Homocysteine and methylmalonic acid in diagnosis and risk assessment from infancy to adolescence

Bjørke Monsen, Anne Lise; Ueland, Per Magne

doi:10.1093/ajcn/78.1.7

Cited by 144Folate and B Vitamins ResearchMetabolism and Genetic DisordersPorphyrin Metabolism and Disorders

Homocysteine and methylmalonic acid in diagnosis and risk assessment from infancy to adolescence

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Bjørke Monsen, Anne Lise, Ueland, Per Magne·2003·The American Journal of Clinical Nutrition

DOI 10.1093/ajcn/78.1.7

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Abstract

The concentration of total homocysteine (tHcy) in serum and plasma is elevated in both folate and cobalamin deficiencies, whereas methylmalonic acid (MMA) in serum, plasma, or urine is a specific marker of cobalamin function. The combined measurement of both metabolites is useful for the diagnosis and follow-up of these deficiency states. In addition, tHcy is elevated under various pathologic states (eg, renal failure), and hyperhomocysteinemia is associated with an increased risk of cardiovascular disease, cognitive dysfunction, and adverse pregnancy outcomes. The diagnostic utility of tHcy and MMA concentrations as markers of folate and cobalamin deficiencies in healthy and diseased children has been documented. This article briefly summarizes the biochemical background of tHcy and MMA and the associations of tHcy and MMA with various disease states and focuses on novel data obtained in infants, children, and adolescents, with emphasis on cobalamin status in infants. The utility of tHcy and MMA as indicators of cobalamin and folate deficiencies in adults can be extended to infants and older children. Furthermore, as in adults, tHcy is related to unhealthy lifestyle factors and is a risk factor for vascular disease. High MMA concentrations in newborns, occasionally denoted as benign methylmalonic aciduria, may reflect impaired cobalamin function.

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The functional markers tHcy and MMA have been established as useful indicators of vitamin B-12 status and may be more sensitive indicators of mild vitamin B-12 deficiency.
“However, the functional markers total homocysteine (tHcy) 13 and methylmalonic acid (MMA) have been established as useful indicators of vitamin B-12 status (13) and may be more sensitive indicators of mild vitamin B-12 deficiency (14,15).”
From Vitamin B-12 status in infancy is positively associated with development and cognitive functioning 5 y later in Nepalese children (2017) · cites this paper as [15]
Elevated tHcy values in these children could not be caused by folate deficiency but rather poor cobalamin status.
“the elevated tHcy values in these children could not be caused by folate deficiency but rather poor cobalamin status (14,15).”
From Vitamin B-12 status in infancy is positively associated with development and cognitive functioning 5 y later in Nepalese children (2017) · cites this paper as [15]

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Facts and recommendations about total homocysteine determinations: an expert opinion
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Biomarkers and Algorithms for the Diagnosis of Vitamin B12 Deficiency
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Causes of Vitamin B <sub>12</sub> and Folate Deficiency
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Vitamin B-12 Supplementation during Pregnancy and Early Lactation Increases Maternal, Breast Milk, and Infant Measures of Vitamin B-12 Status
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Cobalamin and folate status in infants and young children in a low-to-middle income community in India
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Validation of the Diet Quality Index for Adolescents by comparison with biomarkers, nutrient and food intakes: the HELENA study
Vyncke, K. E., Fernandez, E. C., Fajó‐Pascual, M., Cuenca‐García, M., Keyzer, W. D., González‐Gross, M., Moreno, L. A., Béghin, L., Breidenassel, C., Kersting, M., et al. (2012) · British Journal Of Nutrition · doi:10.1017/s000711451200414x · Cited by 120 · see citing works
Kinetic Modeling of Storage Effects on Biomarkers Related to B Vitamin Status and One-Carbon Metabolism
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Self-citation
Vitamin B-12 status in infancy is positively associated with development and cognitive functioning 5 y later in Nepalese children
Kvestad, I., Hysing, M., Shrestha, M., Ulak, M., Thorne-Lyman, A. L., Henjum, S., Ueland, P. M., Midttun, Ø., Fawzi, W., Chandyo, R. K., et al. (2017) · The American Journal of Clinical Nutrition · doi:10.3945/ajcn.116.144931 · Cited by 92 · see citing works
Self-citation
Maternal Folate and Cobalamin Status Predicts Vitamin Status in Newborns and 6-Month-Old Infants
Hay, G., Clausen, T., Whitelaw, A., Trygg, K. U., Johnston, C., Henriksen, T., & Refsum, H. (2010) · Journal of Nutrition · doi:10.3945/jn.109.117424 · Cited by 91 · see citing works
Folate and cobalamin status in relation to breastfeeding and weaning in healthy infants
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Low Plasma Vitamin B-6 Status Affects Metabolism through the Kynurenine Pathway in Cardiovascular Patients with Systemic Inflammation1–4
Midttun, Ø., Ulvik, A., Pedersen, E. R., Ebbing, M., Bleie, Ø., Schartum-Hansen, H., Nilsen, R. M., Nygard, O. K., & Ueland, P. M. (2011) · Journal of Nutrition · doi:10.3945/jn.110.133082 · Cited by 80 · see citing works
Self-citation
Cobalamin supplementation improves motor development and regurgitations in infants: results from a randomized intervention study
Torsvik, I., Ueland, P. M., Markestad, T., & Bjørke-Monsen, A.-L. (2013) · The American Journal of Clinical Nutrition · doi:10.3945/ajcn.113.061549 · Cited by 74 · see citing works
Genome-wide association study of homocysteine levels in Filipinos provides evidence for CPS1 in women and a stronger MTHFR effect in young adults
Lange, L. A., Croteau‐Chonka, D. C., Marvelle, A. F., Li, Q., Gaulton, K. J., Kuzawa, C. W., McDade, T. W., Wang, Y., Li, Y., Levy, S., et al. (2010) · Human Molecular Genetics · doi:10.1093/hmg/ddq062 · Cited by 69 · see citing works
Vitamin B-12, Folic Acid, and Growth in 6- to 30-Month-Old Children: A Randomized Controlled Trial
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Effects of maternal vitamin B12 supplementation on early infant neurocognitive outcomes: a randomized controlled clinical trial
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A simple high-throughput method for the determination of plasma methylmalonic acid by liquid chromatography-tandem mass spectrometry
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Self-citation
A Common Polymorphism in HIBCH Influences Methylmalonic Acid Concentrations in Blood Independently of Cobalamin
Molloy, A. M., Pangilinan, F., Mills, J. L., Shane, B., O’Neill, M. B., McGaughey, D. M., Velkova, A., Abaan, H. Ö., Ueland, P. M., McNulty, H., et al. (2016) · The American Journal of Human Genetics · doi:10.1016/j.ajhg.2016.03.005 · Cited by 59 · see citing works
Self-citation
Plasma cobalamin and folate and their metabolic markers methylmalonic acid and total homocysteine among Egyptian children before and after nutritional supplementation with the probiotic bacteriaLactobacillus acidophilusin yoghurt matrix
Mohammad, M. A., Molloy, A. M., Scott, J. M., & Hussein, L. (2006) · International Journal of Food Sciences and Nutrition · doi:10.1080/09637480600968735 · Cited by 57 · see citing works
Assessment of Micronutrient Status in Critically Ill Children: Challenges and Opportunities
Dao, D. T., Anez‐Bustillos, L., Cho, B. S., Li, Z., Puder, M., & Gura, K. M. (2017) · Nutrients · doi:10.3390/nu9111185 · Cited by 56 · see citing works
Total Homocysteine, Folate, and Cobalamin, and Their Relation to Genetic Polymorphisms, Lifestyle and Body Mass Index in Healthy Children and Adolescents
Huemer, M., Vonblon, K., Födinger, M., Krumpholz, R., Hubmann, M., Ulmer, H., & Simma, B. (2006) · Pediatric Research · doi:10.1203/01.pdr.0000246099.39469.18 · Cited by 53 · see citing works
Total serum homocysteine, folate and vitamin B12 in a Greek school age population
Papandreou, D., Mavromichalis, I., Makedou, A., Rousso, I., & Arvanitidou, M. (2006) · Clinical Nutrition · doi:10.1016/j.clnu.2006.02.006 · Cited by 49 · see citing works
Anemias
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Comparison of the Influence of Volume-Oriented Training and High-Intensity Interval Training on Serum Homocysteine and Its Cofactors in Young, Healthy Swimmers
Herrmann, M., Wilkinson, J., Schorr, H., Obeid, R., Georg, T., Urhausen, A. J. P., Scharhag, J., Kindermann, W., & Herrmann, W. (2003) · Clinical Chemistry and Laboratory Medicine (CCLM) · doi:10.1515/cclm.2003.234 · Cited by 46 · see citing works
Effect of vitamin supplementation to HIV-infected pregnant women on the micronutrient status of their infants
Baylín, A., Villamor, E., Rifai, N., Msamanga, G., & Fawzi, W. W. (2005) · European Journal of Clinical Nutrition · doi:10.1038/sj.ejcn.1602201 · Cited by 45 · see citing works
Iron Deficiency Anemia and Depleted Body Iron Reserves Are Prevalent among Pregnant African-American Adolescents
Iannotti, L. L., O'Brien, K. O., Chang, S.-C., Mancini, J., Nathanson, M. S., Liu, S., Harris, Z. L., & Witter, F. R. (2005) · Journal of Nutrition · doi:10.1093/jn/135.11.2572 · Cited by 45 · see citing works
Does early vitamin B12 supplementation improve neurodevelopment and cognitive function in childhood and into school age: a study protocol for extended follow-ups from randomised controlled trials in India and Tanzania
Winje, B. A., Kvestad, I., Krishnamachari, S., Manji, K. P., Taneja, S., Bellinger, D. C., Bhandari, N., Bisht, S., Darling, A. M., Duggan, C., et al. (2018) · BMJ Open · doi:10.1136/bmjopen-2017-018962 · Cited by 43 · see citing works
Fisiopatologia da deficiência de vitamina B12 e seu diagnóstico laboratorial
Paniz, C., Grotto, D., Schmitt, G. C., Valentini, J., Schott, K. L., Pomblum, V. J., & García, S. C. (2005) · Jornal Brasileiro de Patologia e Medicina Laboratorial · doi:10.1590/s1676-24442005000500007 · Cited by 42 · see citing works
Simple, Fast, and Simultaneous Detection of Plasma Total Homocysteine, Methylmalonic Acid, Methionine, and 2-Methylcitric Acid Using Liquid Chromatography and Mass Spectrometry (LC/MS/MS)
Fu, X., Xu, Y.-K., Chan, P., & Pattengale, P. K. (2013) · JIMD Reports · doi:10.1007/8904_2012_205 · Cited by 42 · see citing works
Impaired arsenic metabolism in children during weaning
Fängström, B., Hamadani, J. D., Nermell, B., Grandér, M., Palm, B., & Vahter, M. (2009) · Toxicology and Applied Pharmacology · doi:10.1016/j.taap.2008.12.019 · Cited by 41 · see citing works
Homozygous nonsense mutation in the MCEE gene and siRNA suppression of methylmalonyl-CoA epimerase expression: A novel cause of mild methylmalonic aciduria
Dobson, C. M., Gradinger, A. B., Longo, N., Wu, X., Leclerc, D., Lerner‐Ellis, J. P., Lemieux, M., Bélair, C., Watkins, D., Rosenblatt, D. S., et al. (2006) · Molecular Genetics and Metabolism · doi:10.1016/j.ymgme.2006.03.009 · Cited by 39 · see citing works
Perspectives on Peripheral Neuropathy as a Consequence of Metformin-Induced Vitamin B12 Deficiency in T2DM
Ahmed, M. A., Muntingh, G. L., & Rheeder, P. (2017) · International Journal of Endocrinology · doi:10.1155/2017/2452853 · Cited by 37 · see citing works
Undernutrition, fatty acid and micronutrient status in relation to cognitive performance in Indian school children: a cross-sectional study
Eilander, A., Muthayya, S., van der Knaap, H. C. M., Srinivasan, K., Thomas, T. S., Kok, F. J., Kurpad, A. V., & Osendarp, S. J. M. (2009) · British Journal Of Nutrition · doi:10.1017/s000711450999273x · Cited by 35 · see citing works
Folate and homocysteine interrelationships including genetics of the relevant enzymes
Molloy, A. M. (2004) · Current Opinion in Lipidology · doi:10.1097/00041433-200402000-00010 · Cited by 35 · see citing works
The Relationship Between Folate, Vitamin B12 and Gestational Diabetes Mellitus with Proposed Mechanisms and Foetal Implications
Maher, A., & Sobczyńska‐Malefora, A. (2021) · Journal of Family & Reproductive Health · doi:10.18502/jfrh.v15i3.7131 · Cited by 34 · see citing works
Long-Term Intermittent Hypoxia Elevates Cobalt Levels in the Brain and Injures White Matter in Adult Mice
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Vitamin B 12 , Folate, Homocysteine and Urinary Methylmalonic Acid Levels in Infants
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Cobalamin and Folate Status in 6 to 35 Months Old Children Presenting with Acute Diarrhea in Bhaktapur, Nepal
Ulak, M., Chandyo, R. K., Adhikari, R., Sharma, P. R., Sommerfelt, H., Refsum, H., & Strand, T. A. (2014) · PLoS ONE · doi:10.1371/journal.pone.0090079 · Cited by 33 · see citing works
Plasma Homocysteine Concentrations in Greek Children Are Influenced by an Interaction between the Methylenetetrahydrofolate Reductase C677T Genotype and Folate Status
Papoutsakis, C., Yiannakouris, N., Μanios, Y., Papaconstantinou, E., Magkos, F., Schulpis, K. H., Zampelas, A., & Matalas, A. (2005) · Journal of Nutrition · doi:10.1093/jn/135.3.383 · Cited by 32 · see citing works
Demographic, Lifestyle, and Health Characteristics and Serum B Vitamin Status Are Determinants of Plasma Total Homocysteine Concentration in the Post-Folic Acid Fortification Period, 1999–2004
Ganji, V., & Kafai, M. R. (2008) · Journal of Nutrition · doi:10.3945/jn.108.092726 · Cited by 31 · see citing works
The effect of MTHFR(C677T) genotype on plasma homocysteine concentrations in healthy children is influenced by gender
Papoutsakis, C., Yiannakouris, N., Μanios, Y., Papaconstantinou, E., Magkos, F., Schulpis, K. H., Zampelas, A., & Matalas, A. (2005) · European Journal of Clinical Nutrition · doi:10.1038/sj.ejcn.1602280 · Cited by 31 · see citing works
Folate and cobalamin status in relation to diet in healthy 2-y-old children
Hay, G., Trygg, K. U., Whitelaw, A., Johnston, C., & Refsum, H. (2011) · American Journal of Clinical Nutrition · doi:10.3945/ajcn.110.003426 · Cited by 29 · see citing works
Serum homocysteine and methylmalonic acid concentrations in Chinese Shar-Pei dogs with cobalamin deficiency
Grützner, N., Heilmann, R. M., Stupka, K. C., Rangachari, V. R., Weber, K., Holzenburg, A., Suchodolski, J. S., & Steiner, J. M. (2013) · The Veterinary Journal · doi:10.1016/j.tvjl.2013.02.002 · Cited by 27 · see citing works
Gas Chromatographic−Mass Spectrometric Analysis of Biomarkers Related to Folate and Cobalamin Status in Human Serum after Dimercaptopropanesulfonate Reduction and Heptafluorobutyl Chloroformate Derivatization
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Population References for Plasma Total Homocysteine Concentrations for U.S. Children and Adolescents in the Post-Folic Acid Fortification Era
Ganji, V., & Kafai, M. R. (2005) · Journal of Nutrition · doi:10.1093/jn/135.9.2253 · Cited by 26 · see citing works
Urinary Methylmalonic Acid as an Indicator of Early Vitamin B12 Deficiency and Its Role in Polyneuropathy in Type 2 Diabetes
Sun, A.-L., Ni, Y., Li, X., Zhuang, X., Liu, Y.-T., Liu, X., & Chen, S. (2014) · Journal of Diabetes Research · doi:10.1155/2014/921616 · Cited by 26 · see citing works
Diagnostic Performances of Urinary Methylmalonic Acid/Creatinine Ratio in Vitamin B12 Deficiency
Supakul, S., Chabrun, F., Genebrier, S., N’Guyen, M., Valarche, G., Derieppe, A., Villoteau, A., Lacombe, V., & Urbanski, G. (2020) · Journal of Clinical Medicine · doi:10.3390/jcm9082335 · Cited by 26 · see citing works
Impairment of homocysteine metabolism in patients with retinal vascular occlusion and non-arteritic ischemic optic neuropathy
Stanger, O., Weger, M., Obeid, R., Temmel, W., Meinitzer, A., Steinbrugger, I., Schmut, O., & Herrmann, W. (2005) · Clinical Chemistry and Laboratory Medicine (CCLM) · doi:10.1515/cclm.2005.179 · Cited by 25 · see citing works
Incorporation of a high level of vitamin B12 into a vegetable, kaiware daikon (Japanese radish sprout), by the absorption from its seeds
Sato, K., Kudo, Y., & 村松, 久. (2004) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2004.03.011 · Cited by 24 · see citing works
Association of the 677C -->T polymorphism in the MTHFR gene with colorectal cancer in Mexican patients.
Gallegos‐Arreola, M. P., García‐Ortíz, J. E., Figuera, L. E., Puebla‐Pérez, A. M., Morgan‐Villela, G., & Zúñiga‐González, G. M. (2009) · PubMed · Cited by 24 · see citing works
The FUT2 secretor variant p.Trp154Ter influences serum vitamin B12 concentration via holo-haptocorrin, but not holo-transcobalamin, and is associated with haptocorrin glycosylation
Velkova, A., Diaz, J. E. L., Pangilinan, F., Molloy, A. M., Mills, J. L., Shane, B., Sanchez, E. L., Cunningham, C. J., McNulty, H., Cropp, C. D., et al. (2017) · Human Molecular Genetics · doi:10.1093/hmg/ddx369 · Cited by 24 · see citing works
Myricetin-loaded SBA-15 silica nanoparticles for enhanced management of pyrexia, pain, and inflammation through modulation of MAPK/NF-κB and COX-2/PGE-2 pathways: Evidence from the biochemical, histological, and metabolomic analysis
El‐Gendy, Z. A., Ammar, N. M., Kassem, A. M., Attia, M. S., Afifi, S. M., Ibrahim, A. H., Emam, S. E., Korany, R. M. S., El‐Gendy, A. E. G., & Elshamy, A. I. (2024) · International Journal of Pharmaceutics · doi:10.1016/j.ijpharm.2024.124775 · Cited by 21 · see citing works
Homocysteine effects on cellular glutathione peroxidase (GPx-1) activity underin vitroconditions
Durmaz, A., & Dikmen, N. (2007) · Journal of Enzyme Inhibition and Medicinal Chemistry · doi:10.1080/14756360601164929 · Cited by 21 · see citing works
NUTRITIONAL VITAMIN B12DEFICIENCY IN HOSPITALIZED YOUNG CHILDREN
Çetinkaya, F., Yildirmak, Y., Kutluk, G., & Eralp, E. E. (2006) · Pediatric Hematology and Oncology · doi:10.1080/08880010601001370 · Cited by 21 · see citing works
Cobalamin and Folate Status among Breastfed Infants in Bhaktapur, Nepal
Chandyo, R., Ulak, M., Kvestad, I., Hysing, M., Shrestha, M., Ranjitkar, S., Ulvik, A., Ueland, P. M., Shrestha, L., & Strand, T. A. (2018) · Nutrients · doi:10.3390/nu10050639 · Cited by 22 · see citing works
Self-citation
Maternal and infant vitamin B12 status during infancy predict linear growth at 5 years
Strand, T. A., Ulak, M., Kvestad, I., Henjum, S., Ulvik, A., Shrestha, M., Thorne‐Lyman, A., Ueland, P. M., Shrestha, P. S., & Chandyo, R. K. (2018) · Pediatric Research · doi:10.1038/s41390-018-0072-2 · Cited by 21 · see citing works
Self-citation
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Cobalamin Status and Its Biochemical Markers Methylmalonic Acid and Homocysteine in Different Age Groups from 4 Days to 19 Years
Monsen, A.-L. B., Refsum, H., Markestad, T., & Ueland, P. M. (2003) · Clinical Chemistry · doi:10.1373/clinchem.2003.019869 · Cited by 135 · see citing works
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Hyperhomocysteinemia and B-vitamin deficiencies in infants and children
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Per Magne Ueland3* Background: Recent data indicate that cobalamin and
Monsen, A.-L. B., Refsum, H., & Markestad, T. (2015)
Methylmalonic acid and homocysteine in plasma as indicators of functional cobalamin deficiency in infants on macrobiotic diets
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Methylmalonic acid values in healthy Dutch children
Hogeveen, M., van Beynum, I., van Rooij, A., Kluijtmans, L. A. J., den Heijer, M., & Blom, H. J. (2007) · European Journal of Nutrition · doi:10.1007/s00394-007-0692-5 · Cited by 12 · see citing works

Authors: Bjørke Monsen, A. L., & Ueland, P. M.
Affiliations: University of Bergen (NO)
Corresponding author: Ueland, Per Magne
ORCID: Ueland, Per Magne
Venue: The American Journal of Clinical Nutrition
Publisher: Elsevier BV
Published: 2003-07
Volume: 78
Issue: 1
Pages: 7-21
ISSN: 0002-9165 (ISSN-L)
DOI: 10.1093/ajcn/78.1.7
OpenAlex: W2156115291
Cited by: 144
References: 188
Citations by year: 2026: 3 · 2024: 8 · 2023: 7 · 2022: 2 · 2021: 7 · 2020: 9 · 2019: 3 · 2018: 5 · 2017: 5 · 2016: 5 · 2015: 2 · 2014: 8 · 2013: 11 · 2012: 7
FWCI: 1.27
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 7168 d)
Locations: American Journal of Clinical Nutrition (publishedVersion)
PubMed (publishedVersion)
Topics: Health Sciences › Medicine › Rheumatology › Folate and B Vitamins Research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Clinical Biochemistry › Metabolism and Genetic Disorders
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Porphyrin Metabolism and Disorders
Keywords: total homocysteine, methylmalonic acid, folate deficiency, vitamin B12 deficiency, hyperhomocysteinemia, infants, children, adolescents, cardiovascular risk, renal failure, pregnancy outcomes, cobalamin status
MeSH terms: Adolescent, Child, Child, Preschool, Folic Acid, Folic Acid Deficiency, Food, Fortified, Homocysteine, Humans, Infant, Infant, Newborn, Methylmalonic Acid, Vitamin B 12 Deficiency

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Homocysteine and methylmalonic acid in diagnosis and risk assessment from infancy to adolescence

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