Circadian Variation in Human Milk Composition, a Systematic Review

Merel F Italianer, Eva F G Naninck, Jorine A Roelants, Gijsbertus T J van der Horst, Irwin K M Reiss, Johannes B van Goudoever, Koen F M Joosten, Inês Chaves, Marijn J Vermeulen, Merel F Italianer, Eva F G Naninck, Jorine A Roelants, Gijsbertus T J van der Horst, Irwin K M Reiss, Johannes B van Goudoever, Koen F M Joosten, Inês Chaves, Marijn J Vermeulen

Abstract

Background: Breastfeeding is considered the most optimal mode of feeding for neonates and mothers. Human milk changes over the course of lactation in order to perfectly suit the infant's nutritional and immunological needs. Its composition also varies throughout the day. Circadian fluctuations in some bioactive components are suggested to transfer chronobiological information from mother to child to assist the development of the biological clock. This review aims to give a complete overview of studies examining human milk components found to exhibit circadian variation in their concentration.

Methods: We included studies assessing the concentration of a specific human milk component more than once in 24 h. Study characteristics, including gestational age, lactational stage, sampling strategy, analytical method, and outcome were extracted. Methodological quality was graded using a modified Newcastle-Ottawa Scale (NOS).

Results: A total of 83 reports assessing the circadian variation in the concentration of 71 human milk components were included. Heterogeneity among studies was high. The methodological quality varied widely. Significant circadian variation is found in tryptophan, fats, triacylglycerol, cholesterol, iron, melatonin, cortisol, and cortisone. This may play a role in the child's growth and development in terms of the biological clock.

Keywords: biorhythms; breast milk; chrono-nutrition; circadian clock; diurnal variations; lactation.

Conflict of interest statement

The authors declare no conflict of interest. The funders had no role in the design of the study, in the collection, analyses, or interpretation of data, in the writing of the manuscript, or in the decision to publish the results.

Figures

Figure 1
Figure 1
Flowchart of a study selection based on the inclusion and exclusion criteria.
Figure 2
Figure 2
Circadian variation in human milk components. Schematic presentation of estimated circadian curves based on peak and trough values reported in the literature. Circadian variation curves are shown for the following components: (a) tryptophan [18,43], (b) total fats, triglycerides, cholesterol [25,32,47,48,50,51,52,53,55,56,58,59], (c) iron [53,67,70,71], (d) melatonin [41,82,83,84,85,86,87,88,89], and (e) glucocorticoids [24,89,90,91,92,93,94].

References

    1. Victora C.G., Bahl R., Barros A.J., França G.V., Horton S., Krasevec J., Murch S., Sankar M.J., Walker N., Rollins N.C. Breastfeeding in the 21st century: Epidemiology, mechanisms, and lifelong effect. Lancet. 2016;387:475–490. doi: 10.1016/S0140-6736(15)01024-7.
    1. World Health Organization. UNICEF . Global Strategy for Infant and Young Child. Feeding. WHO; Geneva, Switzerland: 2003.
    1. Hennet T., Borsig L. Breastfed at Tiffany’s. Trends. Biochem. Sci. 2016;41:508–518. doi: 10.1016/j.tibs.2016.02.008.
    1. Galante L., Milan A.M., Reynolds C.M., Cameron-Smith D., Vickers M.H., Pundir S. Sex-Specific Human Milk Composition: The Role of Infant Sex in Determining Early Life Nutrition. Nutrients. 2018;10:1194. doi: 10.3390/nu10091194.
    1. Hosseini M., Valizadeh E., Hosseini N., Khatibshahidi S., Raeisi S. The Role of Infant Sex on Human Milk Composition. Breastfeed. Med. 2020;15:341–346. doi: 10.1089/bfm.2019.0205.
    1. McKenna H., Reiss I.K.M. The case for a chronobiological approach to neonatal care. Early Hum. Dev. 2018;126:1–5. doi: 10.1016/j.earlhumdev.2018.08.012.
    1. Fuhr L., Abreu M., Pett J.P., Relógio A. Circadian systems biology: When time matters. Comput. Struct. Biotechnol. J. 2015;13:417–426. doi: 10.1016/j.csbj.2015.07.001.
    1. Takahashi J.S. Transcriptional architecture of the mammalian circadian clock. Nat. Rev. Genet. 2016;18:164–179. doi: 10.1038/nrg.2016.150.
    1. Roenneberg T., Merrow M. The Circadian Clock and Human Health. Curr. Biol. 2016;26:R432–R443. doi: 10.1016/j.cub.2016.04.011.
    1. Buhr E.D., Takahashi J.S. Molecular components of the Mammalian circadian clock. Handb. Exp. Pharmacol. 2013;217:3–27. doi: 10.1007/978-3-642-25950-0_1.
    1. Asher G., Sassone-Corsi P. Time for Food: The Intimate Interplay between Nutrition, Metabolism, and the Circadian Clock. Cell. 2015;161:84–92. doi: 10.1016/j.cell.2015.03.015.
    1. Ardura J., Gutierrez R., Andres J., Agapito T. Emergence and evolution of the circadian rhythm of melatonin in children. Horm. Res. 2003;59:66–72. doi: 10.1159/000068571.
    1. Kennaway D.J., Stamp G.E., Goble F.C. Development of melatonin production in infants and the impact of prematurity. J. Clin. Endocrinol. Metab. 1992;75:367–369.
    1. Ivars K., Nelson N., Theodorsson A., Theodorsson E., Ström J.O., Morelius E. Development of Salivary Cortisol Circadian Rhythm and Reference Intervals in Full-Term Infants. PLoS ONE. 2015;10:e0129502. doi: 10.1371/journal.pone.0129502.
    1. Mirmiran M., Maas Y.G.H., Ariagno R.L. Development of fetal and neonatal sleep and circadian rhythms. Sleep Med. Rev. 2003;7:321–334. doi: 10.1053/smrv.2002.0243.
    1. Christ E., Korf H.-W., Von Gall C. When does it start ticking? Ontogenetic development of the mammalian circadian system. Prog. Brain Res. 2012;199:105–118.
    1. Hahn-Holbrook J., Saxbe D., Bixby C., Steele C., Glynn L. Human milk as “chrononutrition”: Implications for child health and development. Pediatr. Res. 2019;85:936–942. doi: 10.1038/s41390-019-0368-x.
    1. Cubero J., Valero V., Sánchez J., Rivero M., Parvez H., Rodríguez A.B., Barriga C. The circadian rhythm of tryptophan in breast milk affects the rhythms of 6-sulfatoxymelatonin and sleep in newborn. Neuroendocr. Lett. 2005;26:657–661.
    1. van der Voorn B., Heijboer A., de Waard M., Verheijen H., Rotteveel J., Finken M. Circadian variation in cortisol concentration in mother’s milk. Horm. Res. Paediatr. 2015;84:513–514.
    1. Shamseer L., Moher D., Clarke M., Ghersi D., Liberati A., Petticrew M., Shekelle P., Stewart L.A. Preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P) 2015: Elaboration and explanation. BMJ. 2015;349:g7647. doi: 10.1136/bmj.g7647.
    1. Modesti P.A., Reboldi G. Panethnic differences in blood pressure in europe: A systematic review and meta-analysis. PLoS ONE. 2016;11:e0147601. doi: 10.1371/journal.pone.0147601.
    1. Neu J. Gastroenterology and Nutrition: Neonatology Questions and Controversies: Expert Consult—Online and Print. Elsevier Health Sciences; Amsterdam, The Netherlands: 2012.
    1. Dizdar E., Yarcı E., Sari F.N., Oguz S.S., Uras N., Canpolat F.E., Çetinkaya A.K. Does Circadian Variation of Mothers Affect Macronutrients of Breast Milk? Am. J. Perinatol. 2016;34:693–696. doi: 10.1055/s-0036-1597327.
    1. Hollanders J.J., Kouwenhoven S.M.P., van der Voorn B., van Goudoever J.B., Rotteveel J., Finken M.J. The Association between Breastmilk Glucocorticoid Concentrations and Macronutrient Contents Throughout the Day. Nutrients. 2019;11:259. doi: 10.3390/nu11020259.
    1. Moran-Lev H., Mimouni F., Ovental A., Mangel L., Mandel D., Lubetzky R. Circadian Macronutrients Variations over the First 7 Weeks of Human Milk Feeding of Preterm Infants. Breastfeed. Med. 2015;10:366–370. doi: 10.1089/bfm.2015.0053.
    1. Arthur P., Kent J.C., Hartmann P. Metabolites of Lactose Synthesis in Milk from Women During Established Lactation. J. Pediatr. Gastroenterol. Nutr. 1991;13:260–266. doi: 10.1097/00005176-199110000-00004.
    1. Lammi-Keefe C.J., Ferris A.M., Jensen R.G. Changes in Human Milk at 0600, 1000, 1400, 1800, and 2200 h. J. Pediatr. Gastroenterol. Nutr. 1990;11:83–88. doi: 10.1097/00005176-199007000-00017.
    1. Cannon A.M., Kakulas F., Hepworth A.R., Lai C.T., Hartmann P., Geddes D.T. The Effects of Leptin on Breastfeeding Behaviour. Int. J. Environ. Res. Public Health. 2015;12:12340–12355. doi: 10.3390/ijerph121012340.
    1. Khan S., Hepworth A.R., Prime D.K., Lai C.T., Trengove N.J., Hartmann P.E. Variation in fat, lactose, and protein composition in breast milk over 24 hours: Associations with infant feeding patterns. J. Hum. Lact. 2013;29:81–89. doi: 10.1177/0890334412448841.
    1. Viverge D., Grimmonprez L., Cassanas G., Bardet L., Solère M. Diurnal Variations and within the Feed in Lactose and Oligosaccharides of Human Milk. Ann. Nutr. Metab. 1986;30:196–209. doi: 10.1159/000177194.
    1. Suryawan A., Davis T.A. Regulation of protein synthesis by amino acids in muscle of neonates. Front. Biosci. 2011;16:1445–1460. doi: 10.2741/3798.
    1. Hall B. Uniformity of human milk. Am. J. Clin. Nutr. 1979;32:304–312. doi: 10.1093/ajcn/32.2.304.
    1. West K.D., Kirksey A. Influence of vitamin B6 intake on the content of the vitamin in human milk. Am. J. Clin. Nutr. 1976;29:961–969. doi: 10.1093/ajcn/29.9.961.
    1. Khan S., Casadio Y.S., Lai C.T., Prime D.K., Hepworth A.R., Trengove N.J., Hartmann P. Investigation of Short-term Variations in Casein and Whey Proteins in Breast Milk of Term Mothers. J. Pediatr. Gastroenterol. Nutr. 2012;55:136–141. doi: 10.1097/MPG.0b013e31824cf386.
    1. Massmann P.F., França E.L., de Souza E.G., Souza M.S., Brune M.F.S.S., Honorio-França A.C. Maternal hypertension induces alterations in immunological factors of colostrum and human milk. Front. Life Sci. 2013;7:155–163. doi: 10.1080/21553769.2013.876451.
    1. López C.L.S., Hernández A., Rodríguez A.B., Rivero M., Barriga C., Cubero J. Nitrogen and protein content analysis of human milk, diurnality vs nocturnality. Nutr. Hosp. 2011;26:511–514.
    1. Clark R., Ross S., Hill D., Ferris A. Within-Day Variation of Taurine and Other Nitrogen Substances in Human Milk. J. Dairy Sci. 1987;70:776–780. doi: 10.3168/jds.S0022-0302(87)80073-5.
    1. LaVine M., Clark R., Hundrieser K., Ferris A. Within-Day Variation of Lipolytic Activity in Human Milk. J. Dairy Sci. 1986;69:1784–1786. doi: 10.3168/jds.S0022-0302(86)80601-4.
    1. Graf M.V., Hunter C.A., Kastin A.J. Presence of delta-sleep-inducing peptide-like material in human milk. J. Clin. Endocrinol. Metab. 1984;59:127–132. doi: 10.1210/jcem-59-1-127.
    1. Freed L.M., Neville M.C., Hamosh P., Hamosh M. Diurnal and within-feed variations in lipase activity and triglyceride content of human milk. J. Pediatr. Gastroenterol. Nutr. 1986;5:938–942. doi: 10.1097/00005176-198611000-00021.
    1. Katzer D., Pauli L., Mueller A., Reutter H., Reinsberg J., Fimmers R., Bartmann P., Bağci S. Melatonin concentrations and antioxidative capacity of human breast milk according to gestational age and the time of day. J. Hum. Lact. 2016;32:NP105–NP110. doi: 10.1177/0890334415625217.
    1. Hegardt P., Lindberg T., Börjesson J., Skude G. Amylase in human milk from mothers of preterm and term infants. J. Pediatr. Gastroenterol. Nutr. 1984;3:563–566. doi: 10.1097/00005176-198409000-00015.
    1. Sánchez C.L., Barriga C., Rodríguez A.B. Handbook of Nutrition, Diet and Sleep. Wageningen Academic Publishers; Wageningen, The Netherlands: 2013. Human milk nucleotides improve sleep: A focus on circadian profiles.
    1. França E.L., Nicomedes T.D.R., Calderon I.M., Honorio-França A.C. Time-dependent alterations of soluble and cellular components in human milk. Biol. Rhythm. Res. 2010;41:333–347. doi: 10.1080/09291010903407441.
    1. Spencer S.A., Hull D. Fat content of expressed breast milk: A case for quality control. BMJ. 1981;282:99–100. doi: 10.1136/bmj.282.6258.99.
    1. Gunther M., Stanier J. Diurnal variation in the fat content of breast-milk. Lancet. 1949;254:235–237. doi: 10.1016/S0140-6736(49)91242-8.
    1. Jackson D.A., Imong S.M., Silprasert A., Ruckphaopunt S., Woolridge M.W., Baum J.D., Amatayakul K. Circadian variation in fat concentration of breast-milk in a rural northern Thai population. Br. J. Nutr. 1988;59:349–363. doi: 10.1079/BJN19880044.
    1. Jensen R.G., Lammi-Keefe C.J., Ferris A.M., Jackson M.B., Couch S.C., Capacchione C.M., Ahn H.S., Murtaugh M. Human milk total lipid and cholesterol are dependent on interval of sampling during 24 hours. J. Pediatr. Gastroenterol. Nutr. 1995;20:91–94. doi: 10.1097/00005176-199501000-00015.
    1. Kociszewska-Najman B., Borek-Dzieciol B., Szpotanska-Sikorska M., Wilkos E., Pietrzak B., Wielgos M. The creamatocrit, fat and energy concentration in human milk produced by mothers of preterm and term infants. J. Matern. Neonatal Med. 2012;25:1599–1602. doi: 10.3109/14767058.2011.648239.
    1. Lubetzky R., Littner Y., Mimouni F.B., Dollberg S., Mandel D. Circadian variations in fat content of expressed breast milk from mothers of preterm infants. J. Am. Coll. Nutr. 2006;25:151–154. doi: 10.1080/07315724.2006.10719526.
    1. Lubetzky R., Mimouni F., Dollberg S., Salomon M., Mandel D. Consistent circadian variations in creamatocrit over the first 7 weeks of lactation: A longitudinal study. Breastfeed. Med. 2007;2:15–18. doi: 10.1089/bfm.2006.0013.
    1. Mes J., Davies D.J. Variation in the polychlorinated biphenyl and organochlorine pesticide residues during human breastfeeding and its diurnal pattern. Chemosphere. 1978;7:699–706. doi: 10.1016/0045-6535(78)90106-6.
    1. Picciano M.F., Guthrie H.A. Copper, iron, and zinc contents of mature human milk. Am. J. Clin. Nutr. 1976;29:242–254. doi: 10.1093/ajcn/29.3.242.
    1. Stafford J., Villalpando S., Aguila B.U. Circadian variation and changes after a meal in volume and lipid production of human milk from rural mexican women. Ann. Nutr. Metab. 1994;38:232–237. doi: 10.1159/000177816.
    1. Kent J.C., Mitoulas L.R., Cregan M.D., Geddes D.T., Doherty R.A., Hartmann P. Volume and frequency of breastfeedings and fat content of breast milk throughout the day. Pediatrics. 2006;117:387–395. doi: 10.1542/peds.2005-1417.
    1. Harzer G., Haug M., Dieterich I., Gentner P.R. Changing patterns of human milk lipids in the course of the lactation and during the day. Am. J. Clin. Nutr. 1983;37:612–621. doi: 10.1093/ajcn/37.4.612.
    1. Delplanque B., Gibson R., Koletzko B., Lapillonne A., Strandvik B. Lipid quality in infant nutrition: Current knowledge and future opportunities. J. Pediatr. Gastroenterol. Nutr. 2015;61:8–17. doi: 10.1097/MPG.0000000000000818.
    1. Ruel M.T., Dewey K.G., Martinez C., Flores R., Brown K.H. Validation of single daytime samples of human milk to estimate the 24-h concentration of lipids in urban Guatemalan mothers. Am. J. Clin. Nutr. 1997;65:439–444. doi: 10.1093/ajcn/65.2.439.
    1. Picciano M.F., Guthrie H.A., Sheehe D.M. The cholesterol content of human milk. A variable constituent among women and within the same woman. Clin. Pediatr. 1978;17:359–362. doi: 10.1177/000992287801700412.
    1. Guthrie H.A., Picciano M.F., Sheehe D. Fatty acid patterns of human milk. J. Pediatr. 1977;90:39–41. doi: 10.1016/S0022-3476(77)80761-0.
    1. Mitoulas L.R., Gurrin L.C., Doherty D.A., Sherriff J.L., Hartmann P.E. Infant intake of fatty acids from human milk over the first year of lactation. Br. J. Nutr. 2003;90:979–986. doi: 10.1079/BJN2003979.
    1. Mitoulas L.R., Kent J.C., Cox D.B., Owens R.A., Sherriff J.L., Hartmann P. Variation in fat, lactose and protein in human milk over 24h and throughout the first year of lactation. Br. J. Nutr. 2002;88:29–37. doi: 10.1079/BJN2002579.
    1. Zeisel S.H., Char D., Sheard N.F. Choline, phosphatidylcholine and sphingomyelin in human and bovine milk and infant formulas. J. Nutr. 1986;116:50–58. doi: 10.1093/jn/116.1.50.
    1. Patton S., Huston G.E. Incidence and characteristics of cell pieces on human milk fat globules. Biochim. Biophys. Acta. 1988;965:146–153. doi: 10.1016/0304-4165(88)90050-5.
    1. Hampel D., Shahab-Ferdows S., Islam M.M., Peerson J.M., Allen L.H. Vitamin Concentrations in Human Milk Vary with Time within Feed, Circadian Rhythm, and Single-Dose Supplementation. J. Nutr. 2017;147:603–611. doi: 10.3945/jn.116.242941.
    1. Mock D.M., Mock N.I., Dankle J.A. Secretory Patterns of Biotin in Human Milk. J. Nutr. 1992;122:546–552. doi: 10.1093/jn/122.3.546.
    1. Barkova E.N., Nazarenko E.V., Zhdanova E.V. Diurnal variations in qualitative composition of breast milk in women with iron deficiency. Bull. Exp. Biol. Med. 2005;140:394–396. doi: 10.1007/s10517-005-0500-2.
    1. Trugo N.M., Sardinha F. Cobalamin and cobalamin-binding capacity in human milk. Nutr. Res. 1994;14:23–33. doi: 10.1016/S0271-5317(05)80364-1.
    1. Udipi S.A., Kirksey A., Roepke J.L. Diurnal variations in folacin levels of human milk: Use of a single sample to represent folacin concentration in milk during a 24-h period. Am. J. Clin. Nutr. 1987;45:770–779. doi: 10.1093/ajcn/45.4.770.
    1. Feeley R.M., Eitenmiller R.R., Jones J.B., Barnhart H. Copper, iron, and zinc contents of human milk at early stages of lactation. Am. J. Clin. Nutr. 1983;37:443–448. doi: 10.1093/ajcn/37.3.443.
    1. Silvestre M.D., Lagarda M.J., Farré R., Martínez-Costa C., Brines J., Molina A., Clemente G. A Study of Factors that May Influence the Determination of Copper, Iron, and Zinc in Human Milk During Sampling and in Sample Individuals. Biol. Trace Element Res. 2000;76:217–228. doi: 10.1385/BTER:76:3:217.
    1. Keenan B.S., Buzek S.W., Garza C., Potts E., Nichols B.L. Diurnal and longitudinal variations in human milk sodium and potassium: Implication for nutrition and physiology. Am. J. Clin. Nutr. 1982;35:527–534. doi: 10.1093/ajcn/35.3.527.
    1. Feeley R.M., Eitenmiller R.R., Jones J.B., Jr., Barnhart H. Calcium, phosphorus, and magnesium contents of human milk during early lactation. J. Pediatr. Gastroenterol. Nutr. 1983;2:262–267. doi: 10.1097/00005176-198302020-00009.
    1. Karra M.V., Kirksey A. Variation in Zinc, Calcium, and Magnesium Concentrations of Human Milk within a 24-Hour Period from 1 to 6 Months of Lactation. J. Pediatr. Gastroenterol. Nutr. 1988;7:100–106. doi: 10.1097/00005176-198801000-00019.
    1. Stawarz R., Formicki G., Massányi P. Daily fluctuations and distribution of xenobiotics, nutritional and biogenic elements in human milk in Southern Poland. J. Environ. Sci. Health Part A Toxic Hazard. Subst. Environ. Eng. 2007;42:1169–1175. doi: 10.1080/10934520701418680.
    1. Shaaban S.Y., El-Hodhod M.A.A., Nassar M.F., Hegazy A.E.-T., El-Arab S.E., Shaheen F.M. Zinc status of lactating Egyptian mothers and their infants: Effect of maternal zinc supplementation. Nutr. Res. 2005;25:45–53. doi: 10.1016/j.nutres.2004.10.006.
    1. Krebs N.F., Hambidge K.M., Jacobs M.A., Mylet S. Zinc in human milk: Diurnal and within-feed patterns. J. Pediatr. Gastroenterol. Nutr. 1985;4:227–229. doi: 10.1097/00005176-198504000-00012.
    1. Kirk A., Dyke J.V., Martin C.F., Dasgupta P.K. Temporal patterns in perchlorate, thiocyanate, and iodide excretion in human milk. Environ. Health Perspect. 2006;115:182–186. doi: 10.1289/ehp.9558.
    1. Lahesmaa P., Vilkki P. The iodine content of human milk in Finland. Acta Paediatr. 1960;49:371–376. doi: 10.1111/j.1651-2227.1960.tb07750.x.
    1. Bouglé D., Bureau F., Foucault P., Duhamel J.F., Müller G., Drosdowsky M. Molybdenum content of term and preterm human milk during the first 2 months of lactation. Am. J. Clin. Nutr. 1988;48:652–654. doi: 10.1093/ajcn/48.3.652.
    1. Anderson G., Vaillancourt C., Maes M., Reiter R.J. Breastfeeding and the gut-brain axis: Is there a role for melatonin? Biomol. Concepts. 2017;8:185–195. doi: 10.1515/bmc-2017-0009.
    1. Engler A.C., Hadash A., Shehadeh N., Pillar G. Breastfeeding may improve nocturnal sleep and reduce infantile colic: Potential role of breast milk melatonin. Eur. J. Pediatr. 2012;174:729–732. doi: 10.1007/s00431-011-1659-3.
    1. Honorio-França A.C., Hara C.C.P., Ormonde J.V.S., Nunes G.T., França E.L. Human colostrum melatonin exhibits a day-night variation and modulates the activity of colostral phagocytes. J. Appl. Biomed. 2013;11:153–162. doi: 10.2478/v10136-012-0039-2.
    1. Illnerova H., Buresova M., Presl J. Melatonin rhythm in human milk. J. Clin. Endocrinol. Metab. 1993;77:838–841.
    1. Molad M., Ashkenazi L., Gover A., Lavie-Nevo K., Zaltsberg-Barak T., Shaked-Mishan P., Soloveichik M., Kessel I., Rotschild A., Etzioni T. Melatonin Stability in Human Milk. Breastfeed. Med. 2019;14:680–682. doi: 10.1089/bfm.2019.0088.
    1. Pontes G.N., Cardoso E.C., Carneiro-Sampaio M.M.S., Markus R.P. Pineal melatonin and the innate immune response: The TNF-alpha increase after cesarean section suppresses nocturnal melatonin production. J. Pineal Res. 2007;43:365–371. doi: 10.1111/j.1600-079X.2007.00487.x.
    1. Pontes G.N., Cardoso E.C., Carneiro-Sampaio M.M.S., Markus R.P. Injury switches melatonin production source from endocrine (pineal) to paracrine (phagocytes)—Melatonin in human colostrum and colostrum phagocytes. J. Pineal Res. 2006;41:136–141. doi: 10.1111/j.1600-079X.2006.00345.x.
    1. Prentice A.M., Whitehead R.G. Breast-milk fat concentrations of rural African women. 1. Short-term variations within individuals. Br. J. Nutr. 1981;45:483–494. doi: 10.1079/BJN19810127.
    1. Silva N.A., Honorio-França A.C., Giachini F.R., Mores L., De Souza E.G., França E.L. Bioactive factors of colostrum and human milk exhibits a day-night variation. Am. J. Immunol. 2013;9:68–74. doi: 10.3844/ajisp.2013.68.74.
    1. Hollanders J.J., Dijkstra L.R., van Der Voorn B., Kouwenhoven S.M., Toorop A.A., van Goudoever J.B., Rotteveel J., Finken M.J. No Association between Glucocorticoid Diurnal Rhythm in Breastmilk and Infant Body Composition at 3 Months. Nutrients. 2019;11:2351. doi: 10.3390/nu11102351.
    1. Keenan B.S., Buzek S.W., Garza C. Cortisol and its possible role in regulation of sodium and potassium in human milk. Am. J. Physiol. Metab. 1983;244:E253–E261. doi: 10.1152/ajpendo.1983.244.3.E253.
    1. Pundir S., Wall C., Mitchell C.J., Thorstensen E.B., Lai C.T., Geddes D.T., Cameron-Smith D. Variation of Human Milk Glucocorticoids over 24 hour Period. J. Mammary Gland. Biol. Neoplasia. 2017;22:85–92. doi: 10.1007/s10911-017-9375-x.
    1. van Der Voorn B., De Waard M., van Goudoever J.B., Rotteveel J., Heijboer A.C., Finken M.J. Breast-milk cortisol and cortisone concentrations follow the diurnal rhythm of maternal hypothalamus-pituitary-adrenal axis activity. J. Nutr. 2016;146:2174–2179. doi: 10.3945/jn.116.236349.
    1. Hollanders J.J., van Der Voorn B., De Goede P., Toorop A.A., Dijkstra L.R., Honig A., Rotteveel J., Dolman K.M., Kalsbeek A., Finken M.J.J. Biphasic Glucocorticoid Rhythm in One-Month-Old Infants: Reflection of a Developing HPA-Axis? J. Clin. Endocrinol. Metab. 2019;105:e544. doi: 10.1210/clinem/dgz089.
    1. Cregan M.D., Mitoulas L.R., Hartmann P. Milk prolactin, feed volume and duration between feeds in women breastfeeding their full-term infants over a 24 h period. Exp. Physiol. 2002;87:207–214. doi: 10.1113/eph8702327.
    1. Cross N.A., Hillman L.S., Forte L.R. The effects of calcium supplementation, duration of lactation, and time of day on concentrations of parathyroid hormone-related protein in human milk: A pilot study. J. Hum. Lact. 1998;14:111–117. doi: 10.1177/089033449801400210.
    1. Goldsmith S.J., Dickson J.S., Barnhart H.M., Toledo R.T., Eiten-Miller R.R. IgA, IgG, IgM and Lactoferrin Contents of Human Milk During Early Lactation and the Effect of Processing and Storage. J. Food Prot. 1983;46:4–7. doi: 10.4315/0362-028X-46.1.4.
    1. Peitersen B., Bohn L., Andersen H. Quantitative determination of immunoglobulins, lysozyme, and certain electrolytes in breast milk during the entire period of lactation, during a 24-hour period, and in milk from the individual mammary gland. Acta Paediatr. 1975;64:709–717. doi: 10.1111/j.1651-2227.1975.tb03909.x.
    1. Morais T.C., Honorio-França A.C., Silva R.R., Fujimori M., Fagundes D.L.G., França E.L. Temporal fluctuations of cytokine concentrations in human milk. Biol. Rhythm. Res. 2015;46:811–821. doi: 10.1080/09291016.2015.1056434.
    1. Houghton M.R., Gracey M., Burke V., Bottrell C., Spargo R.M. Breast milk lactoferrin levels in relation to maternal nutritional status. J. Pediatr. Gastroenterol. Nutr. 1985;4:230–233. doi: 10.1097/00005176-198504000-00013.
    1. Moran J.R., Courtney M.E., Orth D.N., Vaughan R., Coy S., Mount C.D., Sherrell B.J., Greene H.L. Epidermal growth factor in human milk: Daily production and diurnal variation during early lactation in mothers delivering at term and at premature gestation. J. Pediatr. 1983;103:402–405. doi: 10.1016/S0022-3476(83)80412-0.
    1. Sánchez C.L., Cubero J., Sanchez J., Chanclón B., Rivero M., Rodríguez A.B., Barriga C. The possible role of human milk nucleotides as sleep inducers. Nutr. Neurosci. 2009;12:2–8. doi: 10.1179/147683009X388922.
    1. Skala J.P., Koldovský O., Hahn P. Cyclic nucleotides in breast milk. Am. J. Clin. Nutr. 1981;34:343–350. doi: 10.1093/ajcn/34.3.343.
    1. Cubero J., SĂĄnchez C.L., Bravo R., SĂĄnchez J., Rodriguez A.B., Rivero M., Barriga C. Analysis of the antioxidant activity in human milk, day vs night. Cell Membr. Free Radic. Res. 2010;2:36–37.
    1. Jackson J.G., Lien E.L., White S.J., Bruns N.J., Kuhlman C.F. Major Carotenoids in Mature human Milk: Longitudinal and Diurnal Patterns. J. Nutr. Biochem. 1998;9:2–7. doi: 10.1016/S0955-2863(97)00132-0.
    1. Floris I., Billard H., Boquien C.-Y., Joram-Gauvard E., Simon L., Legrand A., Boscher C., Rozé J., Bolaños-Jiménez F., Kaeffer B. MiRNA Analysis by Quantitative PCR in Preterm Human Breast Milk Reveals Daily Fluctuations of hsa-miR-16-5p. PLoS ONE. 2015;10:e0140488. doi: 10.1371/journal.pone.0140488.
    1. Qin Y., Shi W., Zhuang J., Liu Y., Tang L., Bu J., Sun J., Bei F. Variations in melatonin levels in preterm and term human breast milk during the first month after delivery. Sci. Rep. 2019;9:17984. doi: 10.1038/s41598-019-54530-2.
    1. Finger C. Caesarean section rates skyrocket in Brazil. Many women are opting for caesareans in the belief that it is a practical solution. Lancet. 2003;362:628. doi: 10.1016/S0140-6736(03)14204-3.
    1. Lönnerdal B. Trace Element Transport in the Mammary Gland. Annu. Rev. Nutr. 2007;27:165–177. doi: 10.1146/annurev.nutr.27.061406.093809.
    1. Sánchez S., Sánchez C.L., Paredes S.D., Rodriguez A.B., Barriga C. The effect of tryptophan administration on the circadian rhythms of melatonin in plasma and the pineal gland of rats. J. Appl. Biomed. 2008;6:177–186. doi: 10.32725/jab.2008.021.
    1. Kikuchi S., Nishihara K., Eto H., Horiuchi S., Hoshi Y. The influence of feeding method on a mother’s daily rhythm and on the development of her infant’s circadian restactivity rhythm. J. Sleep Res. 2012;21:332.

Source: PubMed

3
Subscribe