Advertisement

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

  • Matthew P. G. Barnett
  • Vic S. C. Chiang
  • Amber M. Milan
  • Shikha Pundir
  • Trevor A. Walmsley
  • Susan Grant
  • James F. Markworth
  • Siew-Young Quek
  • Peter M. George
  • David Cameron-Smith
Original Contribution

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.

Keywords

Iron Zinc Biological availability Mass spectrometry 

Notes

Acknowledgements

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

Author 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.

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).

Compliance with ethical standards

Conflict of interest

The authors have no conflicts of interest to declare.

References

  1. 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 CrossRefGoogle Scholar
  2. 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 CrossRefGoogle Scholar
  3. 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 CrossRefGoogle Scholar
  4. 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 CrossRefGoogle Scholar
  5. 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 CrossRefGoogle Scholar
  6. 6.
    Britton E, McLaughlin JT (2013) Ageing and the gut. Proc Nutr Soc 72(1):173–177.  https://doi.org/10.1017/S0029665112002807 CrossRefGoogle Scholar
  7. 7.
    Lampe JW, Fredstrom SB, Slavin JL, Potter JD (1993) Sex differences in colonic function: a randomised trial. Gut 34(4):531–536CrossRefGoogle Scholar
  8. 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 Google Scholar
  9. 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 CrossRefGoogle Scholar
  10. 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):614–618CrossRefGoogle Scholar
  11. 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 CrossRefGoogle Scholar
  12. 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 CrossRefGoogle Scholar
  13. 13.
    Hunt JR (2003) Bioavailability of iron, zinc, and other trace minerals from vegetarian diets. Am J Clin Nutr 78(3 Suppl):633S–639SCrossRefGoogle Scholar
  14. 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):887–897CrossRefGoogle Scholar
  15. 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 CrossRefGoogle Scholar
  16. 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):124–132CrossRefGoogle Scholar
  17. 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 CrossRefGoogle Scholar
  18. 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 CrossRefGoogle Scholar
  19. 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 CrossRefGoogle Scholar
  20. 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 CrossRefGoogle Scholar
  21. 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 CrossRefGoogle Scholar
  22. 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 CrossRefGoogle Scholar
  23. 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 CrossRefGoogle Scholar
  24. 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 CrossRefGoogle Scholar
  25. 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 Google Scholar
  26. 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 Google Scholar
  27. 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 CrossRefGoogle Scholar
  28. 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 CrossRefGoogle Scholar
  29. 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. 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 CrossRefGoogle Scholar
  31. 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 YorkGoogle Scholar
  32. 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 CrossRefGoogle Scholar
  33. 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 CrossRefGoogle Scholar
  34. 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 CrossRefGoogle Scholar
  35. 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 CrossRefGoogle Scholar
  36. 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 CrossRefGoogle Scholar
  37. 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 CrossRefGoogle Scholar
  38. 38.
    Deguchi Y, Ogata A (1991) Relationship between serum selenium concentration and atherogenic index in Japanese adults. Tohoku J Exp Med 165(4):247–251CrossRefGoogle Scholar
  39. 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 CrossRefGoogle Scholar
  40. 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 CrossRefGoogle Scholar
  41. 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 CrossRefGoogle Scholar
  42. 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 CrossRefGoogle Scholar
  43. 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 CrossRefGoogle Scholar
  44. 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 CrossRefGoogle Scholar
  45. 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):508–516Google Scholar
  46. 46.
    Lonnerdal B (2000) Dietary factors influencing zinc absorption. J Nutr 130(5S Suppl):1378S–1383SCrossRefGoogle Scholar
  47. 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 Google Scholar
  48. 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 CrossRefGoogle Scholar
  49. 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 CrossRefGoogle Scholar
  50. 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 CrossRefGoogle Scholar
  51. 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 CrossRefGoogle Scholar
  52. 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 CrossRefGoogle Scholar
  53. 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 CrossRefGoogle Scholar
  54. 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):105–111CrossRefGoogle Scholar
  55. 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, SydneyGoogle Scholar
  56. 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 CrossRefGoogle Scholar
  57. 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 CrossRefGoogle Scholar
  58. 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 CrossRefGoogle Scholar
  59. 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 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Matthew P. G. Barnett
    • 1
    • 3
    • 4
  • Vic S. C. Chiang
    • 5
  • Amber M. Milan
    • 5
  • Shikha Pundir
    • 5
  • Trevor A. Walmsley
    • 6
  • Susan Grant
    • 6
  • James F. Markworth
    • 5
  • Siew-Young Quek
    • 7
  • Peter M. George
    • 6
  • David Cameron-Smith
    • 2
    • 4
    • 5
  1. 1.Food Nutrition and Health Team, Food and Bio-based Products GroupAgResearch Limited, Grasslands Research CentrePalmerston NorthNew Zealand
  2. 2.Food and Bio-based Products Group, AgResearch Limited, Grasslands Research CentrePalmerston NorthNew Zealand
  3. 3.The High-Value Nutrition National Science ChallengeAucklandNew Zealand
  4. 4.Riddet InstitutePalmerston NorthNew Zealand
  5. 5.The Liggins InstituteThe University of AucklandAucklandNew Zealand
  6. 6.Canterbury Health LaboratoriesChristchurchNew Zealand
  7. 7.Department of Food Sciences, School of Chemical SciencesThe University of AucklandAucklandNew Zealand

Personalised recommendations