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Food Science and Human Wellness 2022, 11(5): 1419-1427 https://doi.org/10.1016/j.fshw.2022.04.033
Research Article | Open Access | Issue | Published: 02 June 2022

The levels of osteopontin in human milk of Chinese mothers and its associations with maternal body composition

Show Author's Information Huijuan Ruana,  Qingya Tanga,  Xuan Zhaoa,  Yajie Zhangb,  Xuelin Zhaoa,  Yi Xianga,  Wei Genga,  Yi Fenga,  Wei Caib,c( )
Department of Clinical Nutrition, Xinhua Hospital Affiliated to Shanghai Jiao Tong University School of Medicine, Shanghai 200092, China
Shanghai Key Laboratory of Pediatric Gastroenterology and Nutrition, Shanghai Institute of Pediatric Research, Xinhua Hospital Affiliated to Shanghai Jiao Tong University School of Medicine, Shanghai 200092, China
Department of Pediatric Surgery, Xinhua Hospital Affiliated to Shanghai Jiao Tong University School of Medicine, Shanghai 200092, China

Peer review under responsibility of KeAi Communications Co., Ltd.

Keywords:
Human milk, Osteopontin, Body composition, Breastfeeding
Cite this article:
Ruan H, Tang Q, Zhao X, et al. The levels of osteopontin in human milk of Chinese mothers and its associations with maternal body composition. Food Science and Human Wellness, 2022, 11(5): 1419-1427. https://doi.org/10.1016/j.fshw.2022.04.033
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Abstract Full text About this article
Objective

This study explored the content and change trend of osteopontin (OPN) in breast milk and analyzed the relationship between OPN in breast milk and maternal body composition.

Methods

Breast-feeding mothers were recruited in Xinhua Hospital to collect breast milk and provide pertinent information. The content of OPN in breast milk was determined by enzyme-linked immunosorbent assay (ELISA). Determination of protein content in human milk was performed via the BCA method. The maternal body composition was determined by the bioelectrical impedance method. Serum glucocorticoid receptor α, adiponectin, insulin, and leptin were determined by ELISA. SPSS 25 was used for statistical analysis.

Results

In the longitudinal cohort, 106 mothers provided 318 milk samples at different lactation periods. The results indicate that the OPN showed dynamic changes. OPN levels were (343.2 ± 163.5) mg/L during 114 days postpartum, (228.4 ± 121.5) mg/L during 24 months postpartum, and (204.8 ± 100.6) mg/L during 57 months postpartum. The content of OPN was very high in the first 114 days postpartum and then decreased. Compared with early postpartum milk, the OPN content of mature milk showed a significant relationship with maternal weight-related parameters. Additional body composition analysis was performed in 88 women at the mature milk phase. The results show that the OPN in milk is related to the mother's body composition, especially the content of skeletal muscle mass, but not to relevant humoral factors.

Conclusions

The levels of OPN in human milk of Chinese mothers showed dynamic changes with the extension of lactation time. The OPN in human milk was related to the mother's body composition but not related to related humoral factors.


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Abstract
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About this article

The levels of osteopontin in human milk of Chinese mothers and its associations with maternal body composition

Show Author's information Huijuan Ruana, Qingya Tanga, Xuan Zhaoa, Yajie Zhangb, Xuelin Zhaoa, Yi Xianga, Wei Genga, Yi Fenga, Wei Caib,c( )
Department of Clinical Nutrition, Xinhua Hospital Affiliated to Shanghai Jiao Tong University School of Medicine, Shanghai 200092, China
Shanghai Key Laboratory of Pediatric Gastroenterology and Nutrition, Shanghai Institute of Pediatric Research, Xinhua Hospital Affiliated to Shanghai Jiao Tong University School of Medicine, Shanghai 200092, China
Department of Pediatric Surgery, Xinhua Hospital Affiliated to Shanghai Jiao Tong University School of Medicine, Shanghai 200092, China

Peer review under responsibility of KeAi Communications Co., Ltd.

Abstract

Objective

This study explored the content and change trend of osteopontin (OPN) in breast milk and analyzed the relationship between OPN in breast milk and maternal body composition.

Methods

Breast-feeding mothers were recruited in Xinhua Hospital to collect breast milk and provide pertinent information. The content of OPN in breast milk was determined by enzyme-linked immunosorbent assay (ELISA). Determination of protein content in human milk was performed via the BCA method. The maternal body composition was determined by the bioelectrical impedance method. Serum glucocorticoid receptor α, adiponectin, insulin, and leptin were determined by ELISA. SPSS 25 was used for statistical analysis.

Results

In the longitudinal cohort, 106 mothers provided 318 milk samples at different lactation periods. The results indicate that the OPN showed dynamic changes. OPN levels were (343.2 ± 163.5) mg/L during 114 days postpartum, (228.4 ± 121.5) mg/L during 24 months postpartum, and (204.8 ± 100.6) mg/L during 57 months postpartum. The content of OPN was very high in the first 114 days postpartum and then decreased. Compared with early postpartum milk, the OPN content of mature milk showed a significant relationship with maternal weight-related parameters. Additional body composition analysis was performed in 88 women at the mature milk phase. The results show that the OPN in milk is related to the mother's body composition, especially the content of skeletal muscle mass, but not to relevant humoral factors.

Conclusions

The levels of OPN in human milk of Chinese mothers showed dynamic changes with the extension of lactation time. The OPN in human milk was related to the mother's body composition but not related to related humoral factors.

Keywords: Human milk, Osteopontin, Body composition, Breastfeeding

References(53)

[1]

L. Bo, Infant formula and infant nutrition: bioactive proteins of human milk and implications for composition of infant formulas, Am. J. Clin. Nutr. 99(2014) 712S. https://doi.org/10.3945/jn.114.197558.
DOI Google Scholar
[2]

R. Jiang, B. Lönnerdal, Biological roles of milk osteopontin, Curr. Opin. Clin. Nutr. Metab. Care 19 (2016) 214-219. https://doi.org/10.1097/MCO.0000000000000275.
DOI Google Scholar
[3]

R. Jiang, C. Prell, B. Lnnerdal, Milk osteopontin promotes brain development by up-regulating osteopontin in the brain in early life, FASEB J. 33 (2019) 1681-1694. https://doi.org/10.1096/fj.201701290RR.
DOI Google Scholar
[4]

S.M. Donovan, M.H. Monac, J. Drnevich, et al., Bovine osteopontin modifies the intestinal transcriptome of formula-fed infant rhesus monkeys to be more similar to those that were breastfed, J. Nutr. 144 (2014) 1910-1919. https://doi.org/10.3945/jn.114.197558.
DOI Google Scholar
[5]

R. Jiang, B. Lönnerdal, Osteopontin in human milk and infant formula affects infant plasma osteopontin concentrations, Pediatr. Res. 85 (2019)502-505. https://doi.org/10.1038/s41390-018-0271-x.
DOI Google Scholar
[6]

B. Depalle, C.M. McGilvery, S. Nobakhti, et al., Osteopontin regulates type I collagen fibril formation in bone tissue, Acta Biomater. 120 (2020) 194-202. https://doi.org/10.1016/j.actbio.2020.04.040.
DOI Google Scholar
[7]

K. Maniatis, G. Siasos, E. Oikonomou, et al., Osteoprotegerin and osteopontin serum levels are associated with vascular function and inflammation in coronary artery disease patients, Curr. Vasc. Pharmacol. 18(2020) 523-530. https://doi.org/10.2174/1570161117666191022095246.
DOI Google Scholar
[8]

D. Tousoulis, G. Siasos, K. Maniatis, et al., Serum osteoprotegerin and osteopontin levels are associated with arterial stiffness and the presence and severity of coronary artery disease, Int. J. Cardiol. 167 (2013) 1924-1928. https://doi.org/10.1016/j.ijcard.2012.05.001.
DOI Google Scholar
[9]

A.B. Tuck, F.P. O'Malley, H. Singhal, et al., Osteopontin and p53 expression are associated with tumor progression in a case of synchronous, bilateral, invasive mammary carcinomas, Arch. Pathol. Lab. Med. 121 (1997) 578-584. https://doi.org/10.1089/oli.1.1997.7.257.
DOI Google Scholar
[10]

H. Singhal, D.S. Bautista, K.S. Tonkin, et al, Elevated plasma osteopontin in metastatic breast cancer associated with increased tumor burden and decreased survival, Clin. Cancer Res. 3 (1997) 605-611.
Google Scholar
[11]

N. Shijubo, T. Uede, S. Kon, et al., Vascular endothelial growth factor and osteopontin in tumor' biology, Crit. Rev. Oncog. 11 (2000) 127-138. https://doi.org/10.3109/03008200009005293.
DOI Google Scholar
[12]

S. Philip, A. Bulbule, G.C. Kundu, Osteopontin stimulates tumor growth and activation of promatrix metalloproteinase-2 through nuclear factorκB-mediated induction of membrane type 1 matrix metalloproteinase in murine melanoma cells, J. Biol. Chem. 276 (2001) 44926-44935. https://doi.org/10.1074/jbc.M103334200.
DOI Google Scholar
[13]

P.Y. Wai, P.C. Kuo, The role of osteopontin in tumor metastasis, J. Surg. Res. 121(2) (2004) 228-241. https://doi.org/10.1016/j.jss.2004.03.028.
DOI Google Scholar
[14]

G. Chakraborty, S. Jain, R. Behera, et al., The multifaceted roles of osteopontin in cell signaling, tumor progression and angiogenesis, Curr. Mol. Med. 6 (2006) 819-830. https://doi.org/10.2174/156652406779010803.
DOI Google Scholar
[15]

S.S. Mcallister, A.M. Gifford, A.L. Greiner, et al., Systemic endocrine instigation of indolent tumor growth requires osteopontin, Cell 133 (2008)994-1005. https://doi.org/10.1016/j.cell.2008.04.045.
DOI Google Scholar
[16]

C. Donald, H. Cao, K. Shirley, et al., The RGD domain of human osteopontin promotes tumor growth and metastasis through activation of survival pathways, PLoS One 5 (2010) e9633. https://doi.org/10.1371/journal.pone.0009633.
DOI Google Scholar
[17]

Y. Sharon, Y. Raz, N. Cohen, et al., Tumor-derived osteopontin reprograms normal mammary fibroblasts to promote inflammation and tumor growth in breast cancer, Cancer Res. 75 (2015) 963-973. https://doi.org/10.1158/0008-5472.CAN-14-1990.
DOI Google Scholar
[18]

X. Ge, Y. Lu, T.M. Leung, et al., Milk osteopontin, a nutritional approach to prevent alcohol-induced liver injury, Am. J. Physiol. Gastrointest. Liver Physiol. 304(10) (2013) G929-G939. https://doi.org/10.1152/ajpgi.00014.2013.
DOI Google Scholar
[19]

J. Zhang, A. Zhao, S. Lai, et al., Longitudinal changes in the concentration of major human milk proteins in the first six months of lactation and their effects on infant growth, Nutrients 13 (2021) 1476. https://doi.org/10.3390/nu13051476.
DOI Google Scholar
[20]

Q. Ren, Y. Zhou, W. Zhang, et al., Longitudinal changes in the bioactive proteins in human milk of the Chinese population: a systematic review, Food Sci. Nutr. 9(8) (2020) 25-35. https://doi.org/10.1002/fsn3.2061.
DOI Google Scholar
[21]

R. Jiang, L. Bo, Effects of milk osteopontin on intestine, neurodevelopment, and immunity, Nestle Nutr. Inst. Workshop Ser. 94 (2020) 152-157. https://doi.org/10.1159/000505067.
DOI Google Scholar
[22]

N. Nourkami-Tutdibi, N. Graf, R. Beier, et al., Plasma levels of osteopontin from birth to adulthood, Pediatr. Blood Cancer 67(7) (2020) e28272. https://doi.org/10.1002/pbc.28272.
DOI Google Scholar
[23]

S. Bruun, L.N. Jacobsen, X. Ze, et al., Osteopontin levels in human milk vary across countries and within lactation period: data from a multicenter study, J. Pediatr. Gastroenterol. Nutr. 67(2) (2018) 250-256. https://doi.org/10.1097/MPG.0000000000002004.
DOI Google Scholar
[24]

D.E.W. Chatterton, D.N. Nguyen, S.B. Bering, et al., Anti-inflammatory mechanisms of bioactive milk proteins in the intestine of newborns, Int. J. Biochem. Cell. Biol. 45(8) (2013) 1730-1747. https://doi.org/10.1016/j.biocel.2013.04.028.
DOI Google Scholar
[25]

R. Jiang, C. Prell, B. Lönnerdal, Milk osteopontin promotes brain development by up-regulating osteopontin in the brain in early life, FASEB J. 33 (2019) 1681-1694. https://doi.org/10.1096/fj.201701290RR.
DOI Google Scholar
[26]

L. Schack, A. Lange, J. Kelsen, et al., Considerable variation in the concentration of osteopontin in human milk, bovine milk, and infant formulas, J. Dairy Sci. 92(11) (2009) 5378-5385. https://doi.org/10.3168/jds.2009-2360.
DOI Google Scholar
[27]

D. Hans, P. Christine, T. Niklas, et al., Bene fits of lactoferrin, osteopontin and milk fat globule membranes for infants, Nutrients 9(8) (2017) 817. https://doi.org/10.3390/nu9080817.
DOI Google Scholar
[28]

A.S. Goldman, C. Garza, B.L. Nichols, et al., Immunologic factors in human milk during the first year of lactation, J. Pediatr. 100(4) (1982) 563-567. https://doi.org/10.1016/s0022-3476(82)80753-1.
DOI Google Scholar
[29]

J.S. You, H. Ji, K.J. Chang, et al., Serum osteopontin concentration is decreased by exercise-induced fat loss but is not correlated with body fat percentage in obese humans, Mol. Med. Rep. 8(2) (2013) 579-584. https://doi.org/10.3892/mmr.2013.1522.
DOI Google Scholar
[30]

R.B. Dell, S. Holleran, R. Ramakrishnan, Sample size determination, ILAR J. 43(4) (2002) 207-213. https://doi.org/10.1093/ilar.43.4.207.
DOI Google Scholar
[31]

T.R. Fenton, J.H. Kim, A systematic review and meta-analysis to revise the Fenton growth chart for preterm infants, BMC Pediatrics. 13(1) (2013) 59-59. https://doi.org/10.1186/1471-2431-13-59.
DOI Google Scholar
[32]

J.L. LaBarre, M. Puttabyatappa, P.X.K. Song, et al., Maternal lipid levels across pregnancy impact the umbilical cord blood lipidome and infant birth weight, Sci. Rep. 10(1) (2020) 14209. https://doi.org/10.1038/s41598-020-71081-z.
DOI Google Scholar
[33]

M.J. Rosa, A. Pajak, A.C. Just, et al, Prenatal exposure to PM(2.5) and birth weight: a pooled analysis from three North American longitudinal pregnancy cohort studies, Environ. Int. 107 (2017) 173-180. https://doi.org/10.1016/j.envint.2017.07.012.
DOI Google Scholar
[34]

L. Bo, L.R. Woodhouse, C. Glazier, Compartmentalization and quantitation of protein in human milk, J. Nutr. 117(8) (1987) 1385-1395. https://doi.org/10.1093/jn/117.8.1385.
DOI Google Scholar
[35]

K.M. Abu, M.J. Mccutcheon, S. Reddy, et al., Electrical impedance in assessing human body composition: the BIA method, Am. J. Clin. Nutr. 5(1988) 789-792. https://doi.org/10.1093/ajcn/47.5.789.
DOI Google Scholar
[36]

C. Robinson, R.E. Schumacker, Interaction effects: centering, variance inflation factor, and interpretation issues, Multiple Linear Regression Viewpoints 35(1) (2009) 1-11.
Google Scholar
[37]

K.E. Joung, H. Christou, K.H. Park, et al., Cord blood levels of osteopontin as a phenotype marker of gestational age and neonatal morbidities, Obesity 22(5) (2014) 1317-1324. https://doi.org/10.1002/oby.20626.
DOI Google Scholar
[38]

C.E. West, A.S. Kvistgaard, J.M. Peerson, et al., Effects of osteopontinenriched formula on lymphocyte subsets in the first 6 months of life: a randomized controlled trial, Pediatr. Res. 82(1) (2017) 63-71.https://doi.org/10.1038/pr.2017.77.
DOI Google Scholar
[39]

A. Aksan, I. Erdal, S.S. Yalcin, et al., Osteopontin levels in human milk are related to maternal nutrition and infant health and growth, Nutrients 13(8)(2021) 2670. https://doi.org/10.3390/nu13082670.
DOI Google Scholar
[40]

R. Miranda, N.G. Saravia, R. Ackerman, et al., Effect of maternal nutritional status on immunological substances in human colostrum and milk, Am. J.Clin. Nutr. 37 (1983) 632-640. https://doi.org/10.1093/ajcn/37.4.632.
DOI Google Scholar
[41]

Y. Hirai, N. Kawakata, K. Satoh, et al., Concentrations of lactoferrin and iron in human milk at different stages of lactation, J. Nutr. Sci. Vitaminol.(Tokyo) 36(6) (1990) 531-544. https://doi.org/10.3177/jnsv.36.531.
DOI Google Scholar
[42]

J. Bauer, J. Gerss, Longitudinal analysis of macronutrients and minerals in human milk produced by mothers of preterm infants, Clin. Nutr. 30 (2011)215-220. https://doi.org/10.1016/j.clnu.2010.08.003.
DOI Google Scholar
[43]

F. Carbone, G. Adami, L. Liberale, et al., Serum levels of osteopontin predict diabetes remission after bariatric surgery, Diabetes Metab. 45 (2019) 356-362. https://doi.org/10.1016/j.diabet.2018.09.007.
DOI Google Scholar
[44]

C. Wang, M. He, J. Peng, et al., Increased plasma osteopontin levels are associated with nonalcoholic fatty liver disease in patients with type 2 diabetes mellitus, Cytokine 125 (2019) 154837-154837.https://doi.org/10.1016/j.cyto.2019.154837.
DOI Google Scholar
[45]

H.A. Motlagh, E.H. Aalipanah, M. Mazidi, et al., Effect of flaxseed consumption on central obesity, serum lipids, and adiponectin level in overweight or obese women: a randomized controlled clinical trial, Int. J.Clin. Pract. 75 (2021) e14592. https://doi.org/10.1111/ijcp.14592.
DOI Google Scholar
[46]

D.H. Lee, J.A. Lim, J.H. Kim, et al., Longitudinal changes of high molecular weight adiponectin are associated with postpartum development of type 2 diabetes mellitus in patients with gestational diabetes mellitus, Endocrinol. Metab. (Seoul) 36(1) (2021) 114-122. https://doi.org/10.3803/EnM.2020.831.
DOI Google Scholar
[47]

M. Khazaei, Z. Tahergorabi, Leptin and its cardiovascular effects: Focus on angiogenesis, Adv. Biomed. Res. 4(79) (2015) 79.https://doi.org/10.4103/2277-9175.156526.
DOI Google Scholar
[48]

A.R. Volkova, G. Semikova, M. Fishman, Thyroid stimulating hormone, insulin resistance and leptin in patients with obesity after bariatric surgery, Endocrine Abstracts (2020). https://doi.org/10.1530/endoabs.70.AEP434.
DOI Google Scholar
[49]

M. Werdermann, I. Berger, L.D. Scriba, et al., Insulin and obesity transforms hypothalamic-pituitary-adrenal axis stemness and function in a hyperactive state, Mol. Metab. 43 (2020) 101112. https://doi.org/10.1016/j.molmet.2020.101112.
DOI Google Scholar
[50]

B. Antuna-Puente, B. Feve, S. Fellahi, et al., Adipokines: the missing link between insulin resistance and obesity, Diabetes Metab. 34(1) (2008) 2-11.https://doi.org/10.1016/j.diabet.2007.09.004.
DOI Google Scholar
[51]

K. John, J.S. Marino, E.R. Sanchez, et al., The glucocorticoid receptor: cause or cure for obesity? Am. J. Physiol. Endocrinol. Metab. 310(4) (2015) E249.https://doi.org/10.1152/ajpendo.00478.2015.
DOI Google Scholar
[52]

G.F.P. Aleixo, S.S. Shachar, K.A. Nyrop, et al., Bioelectrical Impedance analysis for the assessment of sarcopenia in patients with cancer: a systematic review, Oncologist 25(2) (2020) 170-182. https://doi.org/10.1634/theoncologist.2019-0600.
DOI Google Scholar
[53]

P. Sheean, M.C. Gonzalez, C.M. Prado, et al., American society for parenteral and enteral nutrition clinical guidelines: the validity of body composition assessment in clinical populations, J. Parenter Enteral. Nutr. 44(1) (2020) 12-43. https://doi.org/10.1002/jpen.1669.
DOI Google Scholar
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Publication history

Received: 07 September 2021
Revised: 10 October 2021
Accepted: 04 November 2021
Published: 02 June 2022
Issue date: September 2022

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© 2022 Beijing Academy of Food Sciences.

Acknowledgements

Acknowledgement

This study was supported by grants from the Shanghai Key Laboratory of Pediatric Gastroenterology and Nutrition (17dz2272000) and the National Natural Science Foundation of China-Key Program (81630039).

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This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

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