4,451
Views
0
CrossRef citations to date
0
Altmetric
Research Article

Menstrual Cycle-Associated Changes in Micronutrient Biomarkers Concentration: A Prospective Cohort Study

ORCID Icon, ORCID Icon, ORCID Icon & ORCID Icon
Pages 339-348 | Received 08 Nov 2021, Accepted 07 Feb 2022, Published online: 24 Mar 2022

References

  • Dale JC, Burritt MF, Zinsmeister AR. Diurnal variation of serum iron, iron-binding capacity, transferrin saturation, and ferritin levels. Am J Clin Pathol. 2002;117(5):802–8. doi:10.1309/2YT4-CMP3-KYW7-9RK1.
  • Nguyen LT, Buse JD, Baskin L, Sadrzadeh SMH, Naugler C. Influence of diurnal variation and fasting on serum iron concentrations in a community-based population. Clin Biochem. 2017;50(18):1237–42. doi:10.1016/j.clinbiochem.2017.09.018.
  • Cooper MJ, Zlotkin SH. Day-to-day variation of transferrin receptor and ferritin in healthy men and women. Am J Clin Nutr. 1996;64(5):738–42. doi:10.1093/ajcn/64.5.738.
  • Borel MJ, Smith SM, Derr J, Beard JL. Day-to-day variation in iron-status indices in healthy men and women. Am J Clin Nutr. 1991;54(4):729–35. doi:10.1093/ajcn/54.4.729.
  • Favier A, Ruffieux D. Physiological variations of serum levels of copper, zinc, iron and manganese. Biomed Pharmacother. 1983;37(9–10):462–6.
  • Schisterman EF, Mumford SL, Sjaarda LA. Failure to consider the menstrual cycle phase may cause misinterpretation of clinical and research findings of cardiometabolic biomarkers in premenopausal women. Epidemiol Rev. 2014;36:71–82. doi:10.1093/epirev/mxt007.
  • Muneyvirci-Delale O, Nacharaju V, Altura B, Altura B. Sex steroid hormones modulate serum ionized magnesium and calcium levels throughout the menstrual cycle in women. Fertil Steril. 1998;69(5):958–62. doi:10.1016/s0015-0282(98)00053-3.
  • Angeli A, Laine F, Lavenu A, Ropert M, Lacut K, Gissot V, Sacher-Huvelin S, Jezequel C, Moignet A, Laviolle B, et al. Joint model of iron and hepcidin during the menstrual cycle in healthy women. Aaps J. 2016;18(2):490–504. doi:10.1208/s12248-016-9875-4.
  • Deuster PA, Dolev E, Bernier LL, Trostmann UH. Magnesium and zinc status during the menstrual cycle. Am J Obstet Gynecol. 1987;157(4 Pt 1):964–8. doi:10.1016/S0002-9378(87)80096-0.
  • Michos C, Kalfakakou V, Karkabounas S, Kiortsis D, Evangelou A. Changes in copper and zinc plasma concentrations during the normal menstrual cycle in women. Gynecological Endocrinology. 2010;26(4):250–5. doi:10.3109/09513590903247857.
  • Lanje MA, Bhutey AK, Kulkarni SR, Dhawle UP, Sande AS. Serum electrolytes during different phases of menstrual cycle. Int J Pharma Sci Res IJPSR. 2010;1(10):435–7.
  • Pandya AK, Chandwani S, Das TK, Pandya KD. Serum calcium, magnesium and inorganic phosphorous levels during various phases of menstrual cycle. Indian J Physiol Pharmacol. 1995;39(4):411–4.
  • Kim I, Yetley EA, Calvo MS. Variations in iron-status measures during the menstrual cylce. Am J Clin Nutr. 1993;58(5):705–9. doi:10.1093/ajcn/58.5.705.
  • Belza A, Henriksen M, Ersbøll AK, Thilsted SH, Tetens I. Day-to-day variation in iron-status measures in young iron-deplete women. Br J Nutr. 2005;94(4):551–6. doi:10.1079/bjn20051461.
  • Inoue K, Sugiyama M. Changes in body iron status, heart rate, and unspecific symptoms across menstrual cycle in marginally iron-deficient young women. J Clin Biochem Nutr. 1998;24(2):99–104. doi:10.3164/jcbn.24.99.
  • Cole LA, Ladner DG, Byrn FW. The normal variabilities of the menstrual cycle. Fertil Steril. 2009;91(2):522–7. doi:10.1016/j.fertnstert.2007.11.073.
  • Fehring RJ, Schneider M, Raviele K. Variability in the phases of the menstrual cycle. J Obstet Gynecol Neonatal Nurs. 2006;35(3):376–84. doi:10.1111/j.1552-6909.2006.00051.x.
  • Treloar AE, Boynton RE, Behn BG, Brown BW. The menstrual cycle- variation of the human menstrual cycle through the reproductive life. Int J Fertil. 1967;12(1 Pt 2):77–126.
  • Chiazze L, Brayer FT, Macisco JJ, Parker MP, Duffy BJ. The length and variability of the human menstrual cycle. JAMA. 1968;203(6):377–80. doi:10.1001/jama.1968.03140060001001.
  • Buchheit M, Laursen PB, Al Haddad H, Ahmaidi S. Exercise-induced plasma volume expansion and post-exercise parasympathetic reactivation. Eur J Appl Physiol. 2009;105(3):471–81. doi:10.1007/s00421-008-0925-1.
  • Rhibi F, Prioux J, Attia MB, Hackney AC, Zouhal H, Abderrahman AB. Increase interval training intensity improves plasma volume variations and aerobic performances in response to intermittent exercise. Physiol Behav. 2019;199:137–45. doi:10.1016/j.physbeh.2018.11.020.
  • Kalra PR, Anagnostopoulos C, Bolger AP, Coats AJ, Anker SD. The regulation and measurement of plasma volume in heart failure. J Am Coll Cardiol. 2002;39(12):1901–8. doi:10.1016/s0735-1097(02)01903-4.
  • Schrier RW, Howard RL. Unifying hypothesis of sodium and water regulation in health and disease. Hypertension. 1991;18(5 Suppl):III164–168. doi:10.1161/01.hyp.18.5_suppl.iii164.
  • Hammersborg SM, Farstad M, Haugen O, Kvalheim V, Onarheim H, Husby P. Time course variations of haemodynamics, plasma volume and microvascular fluid exchange following surface cooling: An experimental approach to accidental hypothermia. Resuscitation. 2005;65(2):211–9. doi:10.1016/j.resuscitation.2004.11.020.
  • Kenefick RW, Sollanek KJ, Charkoudian N, Sawka MN. Impact of skin temperature and hydration on plasma volume responses during exercise. J Appl Physiol (1985). 2014;117(4):413–20. doi:10.1152/japplphysiol.00415.2014.
  • Bloomer RJ, Farney TM. Acute plasma volume change with high-intensity sprint exercise. J Strength Condition Res. 2013;27(10):2874–8. doi:10.1519/JSC.0b013e318282d416.
  • Jimenez C, Melin B, Koulmann N, Allevard AM, Launay JC, Savourey G. Plasma volume changes during and after acute variations of body hydration level in humans. Eur J Appl Physiol. 1999;80(1):1–8. doi:10.1007/s004210050550.
  • Aguree S, Gernand AD. A methodology for examining the association between plasma volume and micronutrient biomarker mass and concentration in healthy eumenorrheic women. PeerJ. 2020;8:e10535. doi:10.7717/peerj.10535.
  • Hambridge HL, Mumford SL, Mattison DR, Ye A, Pollack AZ, Bloom MS, Mendola P, Lynch KL, Wactawski-Wende J, Schisterman EF. The influence of sporadic anovulation on hormone levels in ovulatory cycles. Human Reprod. 2013;28(6):1687–94. doi:10.1093/humrep/det090.
  • Lynch KE, Mumford SL, Schliep KC, Whitcomb BW, Zarek SM, Pollack AZ, Bertone-Johnson ER, Danaher M, Wactawski-Wende J, Gaskins AJ, et al. Assessment of anovulation in eumenorrheic women: Comparison of ovulation detection algorithms. Fertil Steril. 2014;102(2):511–8. e512,
  • Aguree S, Bethancourt HJ, Taylor LA, Rosinger AY, Gernand AD. Plasma volume variation across the menstrual cycle among healthy women of reproductive age: A prospective cohort study. Physiol Rep. 2020;8(8):e14418. doi:10.14814/phy2.14418.
  • Hess SY, Peerson JM, King JC, Brown KH. Use of serum zinc concentration as an indicator of population zinc status. Food Nutr Bull. 2007;28(3 Suppl):S403–S429. doi:10.1177/15648265070283S303.
  • IOM: Institute of Medicine, Food and Nutrition Board. Dietary reference intakes for vitamin a, vitamin k, arsenic, boron, chromium, copper, iodine, iron, manganese, molybdenum, nickel, silicone, vanadium, and zinc. Washington (DC): National Academies Press, 2001.
  • Grober U, Schmidt J, Kisters K. Magnesium in prevention and therapy. Nutrients. 2015;7(9):8199–226. doi:10.3390/nu7095388.
  • Iyengar V, Woittiez J. Trace elements in human clinical specimens: Evaluation of literature data to identify reference values. Clin Chem. 1988;34(3):474–81.
  • WHO. Serum ferritin concentrations for the assessment of iron status and iron deficiency in populations. Vitamin and mineral nutrition information system. Geneva, World Health Organization, 2011. (who/nmh/nhd/mnm/11.2). (http://www.Who.Int/vmnis/indicators/serum_ferritin.Pdf, accessed March 26, 2019).
  • WHO. Serum retinol concentrations for determining the prevalence of vitamin a deficiency in populations. Vitamin and mineral nutrition information system. Geneva, World Health Organization, 2011. (who/nmh/nhd/mnm/11.3) (http://www.Who.Int/vmnis/indicators/retinol.Pdf, accessed March 26, 2019).
  • CDC. Centers for Disease Control and Prevention. Recommendations to prevent and control iron deficiency in the united states. Morbidity Mortality Weekly Report Recommend Report. 1998;47(RR-3):1–29.
  • WHO/CDC. Assessing the iron status of populations: Report of a joint world health organization/centers for disease control and prevention technical consultation on the assessment of iron status at the population level. Geneva, Switzerland 6–8 April 2004. WHO Library Cataloguing-In-Publication Data 2007. [cited July 21 2017]. http://whqlibdoc.Who.Int/publications/2004/9241593156_eng.Pdf.
  • Thurnham D, McCabe G, Northrop-Clewes C, Nestel P. Effects of subclinical infection on plasma retinol concentrations and assessment of prevalence of vitamin a deficiency: Meta-analysis. Lancet. 2003;362(9401):2052–8. doi:10.1016/s0140-6736(03)15099-4.
  • Fiorentino M, Perignon M, Kuong K, Chamnan C, Berger J, Wieringa FT. Subclinical inflammation affects iron and vitamin a but not zinc status assessment in senegalese children and cambodian children and women. Public Health Nutr. 2018;21(7):1266–77. doi:10.1017/S1368980017003809.
  • Aguree S, Gernand AD. An efficient method for measuring plasma volume using indocyanine green dye. MethodsX. 2019;6:1072–83. doi:10.1016/j.mex.2019.05.003.
  • Aguree S, Murray-Kolb LE, Diaz F, Gernand AD. Menstrual cycle-associated changes in micronutrient biomarkers concentration: A prospective cohort study. Dryad Digital Repository. 2021; 5 October 2021. https://doi.org/10.5061/dryad.547d7wm90.
  • Rosenstein DL, Ryschon TW, Niemela JE, Elin RJ, Balaban RS, Rubinow DR. Skeletal muscle intracellular ionized magnesium measured by 31p-nmr spectroscopy across the menstrual cycle. J Am Coll Nutr. 1995;14(5):486–90. doi:10.1080/07315724.1995.10718540.
  • Chandra S, Gupta N, Patel S. Study of iron status indicators in different phases of menstrual cycle in first year medical college females. Int J Res Med Sci. 2017;5(1):46–49. doi:10.18203/2320-6012.ijrms20164520.
  • Brabin L, Roberts C, Barr F, Agbaje S, Harper G, Briggs N. Sex hormone patterns and serum retinol concentrations in adolescent girls. J Reproduct Med. 2004;49(1):42–51.
  • Laurence PA, Sobel AE. Changes in serum vitamin a level during the human menstrual cycle. J Clin Endocrinol Metab. 1953;13(10):1192–200. doi:10.1210/jcem-13-10-1192.
  • Mumford SL, Browne RW, Schliep KC, Schmelzer J, Plowden TC, Michels KA, Sjaarda LA, Zarek SM, Perkins NJ, Messer LC, et al. Serum antioxidants are associated with serum reproductive hormones and ovulation among healthy women. J Nutr. 2016;146(1):98–106. doi:10.3945/jn.115.217620.
  • Halls DJ, Fell GS. Determination of manganese in serum and urine by electrothermal atomic absorption spectrometry. Anal Chim Acta. 1981;129:205–11. doi:10.1016/S0003-2670(01)84133-7.
  • Rükgauer M, Klein J, Kruse-Jarres JD. 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. 1997;11(2):92–8. doi:10.1016/S0946-672X(97)80032-6.
  • Milne D, Sims R, Ralston N. Manganese content of the cellular components of blood. Clin Chem. 1990;36(3):450–2.
  • Gbemavo MCJ, Bouchard MF. Concentrations of lead, mercury, selenium, and manganese in blood and hand grip strength among adults living in the United States (nhanes 2011–2014). Toxics. 2021;9(8):189. doi:10.3390/toxics9080189.
  • Hennigar SR, Lieberman HR, Fulgoni VL, 3rd, McClung JP. Serum zinc concentrations in the us population are related to sex, age, and time of blood draw but not dietary or supplemental zinc. J Nutr. 2018;148(8):1341–51. doi:10.1093/jn/nxy105.
  • Oosthuyse T, Bosch AN. The effect of the menstrual cycle on exercise metabolism: Implications for exercise performance in eumenorrhoeic women. Sports Med. 2010;40(3):207–27. doi:10.2165/11317090-000000000-00000.
  • Draper CF, Duisters K, Weger B, Chakrabarti A, Harms AC, Brennan L, Hankemeier T, Goulet L, Konz T, Martin FP, et al. Menstrual cycle rhythmicity: Metabolic patterns in healthy women. Sci Rep. 2018;8(1):14568. doi:10.1038/s41598-018-32647-0.
  • Wohlgemuth KJ, Arieta LR, Brewer GJ, Hoselton AL, Gould LM, Smith-Ryan AE. Sex differences and considerations for female specific nutritional strategies: A narrative review. J Int Soc Sports Nutr. 2021;18(1):27. doi:10.1186/s12970-021-00422-8.
  • Prema K, Ramalakshmi BA, Babu S. Serum copper and zinc in hormonal contraceptive users. Fertil Steril. 1980;33(3):267–71. doi:10.1016/s0015-0282(16)44591-7.
  • Alliende ME. Mean versus individual hormonal profiles in the menstrual cycle. Fertil Steril. 2002;78(1):90–5. doi:10.1016/s0015-0282(02)03167-9.
  • Allen AM, McRae-Clark AL, Carlson S, Saladin ME, Gray KM, Wetherington CL, McKee SA, Allen SS. Determining menstrual phase in human biobehavioral research: A review with recommendations. Exp Clin Psychopharmacology. 2016;24(1):1–11. doi:10.1037/pha0000057.
  • Vir SC, Love AH. Zinc and copper nutriture of women taking oral contraceptive agents. Am J Clin Nutr. 1981;34(8):1479–83. doi:10.1093/ajcn/34.8.1479.
  • Miller EM. Iron status and reproduction in us women: National health and nutrition examination survey, 1999–2006. PLoS One. 2014;9(11):e112216. doi:10.1371/journal.pone.0112216.
  • Haile ZT, Teweldeberhan AK, Chavan B, Francescon J. Hormonal contraceptive use and vitamin a deficiency among women in Tanzania. Int J Gynecol Obstet. 2018;141(1):20–5. doi:10.1002/ijgo.12396.
  • Haile ZT, Kingori C, Teweldeberhan AK, Chavan B. The relationship between history of hormonal contraceptive use and iron status among women in tanzania: A population-based study. Sex Reproduct Healthcare. 2017;13:97–102. doi:10.1016/j.srhc.2017.07.003.
  • Lainé F, Angeli A, Ropert M, Jezequel C, Bardou-Jacquet E, Deugnier Y, Gissot V, Lacut K, Sacher-Huvelin S, Lavenu A, et al. Variations of hepcidin and iron-status parameters during the menstrual cycle in healthy women. Br J Haematol. 2016;175(5):980–2. doi:10.1111/bjh.13906.
  • Söderlund M, Sjöberg A, Svärd G, Fex G, Nilsson-Ehle P. Biological variation of retinoids in man. Scandin J Clin Lab Invest. 2002;62(7):511–9. doi:10.1080/003655102321004521.
  • Jahnen-Dechent W, Ketteler M. Magnesium basics. Clin Kidney J. 2012;5(Suppl 1):i3–i14. doi:10.1093/ndtplus/sfr163.
  • Mensink GB, Fletcher R, Gurinovic M, Huybrechts I, Lafay L, Serra-Majem L, Szponar L, Tetens I, Verkaik-Kloosterman J, Baka A, et al. Mapping low intake of micronutrients across europe. Br J Nutr. 2013;110(4):755–73. doi:10.1017/S000711451200565X.
  • Fulgoni VL, 3rd, Keast DR, Bailey RL, Dwyer J. Foods, fortificants, and supplements: Where do americans get their nutrients? J Nutr. 2011;141(10):1847–54. doi:10.3945/jn.111.142257.
  • Workinger JL, Doyle RP, Bortz J. Challenges in the diagnosis of magnesium status. Nutrients. 2018;10(9):1202. doi:10.3390/nu10091202.
  • Ballew C, Bowman BA, Sowell AL, Gillespie C. Serum retinol distributions in residents of the united states: Third national health and nutrition examination survey, 1988–1994. Am J Clin Nutri. 2001;73(3):586–93. doi:10.1093/ajcn/73.3.586.
  • Cusick SE, Mei Z, Freedman DS, Looker AC, Ogden CL, Gunter E, Cogswell ME. Unexplained decline in the prevalence of anemia among us children and women between 1988–1994 and 1999–2002. Am J Clin Nutri. 2008;88(6):1611–7. doi:10.3945/ajcn.2008.25926.
  • Cogswell ME, Looker AC, Pfeiffer CM, Cook JD, Lacher DA, Beard JL, Lynch SR, Grummer-Strawn LM. Assessment of iron deficiency in us preschool children and nonpregnant females of childbearing age: National health and nutrition examination survey 2003–2006. Am J Clin Nutr. 2009;89(5):1334–42. doi:10.3945/ajcn.2008.27151.
  • Gupta PM, Hamner HC, Suchdev PS, Flores-Ayala R, Mei Z. Iron status of toddlers, nonpregnant females, and pregnant females in the united states. Am J Clin Nutr. 2017;106(Suppl 6):1640S–6S. doi:10.3945/ajcn.117.155978.
  • Reider CA, Chung RY, Devarshi PP, Grant RW, Hazels Mitmesser S. Inadequacy of immune health nutrients: Intakes in us adults, the 2005–2016 nhanes. Nutrients. 2020;12(6):1735. doi:10.3390/nu12061735.