The effect of six-week consumption of full-fat yogurt made from the milk of sheep fed with iodine-enriched feed on indicators of thyroid function and selected biochemical and anthropometric parameters
Keywords:
yogurt, sheep, iodine, thyroid, biochemical profile, anthropometric profileAbstract
The purpose of the study was to determine what changes will occur under the influence of six-week consumption of full-fat yogurt made from sheep's milk from ewes fed with iodine-enriched feed in relation to indicators of thyroid function – thyroid-stimulating hormone (TSH), free triiodothyronine (fT3), free thyroxine (fT4), but also to selected biochemical and anthropometric parameters. The intervention group consisted of nineteen women aged 54 ±7 years. It was a hyper-cholesterolemic group with a non-atherogenic lipid profile. Six-week consumption of sheep's yogurt contributed to the intake of an important element in human nutrition, but did not cause changes in the function of the thyroid gland, nor in the state of the hormones that produce or regulate its activity. TSH decreased from 2.6 ±1.0 mlU.l-1 to 2.4 ±1.0 mlU.l-1, fT4 increased from 15.2 ±1.5 pmol.l-1 to 15.3 ±1.7 pmol.l-1, but there were no statistically significant changes (P >0.05). The value of fT3 did not change at all (4.8 pmol.l-1). The intervention had no significant negative impact either on the lipid profile or other biochemical and anthropometric parameters. Our findings indicate that the consumption of full-fat sheep's yogurt not only contributes to the intake of iodine in the diet, but in terms of fat content does not cause health complications and deterioration of the lipid profile or other biochemical or anthropometric parameters
References
Arrizabalaga, J.J., Jalon, M., Espada, M. et al. (2015). Iodine concentration in ultra-high temperature pasteurized cow’s milk. Applications in clinical practice and in community nutrition. Med Clin (Barc)., 145, 55-61.
Atzmon, G., Barzilai, N., Hollowell, J.G., Surks, M.I. and Gabriely, I. (2009). Extreme longevity is associated with increased serum thyrotropin. J Clin Endocrinol Metab., 94, 1251-1254. https://doi.org/10.1210/jc.2008-2325
Banach, M. and Aronow, W.S. (2012). Hypertension therapy in the older adults – do we know the answers to all the questions? The status after publication of the ACCF/AHA 2011 expert consensus document on hypertension in the elderly. J Hum Hypertens., 26, 641-643.
Bednář, J., Rohling, S. and Vohnout, S. (1964). Příspěvek ke stanovení proteinového jodu v krevním séru (Contribution to the determination of protein iodine in blood serum). Československá farmacie. 1964, 1, 203-209.
Bigornia, S.J., LaValley, M.P., Moore, L.L. et al. (2014). Dairy intakes at age 10 years do not adversely affect risk of excess adiposity at 13 years. J Nutr, 144, 1081-1090.
Biondi, B. (2012). Natural history, diagnosis and management of subclinical thyroid dysfunction. Best Pract Res Clin Endocrinol Metab., 26: 431-446. https://doi.org/10.1016/j.beem.2011.12.004
Brites, F., Martin, M., Guillas, I. and Kontush, A. (2017). Antioxidative activity of high-density lipoprotein (HDL): Mechanistic insights into potential clinical benefit. BBA Clin., 8, 66-77. https://doi.org/10.1016/j.bbacli.2017.07.002
Brown, S.J., Bremner, A.P., Hadlow, N.C., Feddema, P., Leedman, P.J., O'Leary, P.C. et al. (2016). The log TSH-free T4 relationship in a community-based cohort is nonlinear and is influenced by age, smoking and thyroid peroxidase antibody status. Clin Endocrinol (Oxf)., 85, 789-796. https://doi.org/10.1111/cen.13107
Chaker, L., Korevaar, T.I., Medici, M., Uitterlinden, A.G., Hofman, A., Dehghan, A. et al. (2016). Thyroid Function Characteristics and Determinants: The Rotterdam Study. Thyroid, 26, 1195-1204. https://doi.org/10.1089/thy.2016.0133
Charlton, K., Probst, Y. and Kiene, G. (2016). Dietary Iodine Intake of the Australian Population after Introduction of a Mandatory Iodine Fortification Programme. Nutrients, 8, 701.
Chiu, S., Bergeron, N., Williams, P.T., Bray, G.A., Sutherland, B. and Krauss, R.M. (2016). Comparison of the DASH (Dietary Approaches to Stop Hypertension) diet and a higher-fat DASH diet on blood pressure and lipids and lipoproteins: a randomized controlled trial. Am J Clin Nutr., 103, 341-347.
Cleeman, J., Grundy, S., Becker, D., Clark, L., Cooper, R., Denke, M., Howard,W., Hunninghake, D. and Illingworth, D. (2001). Executive summary of the third report of the national cholesterol education program (NCEP). Expert panel on detection, evaluation, and treatment of high blood cholesterol in adults (adult treatment panel III). JAMA, 285, 2486-2497.
Cooper, D.S. and Biondi, B. (2012). Subclinical thyroid disease. Lancet, 379: 1142-1154. https://doi.org/10.1016/S0140-6736(11)60276-6
DAPA. Diet, Anthropometry and Physical Activity Measurement Toolkit. (2022). Available online: https://dapa-toolkit.mrc.ac.uk/anthropometry/introduction/anthropometry (accessed on 29 July 2022).
Dayimu, A., Wang, C., Li, J., Fan, B., Ji, X., Zhang, T. and Xue, F. Trajectories of Lipids Profile and Incident Cardiovascular Disease Risk: A Longitudinal Cohort Study. J Am Heart Assoc., 8(21), e013479. doi: https://doi.org/10.1161/JAHA.119.013479
Drouin-Chartier, J.-P., Brassard, D., Tessier-Grenier, M., Côté, J.A., Labonté, M.-È., Desroches, S., Couture, P. and Lamarche, B. (2016). Systematic review of the association between dairy product consumption and risk of cardiovascular-related clinical outcomes. Adv. Nutr., 7, 1026-1040.
Dubois, L., Diasparra, M., Bogl, L. et al. (2016). Dietary intake at 9 years and subsequent body mass index in adolescent boys and girls: a study of monozygotic twin pairs. Twin Res Hum Genet, 19, 47-59.
Dunn, J. (2006). Iodine. In Modern Nutrition in Health and Disease, 10th edition ed.; Shils, M., Ed.; Lippincott Williams & Wilkins: New York.
Fazilah, N.F., Ariff, A.B., Khayat, M.E. et al. (2018). Influence of probiotics, prebiotics, synbiotics and bioactive phytochemicals on the formulation of functional yogurt. J. Funct. Foods., 48, 387-399.
Geiker, N.R.W., Mølgaard, C., Iuliano, S., Rizzoli, R., Manios, Y., van Loon, L.J.C., Lecerf, J.M., Moschonis, G., Reginster, J.Y., Givens, I. et al. (2020). Impact of whole dairy matrix on musculoskeletal health and aging–current knowledge and research gaps. Osteoporos. Int., 31, 601-615.
Generoso, G. et al. (2019). High-density lipoprotein-cholesterol subfractions and coronary artery calcium: The ELSA-Brasil study. Arch. Med. Res., 50, 362-367. https://doi.org/10.1016/j.arcmed.2019.10.006
Gostas, D.E., Larson-Meyer, D.E., Yoder, H.A., Huffman, A.E. and Johnson, E.C. (2020). Dietary Relationship with 24 h Urinary Iodine Concentrations of Young Adults in the Mountain West Region of the United States. Nutrients, 12(1), 121. https://doi.org/10.3390/nu12010121.
Herrick, K.A., Perrine, C.G., Aoki, Y. and Caldwell, K.L. (2018). Iodine Status and Consumption of Key Iodine Sources in the U.S. Population with Special Attention to Reproductive Age Women. Nutrients, 10, 874. doi:10.3390/nu10070874.
Hetzel, B.S. and Zimmermann, M.B. (1993). The Iodine Deficiency Disorders. Iodine Defic. Eur., 25-31.
Hite, A.H., Feinman, R.D., Guzman, G.E., Satin, M., Schoenfeld, P.A. and Wood, R.J. (2010). In the face of contradictory evidence: report of the Dietary Guidelines for Americans Committee. Nutrition, 26(10):915-924. https://doi.org/10.1016/j.nut.2010.08.012
Hollowell, J.G., Staehling, N.W., Flanders, W.D., Hannon, W.H., Gunter, E.W., Spencer, C.A. et al. (2002). Serum TSH, T (4), and thyroid antibodies in the United States population (1988 to 1994): National Health and Nutrition Examination Survey (NHANES III). J Clin Endocrinol Metab., 87, 489-499. https://doi.org/10.1210/jcem.87.2.8182
Hoogeveen, R.C. et al. (2014). Small dense low-density lipoprotein-cholesterol concentrations predict risk for coronary heart disease: the Atherosclerosis Risk In Communities (ARIC) study. Arterioscler Thromb Vasc Biol., 34, 1069-1077. https://doi.org/10.1161/atvbaha.114.303284
Institute of Medicine (US). Panel on Micronutrients. (2001). Iodine. In Dietary Reference Intakes for Vitamin A, Vitamin K, Arsenic, Boron, Chromium, Copper, Iodine, Iron, Manganese, Molybdenum, Nickel, Silicon, Vanadium, and Zinc. National Academies Press: Washington D.C.
Ivanova, E.A., Myasoedova, V.A., Melnichenko, A.A., Grechko, A.V. and Orekhov, A.N. (2017). Small dense low-density lipoprotein as biomarker for atherosclerotic diseases. Oxid. Med. Cell. Longev., 1273042. https://doi.org/10.1155/2017/1273042
Jahreis, G., Hausmann, W., Kiessling, G., Franke, K. and Leiterer, M. (2001). Bioavailability of Iodine from Normal Diets Rich in Dairy Products-Results of Balance Studies in Women. Exp. Clin. Endocrinol. Diabetes, 109, 163-167.
Kajaba, I., Štencl, J., Ginter, E., Šašinka, M.A., Trusková, I., Gazdíková, K., Hamade, J. and Bzdúch, V. (2015). Odporúčané výživové dávky pre obyvateľstvo SR (9. revízia). (Recommended Dietary Allowance for Slovak population.) Vestník MZ SR. 2015, 63(4-5), 17-28. Available online: https://www.uvzsr.sk/docs/info/hv/Recommended_Nutrition_Doses_for_Population_of_the_Slovak_Republic.pdf. (accessed on January 9).
Kaufmann, S., Wolfram, G., Delange, F. and Rambeck, W.A. (1998). Iodine supplementation of laying hen feed: A gland, mammary gland, and gastric mucosa. J. Clin. Endocrinol. Metab., 83, 1746-1751.
Khatana, C., Saini, N.K., Chakrabarti, S., Saini, V., Sharma, A., Saini, R.V. et al. (2020). Mechanistic insights into the oxidized low-density lipoprotein-induced atherosclerosis. Oxid. Med. Cell. Longev., 5245308. https://doi.org/10.1155/2020/5245308
Kidawa, M., Gluba-Brzozka, A., Zielinska, M., Franczyk, B., Banach, M. and Rysz, J. (2019). Cholesterol subfraction analysis in patients with acute coronary syndrome. Curr Vasc Pharmacol., 17, 365-375.
Lee, K.W., Cho, M.S., Shin, D. and Song, W.O. (2016). Changes in iodine status among US adults, 2001-2012. Int J Food Sci Nutr., 67, 184-194. https://doi.org/10.3109/09637486.2016.1144717.
Li, J.J. et al. (2016). Large HDL subfraction but not HDL-C is closely linked with risk factors, coronary severity and outcomes in a cohort of nontreated patients with stable coronary artery disease: A prospective observational study. Medicine (Baltimore), 95, e2600. https://doi.org/10.1097/MD.0000000000002600
Libby, P., Buring, J.E., Badimon, L., Hansson, G.K., Deanfield, J., Bittencourt, M.S. et al. (2019). Atherosclerosis. Nat. Rev. Dis. Prim., 5(1), 56. https://doi.org/10.1038/s41572-019-0106-z
Mackowiak, P.A. (2013). Recycling metchnikoff: probiotics, the intestinal microbiome and the quest for long life. Front. Public Health, 1, 52.
Madsen, C.M., Varbo, A. and Nordestgaard, B.G. (2017). Extreme high highdensity lipoprotein cholesterol is paradoxically associated with high mortality in men and women: two prospective cohort studies. Eur Heart J., 38(32), 2478-2486.
Martin, S.S. et al. (2015). HDL cholesterol subclasses, myocardial infarction, and mortality in secondary prevention: the Lipoprotein Investigators Collaborative. Eur Heart J., 36, 22-30. https://doi.org/10.1093/eurheartj/ehu264
Matsumoto, T., Takashima, H., Ohira, N., Tarutani, Y., Yasuda, Y., Yamane, T. et al. (2004). Plasma level of oxidized low-density lipoprotein is an independent determinant of coronary macrovasomotor and microvasomotor responses induced by bradykinin. J. Am. Coll. Cardiol., 44, 451-457. https://doi.org/10.1016/j.jacc.2004.03.064
Muñiz, N., Nuñez, E., Rivera, M. and Ban, M. (2023). LDL Subfractions Analysis in Pro-atherogenic Dyslipidemia – Quantimetrix, Redondo Beach, CA – #B-099. Available online: https://quantimetrix.com/wp-content/uploads/Quantimetrix_Lipoprint_poster.pdf (accessed on January 6).
Niwattisaiwong, S., Burman, K.D. and Li-Ng, M. (2017). Iodine deficiency: Clinical implications. Cleve Clin J Med., 84, 236-244. https://doi.org/10.3949/ccjm.84a.15053.
Noel, S., Ness, A.R., Northstone, K. et al. (2011). Milk intakes are not associated with percent body fat in children from ages 10 to 13 years. J Nutr, 141, 2035-2041.
Noone, E.J., Roche, H.M., Nugent, A.P. and Gibney, M.J. (2002). The effect of dietary supplementation using isomeric blends of conjugated linoleic acid on lipid metabolism in healthy human subjects. British Journal of Nutrition, 88(03):243-251.
Oravec, S. et al. (2011). HDL subfractions analysis: A new laboratory diagnostic assay for patients with cardiovascular diseases and dyslipoproteinemia. Neuro Endocrinol Lett., 32, 502-509.
Otocka-Kmiecik, A., Mikhailidis, D.P., Nicholls, S.J., Davidson, M. Rysz, J. and Banach, M. (2012). Dysfunctional HDL: a novel important diagnostic and therapeutic target in cardiovascular disease? Prog Lipid Res., 51, 314-324.
Ovadia, Y.S., Gefel, D., Weizmann, N., Raizman, M., Goldsmith, R., Mabjeesh, S.J., Dahl, L. and Troen, A.M. (2018). Low Iodine Intake from Dairy Foods Despite High Milk Iodine Content in Israel. Thyroid, 28, 1042-1051.
Pastorelli, A.A., Stacchini, P. and Olivieri, A. (2015). Daily iodine intake and the impact of salt reduction on iodine prophylaxis in the Italian population. Eur J Clin Nutr., 69, 211-215.
Pearce, E.N., Pino, S., He, X., Bazrafshan, H.R., Lee, S.L. and Braverman, L.E. (2004). Sources of dietary iodine: bread, cows' milk, and infant formula in the Boston area. J Clin Endocrinol Metab. 89, 3421-3424. https://doi.org/10.1210/jc.2003-032002.
Pehrsson, P.R., Roseland, J.M., Patterson, K.Y., Phillips, K.M., Spungen, J.H., Andrews, K.W., Gusev, P.A., Gahche, J.J., Haggans, C.J., Merkel, J.M. et al. (2022). Iodine in foods and dietary supplements: A collaborative database developed by NIH, FDA and USDA. J Food Compost Anal., 109. https://doi.org/10.1016/j.jfca.2021.104369.
Phillips, S.M., Bandini, L.G., Cyr, H. et al. (2003). Dairy food consumption and body weight and fatness studied longitudinally over the adolescent period. Int JObes, 27, 1106-1113.
Rohner, F., Zimmermann, M.B., Jooste, P.L., Pandav, C., Caldwell, K., Raghavan, R. and Raiten, D.J. (2014). Biomarkers of Nutrition for Development - Iodine Review. J. Nutr., 144, 1322S-1342S. https://doi.org/10.3945/jn.113.181974
Rysz-Gorzynska, M., Gluba-Brzozka, A. and Banach, M. (2017). High-density lipoprotein and low-density lipoprotein subfractions in patients with chronic kidney disease. Curr Vasc Pharmacol., 15, 144-151.
Řehůřková, I. and Ruprich, J. (2013). Dietary supply of iodine to Czech population and its most important source. In Proceedings of the 10th Conference of Iodine Day: Iodine supplementation as prevention of thyroid diseases and sources of dietary exposure. The National Institute of Public Health Prague, České Budějovice, Czech Republic, 15 May 2013; p. 13-19.
Schöne, F., Leiterer, M., Lebzien, P., Bemman, D., Spolders, M. and Flachowsky, G. (2009). Iodine concentration of milk in a dose-response study with dairy cows and implications for consumer iodine intake. Journal of Trace Elements in Medicine and Biology, 23, pp. 84-92.
Schöne, F., Spörl, K. and Leiterer, M. (2017). Iodine in the feed of cows and in the milk with a view to the consumer's iodine supply. J Trace Elem Med Biol., 39, 202-209. https://doi.org/10.1016/j.jtemb.2016.10.004.
Schwingshackl, L., Hoffmann, G., Schwedhelm, C., Kalle-Uhlmann, T., Missbach, B., Knüppel, S. et al. (2016). Consumption of Dairy Products in Relation to Changes in Anthropometric Variables in Adult Populations: A Systematic Review and Meta-Analysis of Cohort Studies. PLoS ONE, 11(6): e0157461. https://doi.org/10.1371/journal.pone.0157461
Sekimoto, T., Koba, S., Mori, H., Sakai, R., Arai, T., Yokota, Y. et al. (2021). Small dense low-density lipoprotein cholesterol: A residual risk for rapid progression of non-culprit coronary lesion in patients with acute coronary syndrome. J. Atheroscler. Thromb., 28(11), 1161-1174. https://doi.org/10.5551/jat.60152
Shakerian, M., Razavi, S.H., Ziai, S.A. et al. (2015). Proteolytic and ACE-inhibitory activities of probiotic yogurt containing non-viable bacteria as affected by different levels of fat, inulin and starter culture. J. Food Sci. Technol., 52, 2428-2433.
Sheehan, M.T. (2016). Biochemical Testing of the Thyroid: TSH is the Best and, Oftentimes, Only Test Needed - A Review for Primary Care. Clin Med Res., 14(2), 83-92. https://doi.org/10.3121/cmr.2016.1309
Sirtori, C.R., Ruscica, M., Calabresi, L., Chiesa, G., Giovannoni, R. and Badimon, J.J. (2019). HDL therapy today: from atherosclerosis, to stent compatibility to heart failure. Ann Med., 51(7-8), 345-359.
Skrzypczak, M., Szwed, A., Pawlińska-Chmara, R. and Skrzypulec, V. (2007). Assessment of the BMI, WHR and W/Ht in pre- and post-menopausal women. Anthropol. Rev., 70, 3-13.
Soldin, O.P. (2002). Controversies in urinary iodine determinations. Clin Biochem., 35, 575-579. https://doi.org/10.1016/s0009-9120(02)00406-x.
Sonmez, A., Nikolic, D., Dogru, T. et al. (2015). Low- and high-density lipoprotein subclasses in subjects with nonalcoholic fatty liver disease. J Clin Lipidol., 9, 576-582. 23.
Soriguer, F., Gutierrez-Repiso, C., Gonzalez-Romero, S., Olveira, G., Garriga, M.J. et al. (2011). Iodine Deficiency Disorders Group of Spanish Society of Endocrinology and Nutrition. Iodine concentration in cow's milk and its relation with urinary iodine concentrations in the population. Clin Nutr., 30(1), pp. 44-48. https://doi.org/10.1016/j.clnu.2010.07.001.
van der Reijden, O.L., Zimmermann, M.B. and Galetti, V. (2017). Iodine in dairy milk: Sources, concentrations and importance to human health. Best Pract Res Clin Endocrinol Metab., 31(4), 385-395. https://doi.org/10.1016/j.beem.2017.10.004.
Vaskonen, T. (2003). Dietary minerals and modification of cardiovascular risk factors. The Journal of nutritional biochemistry, 14(9):492-506.
Veldhorst, M., Smeets, A., Soenen, S., Hochstenbach-Waelen, A., Hursel, R., Diepvens, K. et al. (2008). Protein induced satiety: effects and mechanisms of different proteins. Physiology & behavior, 94(2):300-307.
World Health Organization. (2008). Waist Circumference and Waist-Hip Ratio: Report of a WHO Expert Consultation, World Health Organization: Geneva, Switzerland, 2008.
World Health Organization. (2014). Guideline: Fortification of Food-Grade Salt with Iodine for the Prevention and Control of Iodine Deficiency Disorders, WHO: Geneva, Switzerland, 2014.
World Health Organization. (2020). Obesity and Overweight. Available online: https://www.who.int/en/news-room/fact-sheets/detail/obesity-and-overweight (accessed on 11 July 2022).
World Health Organization. (2023). Iodine Deficiency. Available online: https://www.who.int/data/nutrition/nlis/info/iodine-deficiency (accessed on January 9).
Zanoni, P., Khetarpal, S.A., Larach, D.B. et al. (2016). Rare variant in scavenger receptor BI raises HDL cholesterol and increases risk of coronary heart disease. Science, 351, 1166-1171. https://doi.org/10.1126/science.aad3517
Zemel, M.B. (2005). The role of dairy foods in weight management. Journal of the American College of Nutrition, 24(6 Suppl):537S-46S.
Zimmerman, M.B. (2020). Iodine and the Iodine Deficiency Disorders. In Present Knowledge in Nutrition; Elsevier Inc, 1, 429-441. https://doi.org/10.1016/B978-0-323-66162-1.00025-1
Zimmermann, M.B., Jooste, P.L. and Pandav, C.S. (2008). Iodine deficiency disorders. Lancet, 372, 1251-1262.
Downloads
Published
Issue
Section
License
Copyright (c) 2023 Martina Gažarová, Róbert Toman, Petra Lenártová, Martina Pšenková, Marta Habánová, Jana Kopčeková, Vladimír Tančin, Simona Almášiová
This work is licensed under a Creative Commons Attribution 4.0 International License.
