Skip to main content
Springer Nature Link
Log in

Plasma elemental responses to red meat ingestion in healthy young males and the effect of cooking method

  • Original Contribution
  • Published:
European Journal of Nutrition Aims and scope Submit manuscript

Abstract

Purpose

Elemental deficiencies are highly prevalent and have a significant impact on health. However, clinical monitoring of plasma elemental responses to foods remains largely unexplored. Data from in vitro studies show that red meat (beef) is a highly bioavailable source of several key elements, but cooking method may influence this bioavailability. We therefore studied the postprandial responses to beef steak, and the effects of two different cooking methods, in healthy young males.

Methods

In a randomized cross-over controlled trial, healthy males (n = 12, 18–25 years) were fed a breakfast of beef steak (270 ± 20 g) in which the meat was either pan-fried (PF) or sous-vide (SV) cooked. Baseline and postprandial blood samples were collected and the plasma concentrations of 15 elements measured by inductively coupled plasma-mass spectrometry (ICP-MS).

Results

Concentrations of Fe and Zn changed after meal ingestion, with plasma Fe increasing (p < 0.001) and plasma Zn decreasing (p < 0.05) in response to both cooking methods. The only potential treatment effect was seen for Zn, where the postprandial area under the curve was lower in response to the SV meal (2965 ± 357) compared to the PF meal (3190 ± 310; p < 0.05).

Conclusions

This multi-element approach demonstrated postprandial responsiveness to a steak meal, and an effect of the cooking method used. This suggests the method would provide insight in future elemental metabolic studies to evaluate responses to meat-based meals, including longer-term interventions in more specifically defined cohorts to clearly establish the role of red meat as an important source of elements.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Explore related subjects

Discover the latest articles and news from researchers in related subjects, suggested using machine learning.

References

  1. Gupta UC, Gupta SC (2014) Sources and deficiency diseases of mineral nutrients in human health and nutrition: a review. Pedosphere 24(1):13–38. https://doi.org/10.1016/S1002-0160(13)60077-6

    Article  CAS  Google Scholar 

  2. Disease GBD, Injury I, Prevalence C (2016) Global, regional, and national incidence, prevalence, and years lived with disability for 310 diseases and injuries, 1990–2015: a systematic analysis for the Global Burden of Disease Study 2015. Lancet 388(10053):1545–1602. https://doi.org/10.1016/S0140-6736(16)31678-6

    Article  Google Scholar 

  3. Galan MG, Drago SR (2014) Food matrix and cooking process affect mineral bioaccessibility of enteral nutrition formulas. J Sci Food Agric 94(3):515–521. https://doi.org/10.1002/jsfa.6280

    Article  CAS  PubMed  Google Scholar 

  4. Gobbetti M, Rizzello CG, Di Cagno R, De Angelis M (2014) How the sourdough may affect the functional features of leavened baked goods. Food Microbiol 37:30–40. https://doi.org/10.1016/j.fm.2013.04.012

    Article  CAS  Google Scholar 

  5. Acosta A, Camilleri M (2014) Gastrointestinal morbidity in obesity. Ann N Y Acad Sci 1311:42–56. https://doi.org/10.1111/nyas.12385

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Britton E, McLaughlin JT (2013) Ageing and the gut. Proc Nutr Soc 72(1):173–177. https://doi.org/10.1017/S0029665112002807

    Article  Google Scholar 

  7. Lampe JW, Fredstrom SB, Slavin JL, Potter JD (1993) Sex differences in colonic function: a randomised trial. Gut 34(4):531–536

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Hambidge KM, Miller LV, Westcott JE, Sheng X, Krebs NF (2010) Zinc bioavailability and homeostasis. Am J Clin Nutr 91(5):1478S–1483S. https://doi.org/10.3945/ajcn.2010.28674I

    Article  CAS  Google Scholar 

  9. Hunt JR (2005) Dietary and physiological factors that affect the absorption and bioavailability of iron. Int J Vitam Nutr Res 75(6):375–384. https://doi.org/10.1024/0300-9831.75.6.375

    Article  CAS  Google Scholar 

  10. Bosscher D, Van Caillie-Bertrand M, Deelstra H (2001) Effect of thickening agents, based on soluble dietary fiber, on the availability of calcium, iron, and zinc from infant formulas. Nutrition 17(7–8):614–618

    Article  CAS  PubMed  Google Scholar 

  11. Promchan J, Shiowatana J (2005) A dynamic continuous-flow dialysis system with on-line electrothermal atomic-absorption spectrometric and pH measurements for in-vitro determination of iron bioavailability by simulated gastrointestinal digestion. Anal Bioanal Chem 382(6):1360–1367. https://doi.org/10.1007/s00216-005-3288-z

    Article  CAS  PubMed  Google Scholar 

  12. Chin D, Huebbe P, Frank J, Rimbach G, Pallauf K (2014) Curcumin may impair iron status when fed to mice for six months. Redox Biol 2:563–569. https://doi.org/10.1016/j.redox.2014.01.018

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Hunt JR (2003) Bioavailability of iron, zinc, and other trace minerals from vegetarian diets. Am J Clin Nutr 78(3 Suppl):633S–639S

    Article  CAS  PubMed  Google Scholar 

  14. Levander OA, Alfthan G, Arvilommi H, Gref CG, Huttunen JK, Kataja M, Koivistoinen P, Pikkarainen J (1983) Bioavailability of selenium to Finnish men as assessed by platelet glutathione peroxidase activity and other blood parameters. Am J Clin Nutr 37(6):887–897

    Article  CAS  Google Scholar 

  15. Hartman-Craven B, Christofides A, O’Connor DL, Zlotkin S (2009) Relative bioavailability of iron and folic acid from a new powdered supplement compared to a traditional tablet in pregnant women. BMC Pregnancy Childbirth 9:33. https://doi.org/10.1186/1471-2393-9-33

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Navarro M, Wood RJ (2003) Plasma changes in micronutrients following a multivitamin and mineral supplement in healthy adults. J Am Coll Nutr 22(2):124–132

    Article  CAS  PubMed  Google Scholar 

  17. Cabrera MC, Saadoun A (2014) An overview of the nutritional value of beef and lamb meat from South America. Meat Sci 98(3):435–444. https://doi.org/10.1016/j.meatsci.2014.06.033

    Article  CAS  PubMed  Google Scholar 

  18. McNeill S, Van Elswyk ME (2012) Red meat in global nutrition. Meat Sci 92(3):166–173. https://doi.org/10.1016/j.meatsci.2012.03.014

    Article  CAS  PubMed  Google Scholar 

  19. Sánchez del Pulgar J, Gázquez A, Ruiz-Carrascal J (2012) Physico-chemical, textural and structural characteristics of sous-vide cooked pork cheeks as affected by vacuum, cooking temperature, and cooking time. Meat Sci 90(3):828–835. https://doi.org/10.1016/j.meatsci.2011.11.024

    Article  CAS  PubMed  Google Scholar 

  20. Campo MM, Muela E, Olleta JL, Moreno LA, Santaliestra-Pasías AM, Mesana MI, Sañudo C (2013) Influence of cooking method on the nutrient composition of Spanish light lamb. J Food Compos Anal 31(2):185–190. https://doi.org/10.1016/j.jfca.2013.05.010

    Article  CAS  Google Scholar 

  21. Garmyn AJ, Hilton GG, Mateescu RG, Morgan JB, Reecy JM, Tait RG Jr, Beitz DC, Duan Q, Schoonmaker JP, Mayes MS, Drewnoski ME, Liu Q, VanOverbeke DL (2011) Estimation of relationships between mineral concentration and fatty acid composition of longissimus muscle and beef palatability traits. J Anim Sci 89(9):2849–2858. https://doi.org/10.2527/jas.2010-3497

    Article  CAS  PubMed  Google Scholar 

  22. Nikmaram P, Yarmand MS, Emamjomeh Z (2011) Effect of cooking methods on chemical composition, quality and cook loss of camel muscle (Longissimus dorsi) in comparison with veal. Afr J Biotechnol 10(51):10478–10483. https://doi.org/10.5897/AJB10.2534

    Article  CAS  Google Scholar 

  23. Kaur L, Maudens E, Haisman DR, Boland MJ, Singh H (2014) Microstructure and protein digestibility of beef: The effect of cooking conditions as used in stews and curries. LWT Food Sci Technol 55(2):612–620. https://doi.org/10.1016/j.lwt.2013.09.023

    Article  CAS  Google Scholar 

  24. Yarmand MS, Nikmaram P, Djomeh ZE, Homayouni A (2013) Microstructural and mechanical properties of camel longissimus dorsi muscle during roasting, braising and microwave heating. Meat Sci 95(2):419–424. https://doi.org/10.1016/j.meatsci.2013.05.018

    Article  CAS  PubMed  Google Scholar 

  25. Buchowski MS, Mahoney AW, Carpenter CE, Cornforth DP (2006) Heating and distribution of total and heme iron between meat and broth. J Food Sci. https://doi.org/10.1111/j.1365-2621.1988.tb10174.x

    Article  Google Scholar 

  26. Pourkhalili A, Mirlohi M, Rahimi E (2013) Heme iron content in lamb meat is differentially altered upon boiling, grilling, or frying as assessed by four distinct analytical methods. Sci World J. https://doi.org/10.1155/2013/374030

    Article  Google Scholar 

  27. Schricker BR, Miller DD (1983) Effects of cooking and chemical treatment on heme and nonheme iron in meat. J Food Sci 48(4):1340–1343. https://doi.org/10.1111/j.1365-2621.1983.tb09225.x

    Article  CAS  Google Scholar 

  28. da Silva FLF, de Lima JPS, Melo LS, da Silva YSM, Gouveia ST, Lopes GS, Matos WO (2017) Comparison between boiling and vacuum cooking (sous-vide) in the bioaccessibility of minerals in bovine liver samples. Food Res Int 100(Part 1):566–571. https://doi.org/10.1016/j.foodres.2017.07.054

    Article  CAS  PubMed  Google Scholar 

  29. Duh S-H, Cook JD (2005) Laboratory Reference Range Values. University of Maryland School of Medicine, Baltimore City, Maryland, USA. Accessed via http://stedmansonline.com/webFiles/Dict-Stedmans28/APP17.pdf

  30. Goulle JP, Mahieu L, Castermant J, Neveu N, Bonneau L, Laine G, Bouige D, Lacroix C (2005) Metal and metalloid multi-elementary ICP-MS validation in whole blood, plasma, urine and hair. Reference values. Forensic Sci Int 153(1):39–44. https://doi.org/10.1016/j.forsciint.2005.04.020

    Article  CAS  PubMed  Google Scholar 

  31. Laposata M (2014) Clinical laboratory reference values. In: Laposata M (ed) Laboratory medicine: the diagnosis of disease in the clinical laboratory. 2nd edn. McGraw-Hill Medical, New York

    Google Scholar 

  32. Torra M, Rodamilans M, Corbella J, Ferrer R, Mazzara R (1999) Blood chromium determination in assessing reference values in an unexposed Mediterranean population. Biol Trace Elem Res 70(2):183–189. https://doi.org/10.1007/BF02783859

    Article  CAS  PubMed  Google Scholar 

  33. Rukgauer M, Klein J, Kruse-Jarres JD (1997) Reference values for the trace elements copper, manganese, selenium, and zinc in the serum/plasma of children, adolescents, and adults. J Trace Elem Med Biol Org Soc Miner Trace Elem 11(2):92–98. https://doi.org/10.1016/S0946-672X(97)80032-6

    Article  CAS  Google Scholar 

  34. Lech T (2013) Application of ICP-OES to the determination of barium in blood and urine in clinical and forensic analysis. J Anal Toxicol 37(4):222–226. https://doi.org/10.1093/jat/bkt015

    Article  CAS  PubMed  Google Scholar 

  35. Cuenca RE, Pories WJ, Bray J (1988) Bromine levels in human serum, urine, hair. Short communication. Biol Trace Elem Res 16(2):151–154. https://doi.org/10.1007/BF02797099

    Article  CAS  Google Scholar 

  36. Batista BL, Grotto D, Carneiro MF, Barbosa F Jr (2012) Evaluation of the concentration of nonessential and essential elements in chicken, pork, and beef samples produced in Brazil. J Toxicol Environ Health Part A 75(21):1269–1279. https://doi.org/10.1080/15287394.2012.709439

    Article  CAS  PubMed  Google Scholar 

  37. Krachler M, Domej W, Irgolic KJ (2000) Concentrations of trace elements in osteoarthritic knee-joint effusions. Biol Trace Elem Res 75(1–3):253–263. https://doi.org/10.1385/BTER:75:1-3:253

    Article  CAS  PubMed  Google Scholar 

  38. Deguchi Y, Ogata A (1991) Relationship between serum selenium concentration and atherogenic index in Japanese adults. Tohoku J Exp Med 165(4):247–251

    Article  CAS  PubMed  Google Scholar 

  39. Harrington JM, Young DJ, Essader AS, Sumner SJ, Levine KE (2014) Analysis of human serum and whole blood for mineral content by ICP-MS and ICP-OES: development of a mineralomics method. Biol Trace Elem Res 160(1):132–142. https://doi.org/10.1007/s12011-014-0033-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Pereira PM, Vicente AF (2013) Meat nutritional composition and nutritive role in the human diet. Meat Sci 93(3):586–592. https://doi.org/10.1016/j.meatsci.2012.09.018

    Article  CAS  PubMed  Google Scholar 

  41. Serrano A, Cofrades S, Ruiz-Capillas C, Olmedilla-Alonso B, Herrero-Barbudo C, Jimenez-Colmenero F (2005) Nutritional profile of restructured beef steak with added walnuts. Meat Sci 70(4):647–654. https://doi.org/10.1016/j.meatsci.2005.02.014

    Article  CAS  PubMed  Google Scholar 

  42. Williams P (2007) Nutritional composition of red meat. Nutr Diet 64:S113-S119. https://doi.org/10.1111/j.1747-0080.2007.00197.x

    Article  Google Scholar 

  43. Stodolak B, Starzyńska A, Czyszczoń M, Żyła K (2007) The effect of phytic acid on oxidative stability of raw and cooked meat. Food Chem 101(3):1041–1045. https://doi.org/10.1016/j.foodchem.2006.02.061

    Article  CAS  Google Scholar 

  44. Hurrell R, Egli I (2010) Iron bioavailability and dietary reference values. Am J Clin Nutr 91(5):1461S–1467S. https://doi.org/10.3945/ajcn.2010.28674F

    Article  CAS  PubMed  Google Scholar 

  45. King JC, Hambidge KM, Westcott JL, Kern DL, Marshall G (1994) Daily variation in plasma zinc concentrations in women fed meals at six-hour intervals. J Nutr 124(4):508–516

    Article  CAS  PubMed  Google Scholar 

  46. Lonnerdal B (2000) Dietary factors influencing zinc absorption. J Nutr 130(5S Suppl):1378S–1383S

    Article  CAS  PubMed  Google Scholar 

  47. Olivares M, Pizarro F, Ruz M, de Romana DL (2012) Acute inhibition of iron bioavailability by zinc: studies in humans. Biomet Int J Role Met Ions Biol Biochem Med 25(4):657–664. https://doi.org/10.1007/s10534-012-9524-z

    Article  CAS  Google Scholar 

  48. Arsenault JE, Wuehler SE, de Romana DL, Penny ME, Sempertegui F, Brown KH (2011) The time of day and the interval since previous meal are associated with plasma zinc concentrations and affect estimated risk of zinc deficiency in young children in Peru and Ecuador. Eur J Clin Nutr 65(2):184–190. https://doi.org/10.1038/ejcn.2010.234

    Article  CAS  PubMed  Google Scholar 

  49. Parada J, Aguilera JM (2007) Food microstructure affects the bioavailability of several nutrients. J Food Sci 72(2):R21–R32. https://doi.org/10.1111/j.1750-3841.2007.00274.x

    Article  CAS  PubMed  Google Scholar 

  50. Van Buggenhout S, Alminger M, Lemmens L, Colle I, Knockaert G, Moelants K, Van Loey A, Hendrickx M (2010) In vitro approaches to estimate the effect of food processing on carotenoid bioavailability need thorough understanding of process induced microstructural changes. Trends Food Sci Technol 21(12):607–618. https://doi.org/10.1016/j.tifs.2010.09.010

    Article  CAS  Google Scholar 

  51. Lobo AR, Filho JM, Alvares EP, Cocato ML, Colli C (2009) Effects of dietary lipid composition and inulin-type fructans on mineral bioavailability in growing rats. Nutrition 25(2):216–225. https://doi.org/10.1016/j.nut.2008.08.002

    Article  CAS  PubMed  Google Scholar 

  52. Ramos A, Cabrera MC, Saadoun A (2012) Bioaccessibility of Se, Cu, Zn, Mn and Fe, and heme iron content in unaged and aged meat of Hereford and Braford steers fed pasture. Meat Sci 91(2):116–124. https://doi.org/10.1016/j.meatsci.2012.01.001

    Article  CAS  PubMed  Google Scholar 

  53. Cornes MP, Ford C, Gama R (2008) Spurious hyperkalaemia due to EDTA contamination: common and not always easy to identify. Ann Clin Biochem 45(Pt 6):601–603. https://doi.org/10.1258/acb.2008.007241

    Article  CAS  PubMed  Google Scholar 

  54. Imafuku Y, Meguro S, Kanno K, Hiraki H, Nemoto U, Hata R, Takahashi K, Miura Y, Yoshida H (2002) The effect of EDTA contaminated in sera on laboratory data. Clin Chim Acta Int J Clin Chem 325(1–2):105–111

    Article  CAS  Google Scholar 

  55. Bahnisch R, Clark J, Rankin W, Saleem M (2015) Which specimen tube is best for serum/plasma or whole blood trace element analysis? In: Australasian Association of Clinical Biochemists 53rd annual scientific conference, Sydney

  56. Gutierrez OM, Isakova T, Smith K, Epstein M, Patel N, Wolf M (2010) Racial differences in postprandial mineral ion handling in health and in chronic kidney disease. Nephrol Dial Transplant 25(12):3970–3977. https://doi.org/10.1093/ndt/gfq316

    Article  PubMed  PubMed Central  Google Scholar 

  57. Hutchinson C, Conway RE, Bomford A, Hider RC, Powell JJ, Geissler CA (2008) Post-prandial iron absorption in humans: comparison between HFE genotypes and iron deficiency anaemia. Clin Nutr 27(2):258–263. https://doi.org/10.1016/j.clnu.2007.12.007

    Article  CAS  PubMed  Google Scholar 

  58. Young LR, Nestle M (2003) Expanding portion sizes in the US marketplace: implications for nutrition counseling. J Am Diet Assoc 103(2):231–234. https://doi.org/10.1053/jada.2003.50027

    Article  PubMed  Google Scholar 

  59. McAfee AJ, McSorley EM, Cuskelly GJ, Moss BW, Wallace JM, Bonham MP, Fearon AM (2010) Red meat consumption: an overview of the risks and benefits. Meat Sci 84(1):1–13. https://doi.org/10.1016/j.meatsci.2009.08.029

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors thank Drs Scott Knowles and Emma Bermingham (AgResearch Limited) for their critical evaluation of the manuscript.

Funding

This study was supported by an Establishment Grant from the Liggins Institute, The University of Auckland (JFM and DCS) and through AgResearch Strategic Science Investment Fund contract A19079 (Nutritional Strategies for an Ageing Population).

Author information

Authors and Affiliations

  1. Food Nutrition and Health Team, Food and Bio-based Products Group, AgResearch Limited, Grasslands Research Centre, Private Bag 11008, Palmerston North, 4474, New Zealand

    Matthew P. G. Barnett

  2. Food and Bio-based Products Group, AgResearch Limited, Grasslands Research Centre, Palmerston North, 4442, New Zealand

    David Cameron-Smith

  3. The High-Value Nutrition National Science Challenge, Auckland, New Zealand

    Matthew P. G. Barnett

  4. Riddet Institute, Palmerston North, 4442, New Zealand

    Matthew P. G. Barnett & David Cameron-Smith

  5. The Liggins Institute, The University of Auckland, Private Bag 92019, Auckland, 1142, New Zealand

    Vic S. C. Chiang, Amber M. Milan, Shikha Pundir, James F. Markworth & David Cameron-Smith

  6. Canterbury Health Laboratories, 524 Hagley Avenue, Addington, Christchurch, 8011, New Zealand

    Trevor A. Walmsley, Susan Grant & Peter M. George

  7. Department of Food Sciences, School of Chemical Sciences, The University of Auckland, Auckland, 1142, New Zealand

    Siew-Young Quek

Authors
  1. Matthew P. G. Barnett
    View author publications

    Search author on:PubMed Google Scholar

  2. Vic S. C. Chiang
    View author publications

    Search author on:PubMed Google Scholar

  3. Amber M. Milan
    View author publications

    Search author on:PubMed Google Scholar

  4. Shikha Pundir
    View author publications

    Search author on:PubMed Google Scholar

  5. Trevor A. Walmsley
    View author publications

    Search author on:PubMed Google Scholar

  6. Susan Grant
    View author publications

    Search author on:PubMed Google Scholar

  7. James F. Markworth
    View author publications

    Search author on:PubMed Google Scholar

  8. Siew-Young Quek
    View author publications

    Search author on:PubMed Google Scholar

  9. Peter M. George
    View author publications

    Search author on:PubMed Google Scholar

  10. David Cameron-Smith
    View author publications

    Search author on:PubMed Google Scholar

Contributions

MPGB assisted with analysis and interpretation of data, and drafted the manuscript. VSCC carried out ICP-MS analysis (with assistance from TAW and SJG) and helped draft the manuscript. AMM and SP were involved in the coordination, management and implementation of the clinical trial. AMM completed statistical analysis of the data. JFM provided laboratory supervision and assisted with the data analysis. SYQ was involved in the study design and supervision of the intervention. PMG provided oversight and management of the ICP-MS data generation. DCS formulated the research question, and initiated and supervised all aspects of the study. All authors approved the final version of the manuscript for submission.

Corresponding author

Correspondence to Matthew P. G. Barnett.

Ethics declarations

Conflict of interest

The authors have no conflicts of interest to declare.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Barnett, M.P.G., Chiang, V.S.C., Milan, A.M. et al. Plasma elemental responses to red meat ingestion in healthy young males and the effect of cooking method. Eur J Nutr 58, 1047–1054 (2019). https://doi.org/10.1007/s00394-018-1620-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00394-018-1620-6

Keywords