperature of 82°C was reached; no-fat medium or nonstick spray was added. One half of the bird was analyzed with skin, the other without. Ground beef samples were blended for 2 min in a Hobart mixer (Hobart, Troy, OH), pressed into a patty mold (112 g), then broiled in a preheated conventional oven to an internal temperature of 72°C. Beef liver samples were browned in a nonstick Rival skillet (Holmes Group, Kansas City, MO) preheated to 162° C for 5 min, then cooked to an internal temperature of at least 74°C (6–10 min). Chicken livers were simmered in a nonstick Rival skillet for 6–10 min to a minimal internal temperature of 79°C. Plain muffins were prepared according to a recipe (NDB# 18273). Mashed potatoes were prepared by boiling minced potatoes and adding whole milk and mashing until a smooth texture was achieved; no salt or butter was added.
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Homogenates of foods were shipped to the University of North Carolina on dry ice. All of the samples were either analyzed immediately or stored at -80°C until the time of analysis. Frozen food samples were thawed at room temperature for 2–4 h, the sample was mixed for 30 s with a stainless steel spatula and an aliquot was taken. Choline compounds were extracted from foods using the procedure of Bligh and Dyer (28
), spiked with deuterium-labeled internal standards of all the analytes and analyzed using liquid chromatography-electrospray ionization-isotope dilution mass spectrometry as previously described (29
). Quality assurance was monitored through the use of duplicate sampling, in-house control materials, and Standard Reference Materials.
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RESULTS AND DISCUSSION |
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TOPABSTRACTMATERIALS AND METHODSRESULTS AND DISCUSSIONLITERATURE CITED |
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When both cooked and raw vegetables were analyzed, we observed that total choline content of the foods per 100 g remained similar (Table 1). Free choline concentration was lower when the food was cooked, whereas the choline in PtdCho was proportionately higher. We discovered that when raw vegetables were finely minced, phospholipase D was activated, resulting in the conversion of PtdCho to phosphatidic acid and choline (assessed using TLC, data not shown). This enzyme activity can be inhibited by boiling the raw vegetable in water before mincing (at least 3 min; data not shown) or by homogenizing the fresh vegetable in hot (82°C) isopropanol (33 ). We present values for raw vegetables despite this mincing artifact, because chewing foods should produce the same result, i.e., a conversion of PtdCho to choline.
Methyltetrahydrofolate and choline are major dietary methyl donors that are metabolically interrelated (1 ). Both regulate the formation of S-adenosylmethionine, and thereby influence methylation reactions. Diminished folate availability increases demand for choline as a methyl donor (34 ), and decreased choline availability increases demand for folate methyl groups (35 ). For this reason, both methyl donors must be considered in any attempts to understand how methyl status could be mechanistically related to disease processes. Epidemiologists have been interested in methyl metabolism as it relates to chronic diseases. For example, >20 epidemiologic studies indicate a strong inverse association between dietary folate intake or blood folate levels and the risk of developing colorectal adenomas or cancer (15 ). Others have examined dietary folate intake and heart disease (16 ), and clinical trials indicated efficacy for increased diet folic acid intake in hypertension and restenosis of coronary arteries (36 ,37 ). These studies focused on the folate and methionine content of diet, but did not include dietary choline intake as a variable because data were not available on the choline concentration of common foods. Reanalysis of these studies, using the food data we now provide, may identify important interactions between dietary choline and folic acid. Perhaps the most affected groups will be those consuming diets low in both methyl donors. In such analyses, both total choline and betaine should be considered as fungible sources of methyl groups. In other studies in which the suspected mechanism of action is not methyl donation, but rather via the role of choline as a neurotransmitter precursor or membrane precursor, the value for total choline without betaine might be preferred because betaine cannot be converted into acetylcholine or membrane phospholipids. Similarly, betaine does not contribute to trimethylamine formation in trimethylaminuria.
In conclusion, data from this study will be used to establish a choline database to facilitate research relating choline intake to risk for diseases. Furthermore, it will provide the basic information for estimating dietary requirements and for developing nutrient recommendations.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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3 GPCho, glycerophosphocholine; PCho, phosphocholine; PtdCho, phosphatidylcholine; SM, sphingomyelin.
Manuscript received 17 January 2003. Initial review completed 26 January 2003. Revision accepted 14 February 2003.
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LITERATURE CITED |
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TOPABSTRACTMATERIALS AND METHODSRESULTS AND DISCUSSIONLITERATURE CITED |
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21. Engel, R. W. (1943) The choline content of animal and plant products. J. Nutr. 25:441-446.
22. McIntire, J. M., Schweigert, B. S. & Elvehjem, C. A. (1944) The choline and pyridoxine content of meats. J. Nutr. 28:219-223.
23. Weihrauch, J. L. & Son, Y.-S. (1983) The phospholipid content of foods. J. Am. Oil Chem. Soc. 60:1971-1978.
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25. Saarinen, M. T., Kettunen, H., Pulliainen, K., Peuranen, S., Tiihonen, K. & Remus, J. (2001) A novel method to analyze betaine in chicken liver: effect of dietary betaine and choline supplementation on the hepatic betaine concentration in broiler chicks. J. Agric. Food Chem. 49:559-563.[Medline]
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29. Koc, H., Mar, M. H., Ranasinghe, A., Swenberg, J. A. & Zeisel, S. H. (2002) Quantitation of choline and its metabolites in tissues and foods by liquid chromatography/electrospray ionization-isotope dilution mass spectrometry. Anal. Chem. 74:4734-4740.[Medline]
30. Cheng, W.-L., Holmes-McNary, M. Q., Mar, M.-H., Lien, E. L. & Zeisel, S. H. (1996) Bioavailability of choline and choline esters from milk in rat pups. J. Nutr. Biochem. 7:457-464.
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 M. Kohlmeier, K.-A. da Costa, L. M. Fischer, and S. H. Zeisel Genetic variation of folate-mediated one-carbon transfer pathway predicts susceptibility to choline deficiency in humans PNAS, November 1, 2005; 102(44): 16025 - 16030. [Abstract] [Full Text] [PDF]
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J. Song, K. A. da Costa, L. M. Fischer, M. Kohlmeier, L. Kwock, S. Wang, and S. H. Zeisel Polymorphism of the PEMT gene and susceptibility to nonalcoholic fatty liver disease (NAFLD) FASEB J, August 1, 2005; 19(10): 1266 - 1271. [Abstract] [Full Text] [PDF]
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M. R Olthof, E. J Brink, M. B Katan, and P. Verhoef Choline supplemented as phosphatidylcholine decreases fasting and postmethionine-loading plasma homocysteine concentrations in healthy men Am. J. Clinical Nutrition, July 1, 2005; 82(1): 111 - 117. [Abstract] [Full Text] [PDF]
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N. R. Augspurger, C. S. Scherer, T. A. Garrow, and D. H. Baker Dietary S-Methylmethionine, a Component of Foods, Has Choline-Sparing Activity in Chickens J. Nutr., July 1, 2005; 135(7): 1712 - 1717. [Abstract] [Full Text] [PDF]
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A. Melse-Boonstra, P. I Holm, P. M Ueland, M. Olthof, R. Clarke, and P. Verhoef Betaine concentration as a determinant of fasting total homocysteine concentrations and the effect of folic acid supplementation on betaine concentrations Am. J. Clinical Nutrition, June 1, 2005; 81(6): 1378 - 1382. [Abstract] [Full Text] [PDF]
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M. Ishinaga, A. Ueda, T. Mochizuki, S. Sugiyama, and T. Kobayashi Cholesterol Intake Is Associated with Lecithin Intake in Japanese People J. Nutr., June 1, 2005; 135(6): 1451 - 1455. [Abstract] [Full Text] [PDF]
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T. L. Yang, J. Hung, M. A. Caudill, T. F. Urrutia, A. Alamilla, C. A. Perry, R. Li, H. Hata, and E. A. Cogger A Long-Term Controlled Folate Feeding Study in Young Women Supports the Validity of the 1.7 Multiplier in the Dietary Folate Equivalency Equation J. Nutr., May 1, 2005; 135(5): 1139 - 1145. [Abstract] [Full Text] [PDF]
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L. M. Fischer, J. A. Scearce, M.-H. Mar, J. R. Patel, R. T. Blanchard, B. A. Macintosh, M. G. Busby, and S. H. Zeisel Ad Libitum Choline Intake in Healthy Individuals Meets or Exceeds the Proposed Adequate Intake Level J. Nutr., April 1, 2005; 135(4): 826 - 829. [Abstract] [Full Text] [PDF]
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K.-A. da Costa, C. E Gaffney, L. M Fischer, and S. H Zeisel Choline deficiency in mice and humans is associated with increased plasma homocysteine concentration after a methionine load Am. J. Clinical Nutrition, February 1, 2005; 81(2): 440 - 444. [Abstract] [Full Text] [PDF]
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 S. H. Zeisel Nutritional Importance of Choline for Brain Development J. Am. Coll. Nutr., December 1, 2004; 23(suppl_6): 621S - 626S. [Abstract] [Full Text] [PDF]
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S. A. Craig Betaine in human nutrition Am. J. Clinical Nutrition, September 1, 2004; 80(3): 539 - 549. [Abstract] [Full Text] [PDF]
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 G. M. Shaw, S. L. Carmichael, W. Yang, S. Selvin, and D. M. Schaffer Periconceptional Dietary Intake of Choline and Betaine and Neural Tube Defects in Offspring Am. J. Epidemiol., July 15, 2004; 160(2): 102 - 109. [Abstract] [Full Text] [PDF]
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K.-A. da Costa, M. Badea, L. M Fischer, and S. H Zeisel Elevated serum creatine phosphokinase in choline-deficient humans: mechanistic studies in C2C12 mouse myoblasts Am. J. Clinical Nutrition, July 1, 2004; 80(1): 163 - 170. [Abstract] [Full Text] [PDF]
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S.-W. Choi, S. Friso, H. Ghandour, P. J. Bagley, J. Selhub, and J. B. Mason Vitamin B-12 Deficiency Induces Anomalies of Base Substitution and Methylation in the DNA of Rat Colonic Epithelium J. Nutr., April 1, 2004; 134(4): 750 - 755. [Abstract] [Full Text] [PDF]
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K. L. Herron and M. L. Fernandez Are the Current Dietary Guidelines Regarding Egg Consumption Appropriate? J. Nutr., January 1, 2004; 134(1): 187 - 190. [Full Text] [PDF]
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M. R. Olthof, T. van Vliet, E. Boelsma, and P. Verhoef Low Dose Betaine Supplementation Leads to Immediate and Long Term Lowering of Plasma Homocysteine in Healthy Men and Women J. Nutr., December 1, 2003; 133(12): 4135 - 4138. [Abstract] [Full Text] [PDF]
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