Abstract
Purpose
Diet-related diseases are advancing as the leading cause of death globally. As self-reporting of diet by patients can be associated with errors, stable isotopes of human tissues can be used to diagnose diseases, understand physiology, and detect change in diet. This study investigates the effect of type and amount of food on the nitrogen and carbon concentration (Nconc and Cconc) and isotopic composition (δ15N and δ13C) in human scalp hair and fingernails.
Methods
A total of 100 residents participated in the study whereas only 74 individuals provided complete diet history. Sixty-six food items majorly available to them were also collected. The Nconc, Cconc, δ15N and δ13C values of human hair, nails and food items were determined.
Results
The Nconc, Cconc, δ15N and δ13C values between plant-sourced and animal-sourced food items, as well as human hair and nail tissue were significantly different (p < 0.05). The δ15N value of human tissues was distinct between lacto-vegetarians and omnivores by 0.9‰. The δ15N and δ13C values of human tissues increased by 0.4–0.5‰ with every 5% increase in the consumption of animal protein.
Conclusions
The study helps to demarcate lacto-vegetarians from omnivores, and estimate the percentage of animal protein in diet based on the dual isotope values of human tissues. It also acts as a reference to determine isotopic composition of hair tissue provided the isotope value of nail tissue is known and vice versa.
Similar content being viewed by others
Data availability
The Research Data described in the manuscript is freely available in the Table 1 in manuscript, and Supplementary Table 1 in Supporting Information. Any other data described in the manuscript, code book, and analytic code will be made available upon request by the corresponding author.
References
Manual A (2011) Dietary guidelines for Indians. Nat Inst Nutr 2:89–117
World Health Organization (2022) Noncommunicable diseases. World Health Organization. https://www.who.int/news-room/fact-sheets/detail/noncommunicable-diseases. Accessed 20 Dec 2022
Afshin A, Sur PJ, Fay KA et al (2019) Health effects of dietary risks in 195 countries, 1990–2017: a systematic analysis for the Global Burden of Disease Study 2017. Lancet 393:1958–1972. https://doi.org/10.1016/S0140-6736(19)30041-8
Reitsema LJ (2013) Beyond diet reconstruction: stable isotope applications to human physiology, health, and nutrition. Am J Hum Biol 25:445–456. https://doi.org/10.1002/ajhb.22398
O’Connell TC, Kneale CJ, Tasevska N, Kuhnle GGC (2012) The diet-body offset in human nitrogen isotopic values: a controlled dietary study. Am J Phys Anthropol 149:426–434. https://doi.org/10.1002/ajpa.22140
O’Brien DM, Sagi-Kiss V, Palma-Duran SA et al (2022) An evaluation of the serum carbon isotope ratio as a candidate predictive biomarker of the dietary animal protein ratio (animal protein/total protein) in a 15-day controlled feeding study of US adults. Am J Clin Nutr 115:1134–1143. https://doi.org/10.1093/ajcn/nqac004
Dierkes J, Dietrich S, Abraham K et al (2022) Stable isotope ratios of nitrogen and carbon as biomarkers of a vegan diet. Eur J Nutr. https://doi.org/10.1007/s00394-022-02992-
Ehleringer JR, Covarrubias Avalos S, Tipple BJ et al (2020) Stable isotopes in hair reveal dietary protein sources with links to socioeconomic status and health. Proc Natl Acad Sci 117:20044–20051. https://doi.org/10.1073/pnas.1914087117
Petzke KJ, Fuller BT, Metges CC (2010) Advances in natural stable isotope ratio analysis of human hair to determine nutritional and metabolic status. Curr Opin Clin Nutr Metab Care 13:532–540. https://doi.org/10.1097/MCO.0b013e32833c3c84
Kuhnle GGC, Joosen AMCP, Kneale CJ, O’Connell TC (2013) Carbon and nitrogen isotopic ratios of urine and faeces as novel nutritional biomarkers of meat and fish intake. Eur J Nutr 52:389–395. https://doi.org/10.1007/s00394-012-0328-2
Hedges R, Rush E, Aalbersberg W (2009) Correspondence between human diet, body composition and stable isotopic composition of hair and breath in Fijian villagers. Isotopes Environ Health Stud 45:1–17. https://doi.org/10.1080/10256010802522010
O’Brien DM (2015) Stable isotope ratios as biomarkers of diet for health research. Annu Rev Nutr 35:565–594. https://doi.org/10.1146/annurev-nutr-071714-034511
Lacombe RJS, Bazinet RP (2021) Natural abundance carbon isotope ratio analysis and its application in the study of diet and metabolism. Nutr Rev 79:869–888. https://doi.org/10.1093/nutrit/nuaa109
Hatch KA, Crawford MA, Kunz AW et al (2006) An objective means of diagnosing anorexia nervosa and bulimia nervosa using 15N/14N and 13C/12C ratios in hair. Rapid Commun Mass Spectrom Int J Devoted Rapid Dissem Up-to-the-Minute Res Mass Spectrom 20:3367–3373. https://doi.org/10.1002/rcm.2740
Mekota A-M, Grupe G, Ufer S, Cuntz U (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 Int J Devoted Rapid Dissem Up-to-the-Minute Res Mass Spectrom 20:1604–1610. https://doi.org/10.1002/rcm.2477
Fuller BT, Fuller JL, Sage NE et al (2005) Nitrogen balance and ?15N: why you’re not what you eat during nutritional stress. Rapid Commun Mass Spectrom Int J Devoted Rapid Dissem Up-to-the-Minute Res Mass Spectrom 19:2497–2506. https://doi.org/10.1002/rcm.2090
Neuberger FM, Jopp E, Graw M et al (2013) Signs of malnutrition and starvation-reconstruction of nutritional life histories by serial isotopic analyses of hair. Forensic Sci Int 226:22–32. https://doi.org/10.1016/j.forsciint.2012.10.037
Eerkens JW, Hull B, Goodman J et al (2017) Stable C and N isotope analysis of hair suggest undernourishment as a factor in the death of a mummified girl from late 19th century San Francisco, CA. PLoS ONE 12:e0184921. https://doi.org/10.1371/journal.pone.0184921
Waters-Rist AL, Katzenberg MA (2010) The effect of growth on stable nitrogen isotope ratios in subadult bone collagen. Int J Osteoarchaeol 20:172–191. https://doi.org/10.1002/oa.1017
Fuller BT, Fuller JL, Sage NE et al (2004) Nitrogen balance and δ15N: why you’re not what you eat during pregnancy. Rapid Commun Mass SPECTROM 18:2889–2896. https://doi.org/10.1002/rcm.1708
Petzke KJ, Feist T, Fleig WE, Metges CC (2006) Nitrogen isotopic composition in hair protein is different in liver cirrhotic patients. Rapid Commun Mass Spectrom Int J Devoted Rapid Dissem Up-to-the-Minute Res Mass Spectrom 20:2973–2978. https://doi.org/10.1002/rcm.2695
Petzke KJ, Boeing H, Metges CC (2005) Choice of dietary protein of vegetarians and omnivores is reflected in their hair protein 13C and 15N abundance. Rapid Commun Mass Spectrom Int J Devoted Rapid Dissem Up-to-the-Minute Res Mass Spectrom 19:1392–1400. https://doi.org/10.1002/rcm.1925
O’Connell TC, Hedges REM (1999) Investigations into the effect of diet on modern human hair isotopic values. Am J Phys Anthropol Off Publ Am Assoc Phys Anthropol 108:409–425. https://doi.org/10.1002/(SICI)1096-8644(199904)108:4%3c409::AID-AJPA3%3e3.0.CO;2-E
Ishige N (2008) The dietary culture of Asia. Asia Society. https://asiasociety.org/blog/asia/dietary-culture-asia. Accessed 20 Dec 2022
Hülsemann F, Lehn C, Schneiders S et al (2015) Global spatial distributions of nitrogen and carbon stable isotope ratios of modern human hair. Rapid Commun Mass Spectrom 29:2111–2121. https://doi.org/10.1002/rcm.7370
Green R, Milner J, Joy EJM et al (2016) Dietary patterns in India: a systematic review. Br J Nutr 116:142–148. https://doi.org/10.1017/S0007114516001598
Venkatesan P, Prakash SS, Ramasamy J (2022) Regional differences in dietary pattern in India and its relation to nutrition related outcomes. https://doi.org/10.21203/rs.3.rs-1476395/v2
Samantaray S, Sanyal P (2022) Sources and fate of organic matter in a hypersaline lagoon: a study based on stable isotopes from the Pulicat lagoon. India Sci Total Environ 807:150617. https://doi.org/10.1016/j.scitotenv.2021.150617
Samantaray S, Sanyal P (2023) Effect of salinity on the preservation of plant-derived n-alkyl compounds in the terrestrial-aquatic interface. Org Geochem 183:104653. https://doi.org/10.1016/j.orggeochem.2023.104653
Mora A (2022) Stable carbon and nitrogen isotope analysis of archaeological human hair: Reconstructing diet and health of ancient individuals. J Archaeol Sci Rep 43:103439. https://doi.org/10.1016/j.jasrep.2022.103439
Longvah T, Ananthan R, Bhaskarachary K et al (2017) Indian food composition tables. National Institute of Nutrition, Indian Council of Medical Research Hyderabad. ISBN: 978-93-5267-677-4
Global Alliance for Improved Nutrition (GAIN) (2020) Animal-source foods for human and planetary health: GAIN's position. Global Alliance for Improved Nutrition (GAIN). Briefing Paper Series #2, Geneva, Switzerland. https://doi.org/10.36072/bp.2
O’Connell TC, Hedges REM, Healey MA, Simpson AHRW (2001) Isotopic comparison of hair, nail and bone: modern analyses. J Archaeol Sci 28:1247–1255. https://doi.org/10.1006/jasc.2001.0698
Suzuki T, Watanabe S, Matsuo N (1989) Comparison of hair with nail as index media for biological monitoring of mercury. Sangyo Igaku 31:235–238. https://doi.org/10.1539/joh1959.31.235
Meier-Augenstein W, Kemp HF (2012) Stable isotope analysis: hair and nails. Wiley encyclopedia of forensic science. Wiley, New York
Huelsemann F, Flenker U, Koehler K, Schaenzer W (2009) Effect of a controlled dietary change on carbon and nitrogen stable isotope ratios of human hair. Rapid Commun Mass Spectrom Int J Devoted Rapid Dissem Up-to-the-Minute Res Mass Spectrom 23:2448–2454. https://doi.org/10.1002/rcm.4039
Dittmar M, Dindorf W, Banerjee A (2008) Organic elemental composition in fingernail plates varies between sexes and changes with increasing age in healthy humans. Gerontology 54:100–105. https://doi.org/10.1159/000128269
Thompson AH, Chesson LA, Podlesak DW et al (2010) Stable isotope analysis of modern human hair collected from Asia (China, India, Mongolia, and Pakistan). Am J Phys Anthropol Off Publ Am Assoc Phys Anthropol 141:440–451. https://doi.org/10.1002/ajpa.21162
Buchardt B, Bunch V, Helin P (2007) Fingernails and diet: stable isotope signatures of a marine hunting community from modern Uummannaq, North Greenland. Chem Geol 244:316–329. https://doi.org/10.1016/j.chemgeo.2007.06.022
Bol R, Pflieger C (2002) Stable isotope (13C, 15N and 34S) analysis of the hair of modern humans and their domestic animals. Rapid Commun Mass Spectrom 16:2195–2200. https://doi.org/10.1002/rcm.706
DeNiro MJ, Epstein S (1981) Influence of diet on the distribution of nitrogen isotopes in animals. Geochim Cosmochim Acta 45:341–351. https://doi.org/10.1016/0016-7037(81)90244-1
Rose WC, Wixom RL (1955) The amino acid requirements of man XVI. The role of the nitrogen intake. J Biol Chem 2:997–1004. https://doi.org/10.1016/S0021-9258(18)65963-0
Schoeller DA, Minagawa M, Slater R, Kaplan IR (1986) Stable isotopes of carbon, nitrogen and hydrogen in the contemporary North American human food web. Ecol Food Nutr 18:159–170. https://doi.org/10.1080/03670244.1986.9990922
Kiela PR, Ghishan FK (2016) Physiology of intestinal absorption and secretion. Best Pract Res Clin Gastroenterol 30:145–159. https://doi.org/10.1016/j.bpg.2016.02.007
NIDDK (2017) Your digestive system and how it works. National Institute of Diabetes and Digestive and Kidney Diseases. https://www.niddk.nih.gov/health-information/digestive-diseases/digestive-system-how-it-works. Accessed 11 Nov 2022
Liu X, Wang H, Liang X, Roberts MS (2017) Chapter 30-hepatic metabolism in liver health and disease. In: Muriel P (ed) Liver pathophysiology therapies and antioxidants. Academic Press, Boston, pp 391–399
Litwack G (2017) Human biochemistry. Academic Press, New York
Libretexts (2022) 25.6: biosynthesis of nonessential amino acids. Chemistry LibreTexts. https://chem.libretexts.org/Bookshelves/Introductory_Chemistry/Map%3A_Fundamentals_of_General_Organic_and_Biological_Chemistry_(McMurry_et_al.)/25%3A_Protein_and_Amino_Acid_Metabolism/25.06%3A_Biosynthesis_of_Nonessential_Amino_Acids. Accessed 24 Nov 2022
Mohiuddin SS, Khattar D (2022) Biochemistry, ammonia. In: StatPearls [Internet]. StatPearls Publishing, Treasure Island
Naito YI, Morita A, Natsuhara K et al (2015) Association of protein intakes and variation of diet-scalp hair nitrogen isotopic discrimination factor in Papua New Guinea highlanders. Am J Phys Anthropol 158:359–370. https://doi.org/10.1002/ajpa.22798
Yoshinaga J, Komatsuda S, Fujita R et al (2021) Carbon and nitrogen stable isotope ratios of diet of the Japanese and diet–hair offset values. Isotopes Environ Health Stud 57:563–575. https://doi.org/10.1080/10256016.2021.1990276
Kuhnle GGC (2022) Time to wake up sleeping beauty: stable isotope ratios. J Nutr. https://doi.org/10.1016/j.tjnut.2022.10.013
Acknowledgements
GA is grateful to University Grants Commission (UGC) for PhD scholarship (Award No. 190520711319; 08-01-2020), Manoj Jakhar for his assistance in sample collection, Mahesh Ghosh for instrument support, IISER-K Mess Manager for providing data from server, Rohan Agrawal for help in computational analysis and the study participants for providing their samples for the study. PS acknowledges the support from Science and Engineering Research Board (SERB) under Department of Science and Technology (DST), Government of India (Project No. EMR/2017/003673) for the IRMS instrument procurement.
Funding
The IRMS instrument procurement was supported by Science and Engineering Research Board (SERB) under Department of Science and Technology (DST), Government of India (Project No. EMR/2017/003673). GA is supported by PhD fellowship programme of University Grants Commission (UGC) (Award No.: 190520711319; 08-01-2020).
Author information
Authors and Affiliations
Contributions
GA: Conceptualization, Formal analysis, Investigation, Visualization, Writing—Original Draft PS: Resources, Writing—Review and Editing, Supervision.
Corresponding author
Ethics declarations
Conflict of interest
The authors have no competing interests to declare that are relevant to the content of this article.
Ethical standards
The human tissue sample collection protocol was approved by the Institutional Ethical Committee (IISER/IEC/2022/09) and the samples have therefore been collected by adherence to the approved ethical standards. Informed consent after explaining the research was taken from the study participants prior to human tissue collection.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Agrawal, G., Sanyal, P. Discerning animal-sourced food in diet using isotope analysis of human scalp hair and fingernails. Eur J Nutr 63, 409–423 (2024). https://doi.org/10.1007/s00394-023-03273-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00394-023-03273-y