1932
0
  1. Home
  2. A-Z Publications
  3. Annual Review of Nutrition
  4. Volume 35, 2015
  5. Article

Annual Review of Nutrition

Volume 35, 2015

Stable Isotope Ratios as Biomarkers of Diet for Health Research

Abstract

Diet is a leading modifiable risk factor for chronic disease, but it remains difficult to measure accurately due to the error and bias inherent in self-reported methods of diet assessment. Consequently, there is a pressing need for more objective biomarkers of diet for use in health research. The stable isotope ratios of light elements are a promising set of candidate biomarkers because they vary naturally and reproducibly among foods, and those variations are captured in molecules and tissues with high fidelity. Recent studies have identified valid isotopic measures of short- and long-term sugar intake, meat intake, and fish intake in specific populations. These studies provide a strong foundation for validating stable isotopic biomarkers in the general US population. Approaches to improve specificity for specific foods are needed; for example, by modeling intake using multiple stable isotope ratios or by isolating and measuring specific molecules linked to foods of interest.

Keyword(s): carbon-13, isotope ratio mass spectrometry, nitrogen-15, nutritional epidemiology, sulfur-34
Loading

Article metrics loading...

/content/journals/10.1146/annurev-nutr-071714-034511
2015-07-17
2024-04-26
Loading full text...

Full text loading...

/deliver/fulltext/nutr/35/1/annurev-nutr-071714-034511.html?itemId=/content/journals/10.1146/annurev-nutr-071714-034511&mimeType=html&fmt=ahah

Literature Cited

  1. Ambrose SH, Norr L. 1.  1993. Experimental evidence for the relationship of the carbon isotope ratios of whole diet and dietary protein to those of bone collagen and carbonate. Prehistoric Human Bone: Archaeology at the Molecular Level JB Lambert, G Grupe 1–37 Berlin: Springer-Verlag [Google Scholar]
  2. Aslibekyan S, Wiener H, Havel P, Stanhope K, O'Brien D. 2.  et al. 2013. Evidence for novel genetic loci associated with metabolic traits in the Yup'ik. Am. J. Hum. Biol. 25:673–80 [Google Scholar]
  3. Aslibekyan S, Wiener HW, Havel PJ, Stanhope KL, O'Brien DM. 3.  et al. 2014. DNA methylation patterns are associated with n-3 fatty acid intake in Yup'ik people. J. Nutr. 144:425–30 [Google Scholar]
  4. Ayliffe LK, Cerling TE, Robinson T, West AG, Sponheimer M. 4.  et al. 2004. Turnover of carbon isotopes in tail hair and breath CO2 of horses fed an isotopically varied diet. Oecologia 139:11–22 [Google Scholar]
  5. Bahar B, Harrison SM, Moloney AP, Monahan FJ, Schmidt O. 5.  2014. Isotopic turnover of carbon and nitrogen in bovine blood fractions and inner organs. Rapid Commun. Mass Spectrom. 28:1011–18 [Google Scholar]
  6. Bateman AS, Kelly SD. 6.  2007. Fertilizer nitrogen isotope signatures. Isot. Environ. Health Stud. 43:237–47 [Google Scholar]
  7. Bateman AS, Kelly SD, Woolfe M. 7.  2007. Nitrogen isotope composition of organically and conventionally grown crops. J. Agric. Food Chem. 55:2664–70 [Google Scholar]
  8. Bender M. 8.  1968. Mass spectrometric studies of carbon 13 variations in corn and other grasses. Radiocarbon 10:468–72 [Google Scholar]
  9. Bentzen TW, Follmann EH, Amstrup SC, York GS, Wooller MJ, O'Hara TM. 9.  2007. Variation in winter diet of southern Beaufort Sea polar bears inferred from stable isotope analysis. Can. J. Zool. 85:596–608 [Google Scholar]
  10. Bersamin A, Zidenberg-Cherr S, Stern JS, Luick BR. 10.  2007. Nutrient intakes are associated with adherence to a traditional diet among Yup'ik Eskimos living in remote Alaska Native communities: the CANHR study. Int. J. Circumpolar Health 66:62–70 [Google Scholar]
  11. Bingham S. 11.  2002. Biomarkers in nutritional epidemiology. Public Health Nutr. 5:821–27 [Google Scholar]
  12. Bingham SA, Luben R, Welch A, Wareham N, Khaw KT, Day N. 12.  2003. Are imprecise methods obscuring a relation between fat and breast cancer?. Lancet 362:212–14 [Google Scholar]
  13. Bol R, Pflieger C. 13.  2002. Stable isotope (13C, 15N and 34S) analysis of the hair of modern humans and their domestic animals. Rapid Commun. Mass Spectrom. 16:2195–200 [Google Scholar]
  14. Bowen GJ. 14.  2003–2013. Waterisotopes.org. http://wateriso.utah.edu/waterisotopes/index.html
  15. Bowen GJ. 15.  2010. Statistical and geostatistical mapping of precipitation water isotope ratios. Isoscapes: Understanding Movement, Pattern, and Process on Earth Through Isotope Mapping JB West, GJ Bowen, TE Dawson, KP Tu 139–60 New York: Springer [Google Scholar]
  16. Brand WA, Coplen TB. 16.  2012. Stable isotope deltas: tiny, yet robust signatures in nature. Isot. Environ. Health Stud. 48:393–409 [Google Scholar]
  17. Braun A, Auerswald K, Vikari A, Schnyder H. 17.  2013. Dietary protein content affects isotopic carbon and nitrogen turnover. Rapid Commun. Mass Spectrom. 27:2676–84 [Google Scholar]
  18. Buchardt B, Bunch V, Helin P. 18.  2007. Fingernails and diet: stable isotope signatures of a marine hunting community from modem Uummannaq, North Greenland. Chem. Geol. 244:316–29 [Google Scholar]
  19. Butz DE, Cook ME, Eghbalnia HR, Assadi-Porter F, Porter WP. 19.  2009. Changes in the natural abundance of 13CO2/12CO2 in breath due to lipopolysaccharide-induced acute phase response. Rapid Commun. Mass Spectrom. 23:3729–35 [Google Scholar]
  20. Campbell NA, Reece JB. 20.  2005. Biology San Francisco: Pearson-Benjamin Cummings
  21. Carleton SA, del Rio CM. 21.  2005. The effect of cold-induced increased metabolic rate on the rate of 13C and 15N incorporation in house sparrows (Passer domesticus). Oecologia 144:226–32 [Google Scholar]
  22. Carleton SA, Kelly L, Anderson-Sprecher R, del Rio CM. 22.  2008. Should we use one-, or multi-compartment models to describe 13C incorporation into animal tissues?. Rapid Commun. Mass Spectrom. 22:3008–14 [Google Scholar]
  23. Caut S, Angulo E, Courchamp F. 23.  2009. Variation in discrimination factors (Δ15N and Δ13C): the effect of diet isotopic values and applications for diet reconstruction. J. Appl. Ecol. 46:443–53 [Google Scholar]
  24. Cerling TE, Ayliffe LK, Dearing MD, Ehleringer JR, Passey BH. 24.  et al. 2007. Determining biological tissue turnover using stable isotopes: the reaction progress variable. Oecologia 151:175–89 [Google Scholar]
  25. Cerling TE, Wittemyer G, Ehleringer JR, Remien CH, Douglas-Hamiltond I. 25.  2009. History of Animals using Isotope Records (HAIR): a 6-year dietary history of one family of African elephants. PNAS 106:8093–100 [Google Scholar]
  26. Chesson LA, Valenzuela LO, Bowen GJ, Cerling TE, Ehleringer JR. 26.  2011. Consistent predictable patterns in the hydrogen and oxygen stable isotope ratios of animal proteins consumed by modern humans in the USA. Rapid Commun. Mass Spectrom. 25:3713–22 [Google Scholar]
  27. Choy K, Nash SH, Kristal AR, Hopkins SE, Boyer BB, O'Brien DM. 27.  2013. The carbon isotope ratio of alanine in red blood cells is a new candidate biomarker of sugar-sweetened beverage intake. J. Nutr. 143:878–84 [Google Scholar]
  28. Chukhrov F, Ermilova L, Churikov V, Nosik L. 28.  1980. The isotopic composition of plant sulfur. Org. Geochem. 2:69–75 [Google Scholar]
  29. Claydon AJ, Thom MD, Hurst JL, Beynon RJ. 29.  2012. Protein turnover: measurement of proteome dynamics by whole animal metabolic labelling with stable isotope labelled amino acids. Proteomics 12:1194–206 [Google Scholar]
  30. Cohen RM, Franco RS, Khera PK, Smith EP, Lindsell CJ. 30.  et al. 2008. Red cell life span heterogeneity in hematologically normal people is sufficient to alter HbA1c. Blood 112:4284–91 [Google Scholar]
  31. Cook CM, Alvig AL, Liu YQ, Schoeller DA. 31.  2010. The natural 13C abundance of plasma glucose is a useful biomarker of recent dietary caloric sweetener intake. J. Nutr. 140:333–37 [Google Scholar]
  32. Corr LT, Sealy JC, Horton MC, Evershed RP. 32.  2005. A novel marine dietary indicator utilising compound-specific bone collagen amino acid delta C-13 values of ancient humans. J. Archaeological Sci. 32:321–30 [Google Scholar]
  33. Davy BM, Jahren AH, Hedrick VE, Comber DL. 33.  2011. Association of δ13C in fingerstick blood with added-sugar and sugar-sweetened beverage intake. J. Am. Diet. Assoc. 111:874–78 [Google Scholar]
  34. del Rio CM, Wolf N, Carleton SA, Gannes LZ. 34.  2009. Isotopic ecology ten years after a call for more laboratory experiments. Biol. Rev. 84:91–111 [Google Scholar]
  35. DeNiro MJ, Epstein S. 35.  1977. Mechanisms of carbon isotope fractionation associated with lipid synthesis. Science 197:261–63 [Google Scholar]
  36. DeNiro MJ, Epstein S. 36.  1978. Influence of diet on the distribution of carbon isotopes in animals. Geochim. Cosmochim. Acta 42:495–506 [Google Scholar]
  37. DeNiro MJ, Epstein S. 37.  1981. Influence of diet on the distribution of nitrogen isotopes in animals. Geochim. Cosmochim. Acta 45:341–51 [Google Scholar]
  38. Downton WJS. 38.  1975. The occurrence of C4 photosynthesis among plants. Photosynthetica 9:96–105 [Google Scholar]
  39. Ehleringer JR, Bowen GJ, Chesson LA, West AG, Podlesak DW, Cerling TE. 39.  2008. Hydrogen and oxygen isotope ratios in human hair are related to geography. PNAS 105:2788–93 [Google Scholar]
  40. 40. Environ. Prot. Agency 2014. Estimated Fish Consumption Rates for the U.S. Population and Selected Subpopulations (NHANES 2003–2010)—Final Report. Washington, DC: US Environ. Prot. Agency [Google Scholar]
  41. Evans RD. 41.  2001. Physiological mechanisms influencing plant nitrogen isotope composition. Trends Plant Sci. 6:121–26 [Google Scholar]
  42. Fakhouri THI, Jahren AH, Appel LJ, Chen LW, Alavi R, Anderson CAM. 42.  2014. Serum carbon isotope values change in adults in response to changes in sugar-sweetened beverage intake. J. Nutr. 144:902–5 [Google Scholar]
  43. Farquhar GD, Ehleringer JR, Hubick KT. 43.  1989. Carbon isotope discrimination and photosynthesis. Annu. Rev. Plant Physiol. Plant Mol. Biol. 40:503–37 [Google Scholar]
  44. Farquhar GD, O'Leary MH, Berry JA. 44.  1982. On the relationship between carbon isotope discrimination and the intercellular carbon dioxide concentration in leaves. Aust. J. Plant Physiol. 9:121–37 [Google Scholar]
  45. Fischer A, Olsen J, Richards M, Heinemeier J, Sveinbjornsdottir AE, Bennike P. 45.  2007. Coast-inland mobility and diet in the Danish Mesolithic and Neolithic: evidence from stable isotope values of humans and dogs. J. Archaeol. Sci. 34:2125–50 [Google Scholar]
  46. Fry B. 46.  2006. Stable Isotope Ecology New York: Springer308
  47. Fuller BT, Fuller JL, Sage NE, Harris DA, O'Connell TC, Hedges REM. 47.  2004. Nitrogen balance and δ15N: why you're not what you eat during pregnancy. Rapid Commun. Mass Spectrom. 18:2889–96 [Google Scholar]
  48. Fuller BT, Fuller JL, Sage NE, Harris DA, O'Connell TC, Hedges REM. 48.  2005. Nitrogen balance and δ15N: why you're not what you eat during nutritional stress. Rapid Commun. Mass Spectrom. 19:2497–506 [Google Scholar]
  49. Gaye-Siessegger J, Focken U, Abel HJ, Becker K. 49.  2003. Feeding level and diet quality influence trophic shift of C and N isotopes in Nile tilapia (Oreochromis niloticus (L.)). Isot. Environ. Health Stud. 39:125–34 [Google Scholar]
  50. Godbout L, Trudel M, Irvine JR, Wood CC, Grove MJ. 50.  et al. 2010. Sulfur isotopes in otoliths allow discrimination of anadromous and non-anadromous ecotypes of sockeye salmon (Oncorhynchus nerka). Environ. Biol. Fishes 89:521–32 [Google Scholar]
  51. Gonzalez-Martin I, Perez CG, Mendez JH, Gonzalez CS. 51.  2001. Differentiation of dietary regimene of Iberian swine by means of isotopic analysis of carbon and sulphur in hepatic tissue. Meat Sci. 58:25–30 [Google Scholar]
  52. Haley S. 52.  2013. Sugar and sweeteners outlook. Outlook No. SSSM-293 Washington, DC: US Dep. Agric. Electron. Outlook Rep. Econ. Res. Serv.
  53. Hare PE, Fogel ML, Stafford TW, Mitchell AD, Hoering TC. 53.  1991. The isotopic composition of carbon and nitrogen in individual amino acids isolated from modern and fossil proteins. J. Archaeolog. Sci. 18:277–92 [Google Scholar]
  54. Hartman G. 54.  2011. Are elevated δ15N values in herbivores in hot and arid environments caused by diet or animal physiology?. Funct. Ecol. 25:122–31 [Google Scholar]
  55. Hatch KA, Crawford MA, Kunz AW, Thomsen SR, Eggett DL. 55.  et al. 2006. An objective means of diagnosing anorexia nervosa and bulimia nervosa using N-15/N-14 and C-13/C-12 ratios in hair. Rapid Commun. Mass Spectrom. 20:3367–73 [Google Scholar]
  56. Hobson KA, Atwell L, Wassenaar LI. 56.  1999. Influence of drinking water and diet on the stable-hydrogen isotope ratios of animal tissues. PNAS 96:8003–6 [Google Scholar]
  57. Hobson KA, Clark RG. 57.  1992. Assessing avian diets using stable isotopes II. Factors influencing diet-tissue fractionation. Condor 94:189–97 [Google Scholar]
  58. Hobson KA, Wassenaar LI. 58.  1997. Linking breeding and wintering grounds of neotropical migrant songbirds using stable hydrogen isotopic analysis of feathers. Oecologia 109:142–48 [Google Scholar]
  59. Hobson KA, Wassenaar LI. 59.  2008. Tracking Animal Migration with Stable Isotopes Amsterdam: Academic
  60. Hobson KA, Wassenaar LI, Taylor OR. 60.  1999. Stable isotopes δD and δ13C are geographic indicators of natal origins of monarch butterflies in eastern North America. Oecologia 120:397–404 [Google Scholar]
  61. Hobson KA, Welch HE. 61.  1992. Determination of trophic relationships within a high Arctic marine food web using delta-C-13 and delta-N-15 analysis. Mar. Ecol.-Prog. Ser. 84:9–18 [Google Scholar]
  62. Hoefs J. 62.  2004. Stable Isotope Geochemistry Berlin: Springer-Verlag
  63. Huelsemann F, Flenker U, Koehler K, Schaenzer W. 63.  2009. Effect of a controlled dietary change on carbon and nitrogen stable isotope ratios of human hair. Rapid Commun. Mass Spectrom. 23:2448–54 [Google Scholar]
  64. Huelsemann F, Koehler K, Braun H, Schaenzer W, Flenker U. 64.  2013. Human dietary delta N-15 intake: representative data for principle food items. Am. J. Phys. Anthropol. 152:58–66 [Google Scholar]
  65. Jahren A, Saudek C, Yeung E, Kao W, Kraft R, Caballero B. 65.  2006. An isotopic method for quantifying sweeteners derived from corn and sugar cane. Am. J. Clin. Nutr. 84:1380–84 [Google Scholar]
  66. Jahren AH, Bostic JN, Davy BM. 66.  2014. The potential for a carbon stable isotope biomarker of dietary sugar intake. J. Anal. Atomic Spectrom. 29:795–816 [Google Scholar]
  67. Jahren AH, Kraft RA. 67.  2008. Carbon and nitrogen stable isotopes in fast food: signatures of corn and confinement. PNAS 105:17855–60 [Google Scholar]
  68. Jarnum S, Jensen KB. 68.  1972. Plasma protein turnover (albumin, transferrin, IgG, IgM) in Menetrier's disease (giant hypertrophic gastritis): evidence of non-selective protein loss. Gut 13:128–37 [Google Scholar]
  69. Jenab M, Slimani N, Bictash M, Ferrari P, Bingham SA. 69.  2009. Biomarkers in nutritional epidemiology: applications, needs and new horizons. Hum. Genet. 125:507–25 [Google Scholar]
  70. Kipnis V, Subar AF, Midthune D, Freedman LS, Ballard-Barbash R. 70.  et al. 2003. Structure of dietary measurement error: results of the OPEN biomarker study. Am. J. Epidemiol. 158:14–21 [Google Scholar]
  71. Klimentidis YC, Lemas DJ, Wiener HH, O'Brien DM, Havel PJ. 71.  et al. 2014. CDKAL1 and HHEX are associated with type 2 diabetes-related traits among Yup'ik people. J. Diabetes 6:251–59 [Google Scholar]
  72. Koch PL. 72.  2007. Isotopic study of the biology of modern and fossil vertebrates. Stable Isotopes in Ecology and Environmental Science R Michener, K Lajtha 99–154 Malden, MA: Blackwell [Google Scholar]
  73. Kraeer K, Arneson LS, MacAvoy SE. 73.  2014. The intraspecies relationship between tissue turnover and metabolic rate in rats. Ecol. Res. 29:937–47 [Google Scholar]
  74. Kraft RA, Jahren AH, Saudek CD. 74.  2008. Clinical-scale investigation of stable isotopes in human blood: δ13N and δ15N from 406 patients at the Johns Hopkins Medical Institutions. Rapid Commun. Mass Spectrom. 22:3683–92 [Google Scholar]
  75. Krouse H, Herbert M. 75.  1988. Sulphur and carbon isotope studies of food webs. Diet and Subsistence: Current Archaeological Perspectives B Kennedy, G LeMoine 315–22 Calgary: Univ. Calg. Archaeol. Assoc. [Google Scholar]
  76. Kuhnle GG, Joosen AM, Kneale CJ, O'Connell TC. 76.  2012. Carbon and nitrogen isotopic ratios of urine and faeces as novel nutritional biomarkers of meat and fish intake. Eur. J. Clin. Nutr. 52:389–95 [Google Scholar]
  77. Kuhnle GGC. 77.  2012. Nutritional biomarkers for objective dietary assessment. J. Sci. Food Agric. 92:1145–49 [Google Scholar]
  78. Kwak TJ, Zedler JB. 78.  1997. Food web analysis of southern California coastal wetlands using multiple stable isotopes. Oecologia 110:262–77 [Google Scholar]
  79. Lee-Thorp JA. 79.  2008. On isotopes and old bones. Archaeometry 50:925–50 [Google Scholar]
  80. Lee TN, Buck CL, Barnes BM, O'Brien DM. 80.  2012. A test of alternative models for increased tissue nitrogen isotope ratios during fasting in hibernating arctic ground squirrels. J. Exp. Biol. 215:3354–61 [Google Scholar]
  81. Lemas D, Klimentidis Y, Wiener H, O'Brien D, Hopkins S. 81.  et al. 2013. Obesity polymorphisms identified in genome-wide association studies interact with n-3 polyunsaturated fatty acid intake and modify the genetic association with adiposity phenotypes in Yup'ik people. Genes Nutr. 8:495–505 [Google Scholar]
  82. Lemas DJ, Wiener HW, O'Brien DM, Hopkins S, Stanhope KL. 82.  et al. 2012. Genetic polymorphisms in carnitine palmitoyltransferase 1A gene are associated with variation in body composition and fasting lipid traits in Yup'ik Eskimos. J. Lipid Res. 53:175–84 [Google Scholar]
  83. Macko SA, Engel MH, Andrusevich V, Lubec G, O'Connell TC, Hedges REM. 83.  1999. Documenting the diet in ancient human populations through stable isotope analysis of hair. Philos. Trans. R. Soc. B 354:65–75 [Google Scholar]
  84. Makhoul Z, Kristal AR, Gulati R, Luick B, Bersamin A. 84.  et al. 2010. Associations of very high intakes of eicosapentaenoic and docosahexaenoic acids with biomarkers of chronic disease risk among Yup'ik Eskimos. Am. J. Clin. Nutr. 91:777–85 [Google Scholar]
  85. McCutchan JH Jr, Lewis WM Jr, Kendall C, McGrath CC. 85.  2003. Variation in trophic shift for stable isotope ratios of carbon, nitrogen, and sulfur. Oikos 102:378–90 [Google Scholar]
  86. McKinney C, McCrea J, Epstein S, Allen H, Urey H. 86.  1950. Improvements in mass spectrometers for the measurement of small differences in isotope abundance ratios. Rev. Sci. Instrum. 21:724–30 [Google Scholar]
  87. McMahon KW, Fogel ML, Elsdon TS, Thorrold SR. 87.  2010. Carbon isotope fractionation of amino acids in fish muscle reflects biosynthesis and isotopic routing from dietary protein. J. Anim. Ecol. 79:1132–41 [Google Scholar]
  88. Meier-Augenstein W. 88.  2010. Stable Isotope Forensics: An Introduction to the Forensic Application of Stable Isotope Analysis Chichester, UK: Wiley-Blackwell
  89. Mekota AM, Grupe G, Ufer S, Cuntz U. 89.  2006. Serial analysis of stable nitrogen and carbon isotopes in hair: monitoring starvation and recovery phases of patients suffering from anorexia nervosa. Rapid Commun. Mass Spectrom. 20:1604–10 [Google Scholar]
  90. Minagawa M. 90.  1992. Reconstruction of human diet from δ13N and δ15N in contemporary Japanese hair—a stochastic method for estimating multisource contribution by double isotopic tracers. Appl. Geochem. 7:145–58 [Google Scholar]
  91. Minagawa M, Wada E. 91.  1984. Stepwise enrichment of 15N along food chains: further evidence and the relations between δ15N and animal age. Geochim. Cosmochim. Acta 48:1135–40 [Google Scholar]
  92. Mook WG, Bommerson JC, Staverman WH. 92.  1974. Carbon isotope fractionation between dissolved bicarbonate and gaseous carbon dioxide. Earth Planetary Sci. Lett. 22:169–76 [Google Scholar]
  93. Muccio Z, Jackson GP. 93.  2009. Isotope ratio mass spectrometry. Analyst 134:213–22 [Google Scholar]
  94. Nakamura K, Schoeller DA, Winkler FJ, Schmidt HL. 94.  1982. Geographical variations in the carbon isotope composition of the diet and hair in contemporary man. Biomed. Mass Spectrom. 9:390–94 [Google Scholar]
  95. Nardoto GB, Silva S, Kendall C, Ehleringer JR, Chesson LA. 95.  et al. 2006. Geographical patterns of human diet derived from stable-isotope analysis of fingernails. Am. J. Phys. Anthropol. 131:137–46 [Google Scholar]
  96. Nash S, Kristal A, Bersamin A, Choy K, Hopkins S. 96.  et al. 2014. Isotopic estimates of sugar intake are related to chronic disease risk factors but not obesity in an Alaska native (Yup'ik) study population. Eur. J. Clin. Nutr. 68:91–96 [Google Scholar]
  97. Nash S, Kristal A, Bersamin A, Hopkins S, Boyer B, O'Brien D. 97.  2013. Carbon and nitrogen isotope ratios predict intake of sweeteners in a Yup'ik study population. J. Nutr. 143:161–65 [Google Scholar]
  98. Nash SH, Bersamin A, Kristal AR, Hopkins SE, Church RS. 98.  et al. 2012. Stable nitrogen and carbon isotope ratios indicate traditional and market food intake in an indigenous circumpolar population. J. Nutr. 142:84–90 [Google Scholar]
  99. Nash SH, Kristal AR, Boyer BB, King IB, Metzgar JS, O'Brien DM. 99.  2009. Relation between stable isotope ratios in human red blood cells and hair: implications for using the nitrogen isotope ratio of hair as a biomarker of eicosapentaenoic acid and docosahexaenoic acid. Am. J. Clin. Nutr. 90:1642–47 [Google Scholar]
  100. Nash SH, Kristal AR, Hopkins SE, Boyer BB, O'Brien DM. 100.  2014. Stable isotope models of sugar intake using hair, red blood cells, and plasma, but not fasting plasma glucose, predict sugar intake in a Yup'ik study population. J. Nutr. 144:75–80 [Google Scholar]
  101. O'Brien DM, Kristal AR, Jeannet MA, Wilkinson MJ, Bersamin A, Luick B. 101.  2009. Red blood cell δ15N: a novel biomarker of dietary eicosapentaenoic acid and docosahexaenoic acid intake. Am. J. Clin. Nutr. 89:913–19 [Google Scholar]
  102. O'Brien DM, Kristal AR, Nash SH, Hopkins SE, Luick BR. 102.  et al. 2014. A stable isotope biomarker of marine food intake captures associations between n-3 fatty acid intake and chronic disease risk in a Yup'ik study population, and detects new associations with blood pressure and adiponectin. J. Nutr. 144:706–13 [Google Scholar]
  103. O'Brien DM, Wooller MJ. 103.  2007. Tracking human travel using stable oxygen and hydrogen isotope analyses of hair and urine. Rapid Commun. Mass Spectrom. 21:2422–30 [Google Scholar]
  104. O'Connell TC, Hedges REM. 104.  1999. Investigations into the effect of diet on modern human hair isotopic values. Am. J. Phys. Anthropol. 108:409–25 [Google Scholar]
  105. O'Connell TC, Hedges REM, Healey MA, Simpson AHRW. 105.  2001. Isotopic comparison of hair, nail and bone: modern analyses. J. Archaeol. Sci. 28:1247–55 [Google Scholar]
  106. O'Connell TC, Kneale CJ, Tasevska N, Kuhnle GG. 106.  2012. The diet-body offset in human nitrogen isotopic values: a controlled dietary study. Am. J. Phys. Anthropol. 149:426–34 [Google Scholar]
  107. O'Leary MH. 107.  1988. Carbon isotopes in photosynthesis. BioScience 38:328–36 [Google Scholar]
  108. Ocke MC, Kaaks RJ. 108.  1997. Biochemical markers as additional measurements in dietary validity studies: application of the method of triads with examples from the European Prospective Investigation into Cancer and Nutrition. Am. J. Clin. Nutr. 65:1240–45S [Google Scholar]
  109. Ogden LJE, Hobson KA, Lank DB. 109.  2004. Blood isotopic (δ13N and δ15N) turnover and diet-tissue fractionation factors in captive Dunlin (Calidris alpina pacifica). Auk 121:170–77 [Google Scholar]
  110. Oppel S, Federer RN, O'Brien DM, Powell AN, Hollmen TE. 110.  2010. Effects of lipid extraction on stable isotope ratios in avian egg yolk: Is arithmetic correction a reliable alternative?. Auk 127:72–78 [Google Scholar]
  111. Passey BH, Robinson TF, Ayliffe LK, Cerling TE, Sponheimer M. 111.  et al. 2005. Carbon isotope fractionation between diet, breath CO2, and bioapatite in different mammals. J. Archaeol. Sci. 32:1459–70 [Google Scholar]
  112. Patel PS, Cooper AJM, O'Connell TC, Kuhnle GGC, Kneale CK. 112.  et al. 2014. Serum carbon and nitrogen stable isotopes as potential biomarkers of dietary intake and their relation with incident type 2 diabetes: the EPIC-Norfolk study. Am. J. Clin. Nutr. 100:708–18 [Google Scholar]
  113. Perriello G, Jorde R, Nurjhan N, Stumvoll M, Dailey G. 113.  et al. 1995. Estimation of glucose-alanine-lactate-glutamine cycles in postabsorptive humans: role of skeletal muscle. Am. J. Physiol. 269:E443–50 [Google Scholar]
  114. Peterson BJ, Fry B. 114.  1987. Stable isotopes in ecosystem studies. Annu. Rev. Ecol. Syst. 18:293–320 [Google Scholar]
  115. Petzke KJ, Boeing H, Klaus S, Metges CC. 115.  2005. Carbon and nitrogen stable isotopic composition of hair protein and amino acids can be used as biomarkers for animal-derived dietary protein intake in humans. J. Nutr. 135:1515–20 [Google Scholar]
  116. Petzke KJ, Boeing H, Metges CC. 116.  2005. Choice of dietary protein of vegetarians and omnivores is reflected in their hair protein 13C and 15N abundance. Rapid Commun. Mass Spectrom. 19:1392–400 [Google Scholar]
  117. Petzke KJ, Feist T, Fleig WE, Metges CC. 117.  2006. Nitrogen isotopic composition in hair protein is different in liver cirrhotic patients. Rapid Commun. Mass Spectrom. 20:2973–78 [Google Scholar]
  118. Petzke KJ, Fuller BT, Metges CC. 118.  2010. Advances in natural stable isotope ratio analysis of human hair to determine nutritional and metabolic status. Curr. Opin. Clin. Nutr. Metab. Care 13:532–40 [Google Scholar]
  119. Petzke KJ, Lemke S. 119.  2009. Hair protein and amino acid C-13 and N-15 abundances take more than 4 weeks to clearly prove influences of animal protein intake in young women with a habitual daily protein consumption of more than 1 g per kg body weight. Rapid Commun. Mass Spectrom. 23:2411–20 [Google Scholar]
  120. Phillips DL, Eldridge PM. 120.  2006. Estimating the timing of diet shifts using stable isotopes. Oecologia 147:195–203 [Google Scholar]
  121. Pikosky MA, Gaine PC, Martin WF, Grabarz KC, Ferrando AA. 121.  et al. 2006. Aerobic exercise training increases skeletal muscle protein turnover in healthy adults at rest. J. Nutr. 136:379–83 [Google Scholar]
  122. Podlesak DW, Bowen GJ, O'Grady S, Cerling TE, Ehleringer JR. 122.  2012. delta H-2 and delta O-18 of human body water: a GIS model to distinguish residents from non-residents in the contiguous USA. Isot. Environ. Health Stud. 48:259–79 [Google Scholar]
  123. Podlesak DW, McWilliams SR. 123.  2006. Metabolic routing of dietary nutrients in birds: effects of diet quality and macronutrient composition revealed using stable isotopes. Physiol. Biochem. Zool. 79:534–49 [Google Scholar]
  124. Post DM, Layman CA, Arrington DA, Takimoto G, Quattrochi J, Montana CG. 124.  2007. Getting to the fat of the matter: models, methods and assumptions for dealing with lipids in stable isotope analyses. Oecologia 152:179–89 [Google Scholar]
  125. Prentice RL, Mossavar-Rahmani Y, Huang Y, Van Horn L, Beresford SA. 125.  et al. 2011. Evaluation and comparison of food records, recalls, and frequencies for energy and protein assessment by using recovery biomarkers. Am. J. Epidemiol. 174:591–603 [Google Scholar]
  126. Prentice RL, Pettinger M, Tinker LF, Huang Y, Thomson CA. 126.  et al. 2013. Regression calibration in nutritional epidemiology: example of fat density and total energy in relationship to postmenopausal breast cancer. Am. J. Epidemiol. 178:1663–72 [Google Scholar]
  127. Prentice RL, Shaw PA, Bingham SA, Beresford SAA, Caan B. 127.  et al. 2009. Biomarker-calibrated energy and protein consumption and increased cancer risk among postmenopausal women. Am. J. Epidemiol. 169:977–89 [Google Scholar]
  128. Prentice RL, Sugar E, Wang CY, Neuhouser M, Patterson R. 128.  2002. Research strategies and the use of nutrient biomarkers in studies of diet and chronic disease. Public Health Nutr. 5:977–84 [Google Scholar]
  129. Privat KL, O'Connell TC, Hedges REM. 129.  2007. The distinction between freshwater- and terrestrial-based diets: methodological concerns and archaeological applications of sulphur stable isotope analysis. J. Archaeol. Sci. 34:1197–204 [Google Scholar]
  130. Reese AC, Fradet V, Witte JS. 130.  2009. Omega-3 fatty acids, genetic variants in COX-2 and prostate cancer. J. Nutrigenet. Nutrigenomics 2:149–58 [Google Scholar]
  131. Richards MP, Fuller BT, Sponheimer M, Robinson T, Ayliffe L. 131.  2003. Sulphur isotopes in palaeodietary studies: a review and results from a controlled feeding experiment. Int. J. Osteoarchaeol. 13:37–45 [Google Scholar]
  132. Richards MP, Jacobi R, Cook J, Pettitt PB, Stringer CB. 132.  2005. Isotope evidence for the intensive use of marine foods by Late Upper Palaeolithic humans. J. Hum. Evol. 49:390–94 [Google Scholar]
  133. Robbins CT, Felicetti LA, Sponheimer M. 133.  2005. The effect of dietary protein quality on nitrogen isotope discrimination in mammals and birds. Oecologia 144:534–40 [Google Scholar]
  134. Santamaria-Fernandez R, Martinez-Sierra JG, Marchante-Gayón JM, García-Alonso JI, Hearn R. 134.  2009. Measurement of longitudinal sulfur isotopic variations by laser ablation MC-ICP-MS in single human hair strands. Anal. Bioanal. Chem. 394:225–33 [Google Scholar]
  135. Schoeller DA. 135.  1999. Isotope fractionation: Why aren't we what we eat?. J. Archaeol. Sci. 26:667–73 [Google Scholar]
  136. Schoeller DA, Brown C, Nakamura K, Nakagawa A, Mazzeo RS. 136.  et al. 1984. Influence of metabolic fuel on the 13C/12C ratio of breath CO2. Biomed. Mass Spectrom. 11:557–61 [Google Scholar]
  137. Schoeller DA, Klein PD, Watkins JB, Heim T, MacLean WC Jr. 137.  1980. 13C abundances of nutrients and the effect of variations in 13C isotopic abundances of test meals formulated for 13CO2 breath tests. Am. J. Clin. Nutr. 33:2375–85 [Google Scholar]
  138. Schoeller DA, Minagawa M, Slater R, Kaplan IR. 138.  1986. Stable isotopes of carbon, nitrogen and hydrogen in the contemporary North American human food web. Ecol. Food Nutr. 18:159–70 [Google Scholar]
  139. Schoeller DA, Schneider JF, Solomons NW, Watkins JB, Klein PD. 139.  1977. Clinical diagnosis with the stable isotope 13C in CO2 breath tests: methodology and fundamental considerations. J. Lab. Clin. Med. 90:412–21 [Google Scholar]
  140. Sharp Z. 140.  2007. Stable Isotope Geochemistry Upper Saddle River, NJ: Pearson/Prentice Hall
  141. Steele KW, Daniel RM. 141.  1978. Fractionation of nitrogen isotopes by animals: a further complication to the use of variations in the natural abundance of 15N for tracer studies. J. Agric. Sci. 90:7–9 [Google Scholar]
  142. Subar AF, Kipnis V, Troiano RP, Midthune D, Schoeller DA. 142.  et al. 2003. Using intake biomarkers to evaluate the extent of dietary misreporting in a large sample of adults: the OPEN Study. Am. J. Epidemiol. 158:1–13 [Google Scholar]
  143. Sweeting CJ, Polunin NVC, Jennings S. 143.  2006. Effects of chemical lipid extraction and arithmetic lipid correction on stable isotope ratios of fish tissues. Rapid Commun. Mass Spectrom. 20:595–601 [Google Scholar]
  144. Tasevska N, Midthune D, Tinker L, Potischman N, Lampe JW. 144.  et al. 2014. Use of a urinary sugars biomarker to assess measurement error in self-reported sugars intake in the Nutrition and Physical Activity Assessment Study (NPAAS). Cancer Epidemiol. Biomarkers Prev. 23:2874–83 [Google Scholar]
  145. Tasevska N, Runswick SA, McTaggart A, Bingham SA. 145.  2005. Urinary sucrose and fructose as biomarkers for sugar consumption. Cancer Epidemiol. Biomarkers Prev. 14:1287–94 [Google Scholar]
  146. Tasevska N, Runswick SA, Welch AA, McTaggart A, Bingham SA. 146.  2009. Urinary sugars biomarker relates better to extrinsic than to intrinsic sugars intake in a metabolic study with volunteers consuming their normal diet. Eur. J. Clin. Nutr. 63:653–59 [Google Scholar]
  147. Tieszen LL, Boutton TW, Tesdahl KG, Slade NA. 147.  1983. Fractionation and turnover of stable isotopes in animal tissues: implications for δ13C analysis of diet. Oecologia 57:32–37 [Google Scholar]
  148. Trust BA, Fry B. 148.  1992. Stable sulfur isotopes in plants—a review. Plant Cell Environ. 15:1105–10 [Google Scholar]
  149. Tucker KL, Smith CE, Lai CQ, Ordovas JM. 149.  2013. Quantifying diet for nutrigenomic studies. Annu. Rev. Nutr. 33:349–71 [Google Scholar]
  150. Valenzuela LO, Chesson LA, O'Grady SP, Cerling TE, Ehleringer JR. 150.  2011. Spatial distributions of carbon, nitrogen and sulfur isotope ratios in human hair across the central United States. Rapid Commun. Mass Spectrom. 25:861–68 [Google Scholar]
  151. Van Der Merwe NJ, Vogel JC. 151.  1978. 13C Content of human collagen as a measure of prehistoric diet in woodland North America. Nature 276:815–16 [Google Scholar]
  152. Vitòria L, Otero N, Soler A, Canals À. 152.  2004. Fertilizer characterization: isotopic data (N, S, O, C, and Sr). Environ. Sci. Technol. 38:3254–62 [Google Scholar]
  153. Vogel JC, Van der Merwe NJ. 153.  1977. Isotopic evidence for early maize cultivation in New York State. Am. Antiquity 42:238–42 [Google Scholar]
  154. Voigt CC, Baier L, Speakman JR, Siemers BM. 154.  2008. Stable carbon isotopes in exhaled breath as tracers for dietary information in birds and mammals. J. Exp. Biol. 211:2233–38 [Google Scholar]
  155. Waterhouse C, Keilson J. 155.  1978. The contribution of glucose to alanine metabolism in man. J. Lab. Clin. Med. 92:803–12 [Google Scholar]
  156. Waterlow JC. 156.  2006. Protein Turnover Cambridge, MA: CABI Publ.
  157. Whigham LD, Butz DE, Johnson LK, Schoeller DA, Abbott DH. 157.  et al. 2014. Breath carbon stable isotope ratios identify changes in energy balance and substrate utilization in humans. Int. J. Obes. (Lond.) 38:1248–50 [Google Scholar]
  158. Wilkinson MJ, Yai Y, O'Brien DM. 158.  2007. Age-related variation in red blood cell stable isotope ratios (δ13C and δ15N) from two Yupik villages in Southwest Alaska: a pilot study.. Int. J. Circumpolar Health 66:31–41 [Google Scholar]
  159. Wolf N, Bowen GJ, del Rio CM. 159.  2011. The influence of drinking water on the δD and δ18O values of house sparrow plasma, blood and feathers. J. Exp. Biol. 214:98–103 [Google Scholar]
  160. Wolf N, Newsome SD, Fogel ML, del Rio CM. 160.  2012. An experimental exploration of the incorporation of hydrogen isotopes from dietary sources into avian tissues. J. Exp. Biol. 215:1915–22 [Google Scholar]
  161. Yeung EH, Saudek CD, Jahren AH, Kao WHL, Islas M. 161.  et al. 2010. Evaluation of a novel isotope biomarker for dietary consumption of sweets. Am. J. Epidemiol. 172:1045–52 [Google Scholar]
/content/journals/10.1146/annurev-nutr-071714-034511
Loading
Stable Isotope Ratios as Biomarkers of Diet for Health Research
Annual Review of Nutrition 35, 565 (2015); https://doi.org/10.1146/annurev-nutr-071714-034511
/content/journals/10.1146/annurev-nutr-071714-034511
/content/journals/10.1146/annurev-nutr-071714-034511
Loading

Data & Media loading...

  • Article Type: Review Article

Most Cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error