Survival and composition of the cellular component of breast milk under various conditions of its expression and storage

Ryumina I.I., Fatkhudinov T.Kh., Arutyunyan I.V., Makarov A.V., Lokhonina A.V., Narogan M.V., Sharipova K.R., Orlovskaya I.V., Zubkov V.V., Baibarina E.N.

1) Academician V.I. Kulakov National Medical Research Center of Obstetrics, Gynecology, and Perinatology, Ministry of Health of Russia, Moscow, Russia; 2) Research Institute of Human Morphology, Moscow, Russia; 3) I.M. Sechenov First Moscow State Medical University (Sechenov University), Ministry of Health of Russia, Moscow, Russia
Objective. To determine the composition and survival of the cellular component of breast milk under various conditions of its single and double pumping and storage.
Materials and methods. Eighty-six breast milk samples were collected using a Symphony Medela single (n = 63) or double (n = 23) clinical breast pump. Each sample was divided into two halves and stored for 72 hours when it was cooled to 4°C or room temperature. The fractions of living cells were assessed at 4, 24, and 72 hours after breast milk expression. Flow cytofluorometry was used to determine the expression of specific surface and intracellular markers.
Results. The total number of cells in breast milk did not depend on the method of its expression, gestational age, or number of fetuses; the median was about 80,000 cells per ml. The main milk cell populations were epithelial cells and white blood cells; vimentin-positive stromal cells were a minor population. The storage of breast milk, regardless of its expression method, led to a gradual decrease in the number of living cells due to the partial death of short-lived leukocyte subpopulations. After 4 hours, about a third of all cells remained alive; cooling the milk to +4°C could prolong the period of this level of cell survival. Moreover, this effect was more pronounced in the samples obtained using a double clinical breast pump.
Conclusion. The total number of cells in breast milk does not depend on its expression method, gestational age, or number of fetuses. To preserve the cellular component of the expressed breast milk, the latter can be stored at room temperature for the first 4 hours when it was cooled to +4°C for 24 hours; in this case double pumping has some advantage over single pumping.

Keywords

breast milk
cells
storage mode
breast pump
single pumping
double pumping

References

  1. Hassiotou F., Twigger A., Hartmann P.E., Hodgetts S., Filgueira L. Neural differentiation of human breastmilk stem cells. Paper presented at: International Society for Research in Human Milk and Lactation; 2012; Trieste, Italy.
  2. Weiler I.J., Hickler W., Sprenger R. Demonstration that milk cells invade the suckling neonatal mouse. Am J Reprod Immunol. 1983; 4(2): 95–8. doi: 10.1111/j.1600-0897.1983.tb00261.x
  3. Zhou L., Yoshimura Y., Huang Y., Suzuki R., Yokoyama M., Okabe M., Shimamura M. Two independent pathways of maternal cell transmission to offspring: through placenta during pregnancy and by breast-feeding after birth. Immunology. 2000; 101(4): 570–81. doi: 10.1046/j.1365-2567.2000.00144.x
  4. Hassiotou F., Hepworth A.R., Metzger P., Tat Lai C., Trengove N., Hartmann P.E., et al. Maternal and infant infections stimulate a rapid leukocyte response in breastmilk. Clin Transl Immunol. 2013; 2(4): e3. doi: 10.1038/cti.2013.1
  5. Twigger A.J., Hodgetts S., Filgueira L., Hartmann P.E., Hassiotou F. From breast milk to brains: the potential of stem cells in human milk. J Hum Lact. 2013; 29(2): 136–9. doi: 10.1177/0890334413475528.
  6. Twigger A.J., Hepworth A.R., Lai C.T., Chetwynd E., Stuebe A.M., Blancafort P., et al. Gene expression in breastmilk cells is associated with maternal and infant characteristics. Sci Rep. 2015; 5: 12933. doi: 10.1038/srep12933.
  7. Sani M., Hosseini S.M., Salmannejad M., Aleahmad F., Ebrahimi S., Jahanshahi S., Talaei-Khozani T. Origins of the breast milk-derived cells; an endeavor to find the cell sources. Cell Biol Int. 2015; 39(5): 611-8. http://dx.doi.org/10.1002/cbin.10432
  8. Meier P.P., Engstrom J.L., Janes J.E., Jegier B.J., Loera F. Breast pump suction patterns that mimic the human infant during breastfeeding: Greater milk output in less time spent pumping for breast pump-dependent mothers with premature infants. J Perinatol. 2012; 32: 103–10. doi: 10.1038/jp.2011.64.
  9. Eglash A., Simon L.; Academy of Breastfeeding Medicine. ABM Clinical Protocol #8: Human Milk Storage Information for Home Use for Full-Term Infants, Revised 2017. Breastfeed Med. 2017; 12(7): 390–5. doi: 10.1089/bfm.2017.29047.aje.
  10. Jones F. Best Practice for Expressing, Storing and Handling Human Milk in Hospitals, Homes and Child Care Settings, Second Edition. The Human Milk Banking Association of NorthAmerica, (HMBANA). 3rd edition, 2011.
  11. ВОЗ. Руководство по грудному вскармливанию. Хранение сцеженного молока, 1997. [WHO. Breastfeeding Guide. Storage of expressed milk, 1997. (in Russian)].
  12. Родригес Х.М. Микробиота женского молока. Consilium medicum/ Педиатрия, 2016; 4: 35-40. [Rodríguez J.M. The human milk microbiota. Consilium Medicum. Pediatrics (Suppl.). 2016; 4: 35–40. (in Russian)]
  13. Prime D.K., Garbin C.P., Hartmann P.E., Kent J.C. Simultaneous breast expression in breastfeeding women is more efficacious than sequential breast expression. Breastfeed Med. 2012; 7: 442–7. doi: 10.1089/bfm.2011.0139
  14. Jones E., King C., Spencer A. Feeding and Nutrition in the Preterm Infant. Edinburgh. New York: Elsevier Churchill Livingstone, 2005. 205 р.
  15. Slutzah M., Codipilly C.N., Potak D., et al. Refrigerator storage of expressed human milk in the neonatl intensive care unit. J Pediatr. 2010; 156: 26–8. doi: 10.1016/j.jpeds.2009.07.023.
  16. СанПиН 2.1.3.2630-10. Санитарно-эпидемиологические требования к организациям, осуществляющим медицинскую деятельность. [SanPiN 2.1.3.2630-10. Sanitarno-epidemiologicheskiye trebovaniya k organizatsiyam, osushchestvlyayushchim meditsinskuyu deyatel’nost’. (in Russian)].
  17. Fan Y., Chong Y.S., Choolani M.A., Cregan M.D., Chan J.K.Y. Unravelling the Mystery of Stem/Progenitor Cells in Human Breast Milk. PLoS ONE. 2010; 5(12): e14421. https://doaj.org/article/3c23575beeb14201af7df8e124
  18. Indumathi S., Dhanasekaran M., Rajkumar J.S., Sudarsanam D. Exploring the stem cell and non-stem cell constituents of human breast milk. Cytotechnology. 2013; 65(3): 385–93. doi: 10.1007/s00464-014-3917-8
  19. Hassiotou F., Hartmann P.E. At the Dawn of a New Discovery: The Potential of Breast Milk Stem Cells. Adv Nutr. 2014; 5(6): 770–8. doi: 10.3945/an.114.006924.
  20. Pechoux C., Gudjonsson T., Ronnov-Jessen L., Bissell M.J., Petersen O.W. Human mammary luminal epithelial cells contain progenitors to myoepithelial cells. Dev Biol. 1999; 206: 88–99. doi: 10.1006/dbio.1998.9133
  21. Thomas E., Zeps N., Cregan M., Hartmann P., Martin T. 14-3-3σ (sigma) regulates proliferation and differentiation of mmultipotentp63-positive cells isolated from human breastmilk. CellCycle. 2011; 10(2): 1–7. DOI: 10.4161/cc.10.2.14470
  22. Hassiotou F., Geddes D.T., Hartmann P.E. Cells in human milk: state of the science. J Hum Lact. 2013; 29(2): 171–82. doi: 10.1177/0890334413477242.
  23. Patki S., Kadam S., Chandra V., Bhonde R. Human breast milk is a rich source of multipotent mesenchymal stem cells. Human Cell. 2010; 23(2): 35–40. doi: 10.1111/j.1749-0774.2010.00083.x.
  24. Sani M., Hosseini S.M., Salmannejad M., Aleahmad F., Ebrahimi S., Jahanshahi S., Talaei-Khozani T. Origins of the breast milk-derived cells; an endeavor to find the cell sources. Cell Biol Int. 2015; 39(5): 611–8. http://dx.doi.org/10.1002/cbin.10432
  25. Goldman A.S., Chheda S., Garofalo R. Spectrum of immunomodulating agents in human milk. Int J Pediatr. 1997, 4: 491.
  26. Jin Y.Y., Wei Zhao, Cao R.M, Xi Wang, Wu S.M., Chen T.X. Characterization of immunocompetent cells in human milk of Han Chinese. J Hum Lact. 2011; 27(2): 155-62. doi: 10.1177/0890334410392041.
  27. Hamprecht K., Maschmann J., Vochem M., Dietz K., Speer C.P., Jahn G. Epidemiology of transmission of cytomegalovirus from mother to preterm infant by breastfeeding. Lancet. 2001; 357: 513–8. DOI: 10.1016/S0140-6736(00)04043-5

Received 13.11.2019

Accepted 29.11.2019

About the Authors

Irina I. Ryumina, MD, Head of the Department of Pathology of Newborns and Premature Children, Scientific and Research Center for Microbiology, AGP named after Academician V.I. Kulakova “Ministry of Health of Russia. Tel.: +7 (903) 7708048. E-mail: i_ryumina@oparina4.ru
Address: 117997, Russia, Moscow, ul. Academician Oparin, d. 4.
Timur Kh. Fatkhudinov, MD, Deputy Director for Scientific Development, Federal State Budget Scientific Institution Scientific Research Institute of Human Morphology, Leading Scientific Researcher at the Laboratory of Regenerative Medicine, Scientific Research Center for Scientific and Applied Mathematics Academician V.I. Kulakova Ministry of Health of Russia. Tel.: +7 (903)256-11-57. E-mail: tfat@yandex.ru. ORCID iD 0000-0002-6498-5764.
Address: 117997, Russia, Moscow, ul. Academician Oparin, d. 4.
Irina V. Arutyunyan, Ph.D., Senior Researcher, Laboratory of Regenerative Medicine, Scientific Research Center of Medical Sciences named after A.P. Academician V.I. Kulakova “Ministry of Health of Russia, NS growth and development laboratories of FSBI NIIMCH. Tel.: +7 (926)147-44-30. E-mail: labrosta@yandex.ru.
ORCID iD 0000-0002-4344-8943.
Address: 117997, Russia, Moscow, ul. Academician Oparin, d. 4.
Andrey V. Makarov, candidate of medical sciences, senior researcher at the Laboratory of Regenerative Medicine of the Scientific and Research Center “AGP named
after Academician V.I. Kulakova “Ministry of Health of Russia. Tel.: +7 (903) 256-34-04. E-mail: anvitmak@yandex.ru. ORCID iD 0000-0003-2133-2293.
Address: 117997, Russia, Moscow, ul. Academician Oparin, d. 4.
Anastasia V. Lokhonina, Researcher at the Laboratory of Regenerative Medicine, Russian Research Center for Medical Research “AGP named after Academician V.I. Kulakova of the Ministry of Health of Russia. Tel.: +7 (910)431-66-76. Email: nastya.serbsky@gmail.com. ORCID ID: 0000-0001-8077-2307.
Address: 117437, Russia, Moscow, ul. Academician Oparin, d. 4.
Marina V. Narogan, MD, Leading Researcher, Department of Pathology of Newborns and Premature Children, NICC “AGP named after Academician V.I. Kulakova
“Ministry of Health of Russia; Professor, Department of Neonatology, Federal State Autonomous Educational Institution of Higher Education “First MGMU named
after THEM. Sechenov »Ministry of Health of Russia (Sechenov University). Tel.: +7 (905) 5501621. E-mail: m_narogan@oparina4.ru
Address: 117997, Russia, Moscow, ul. Academician Oparin, d. 4; 119991, Moscow, st. Trubetskaya, d. 8, p. 2.
Kamila R. Sharipova, Clinical Resident of the Scientific and Research Center “AGP named after Academician V.I. Kulakova “Ministry of Health of Russia.
Tel.: +7 (977) 503-47-21. Email: k.r.sharipovaa@gmail.com
Address: 117997, Russia, Moscow, ul. Academician Oparin, d. 4.
Irina V. Orlovskaya, head of the clinical work of the department of pathology of newborns and premature babies NICC “AGP named after Academician V.I. Kulakova “Ministry of Health of Russia. Tel.: +7 (916) 6962056. E-mail: i_orlovskaya@oparina4.ru.
Address: 117997, Russia, Moscow, ul. Academician Oparin, d. 4.
Victor V. Zubkov, MD, director of the Institute of Neonatology and Pediatrics, NICC “AGP named after Academician V.I. Kulakova “Ministry of Health of Russia; Professor, Department of Neonatology, Federal State Autonomous Educational Institution of Higher Education “First MGMU named after THEM. Sechenov »Ministry of Health of Russia (Sechenov University).
Elena N. Baibarina, Chief Researcher, Institute of Neonatology and Pediatrics, NICC “AGP named after Academician V.I. Kulakova “Ministry of Health of Russia.

For citation: Ryumina I.I., Fatkhudinov T.Kh., Arutyunyan I.V., Makarov A.V., Lokhonina A.V., Narogan M.V., Sharipova K.R., Orlovskaya I.V., Zubkov V.V., Baibarina E.N. Survival and composition of the cellular component of breast milk under various conditions of its expression and storage.
Akusherstvo i Ginekologiya/ Obstetrics and gynecology. 2020; 3: 164-72.(In Russian).
https://dx.doi.org/10.18565/aig.2020.3.164-172

Similar Articles

By continuing to use our site, you consent to the processing of cookies that ensure the proper functioning of the site.