The Results of Different Heating Temperatures on Activities of Bioactive Proteins in Human Milk

Abstract

Background:

The most utilized pasteurization method in donor human milk banks is Holder pasteurization (heating 62.5 °C for 30 min). However, many bioactive proteins are heat sensitive and are inactivated.

Research Aim:

To determine the results of a range of heating regimes on the activities of xanthine oxidase, lactoperoxidase and lysozyme, the concentrations of immunoglobulin A and lactoferrin, as well as bacterial inactivation.

Method:

This prospective, cross-sectional, intervention study was designed to measure the influence of heating temperatures on bioactive components in donor human milk. Milk samples were processed at 40, 50, 55, 62.5, 75, 127 °C and the activities of the enzymes, and the concentration of immune proteins, were measured.

Results:

No bacterial colonies were detectable, using standard culture methods, after heating above 50 ºC. All proteins studied retained over 60% concentrations or activities when the pasteurization temperature was 50 ºC or lower, while their concentrations or activities were lost at higher temperatures. For lactoferrin, the residual concentration was above 80% when heating temperature was under 55 °C, while only 20% remained after Holder pasteurization. Both xanthine oxidase and lactoperoxidase had little residual activity when temperatures were above Holder pasteurization. Lysozyme retained a greater proportion of residual activity than other proteins, following heating at all temperatures.

Conclusions:

The concentrations or activities of immune proteins and bioactive enzymes decreased when heated above 50 °C. The results of this study can be used to design temperature control guidance during alternative methods of pasteurization.

Keywords

Australia breastfeeding human milk human milk banking immunoglobulin A lactoferrin lactoperoxidase lysozyme non-thermal pasteurisation xanthine oxidase

Get full access to this article

View all access options for this article.

References

Akinbi

Meinzen-Derr

Auer

Pullum

Kusano

Reszka

K. J.

Zimmerly

(2010). Alterations in the host defense properties of human milk following prolonged storage or pasteurization. Journal of Pediatric Gastroenterology and Nutrition, 51(3), 347–352. https://doi.org/10.1097/MPG.0b013e3181e07f0a

Al-Shehri

S. S.

Knox

C. L.

Liley

H. G.

Cowley

D. M.

Wright

J. R.

Henman

M. G.

Hewavitharana

A. K.

Charles

B. G.

Shaw

P. N.

Sweeney

E. L.

Duley

J. A.

(2015). Breastmilk-saliva interactions boost innate immunity by regulating the oral microbiome in early infancy. PloS one, 10(9), e0135047. https://doi.org/10.1371/journal.pone.0135047

Bakar

Salim

Clulow

A. J.

Nicholas

K. R.

Boyd

B. J.

(2021). Human milk composition and the effects of pasteurisation on activity of components. Trends in Food Science & Technology, 111(3), 166–174. https://doi.org/10.1016/j.tifs.2021.02.055

Bansal

Zhang

Zou

(2021). Antimicrobial enzymes in milk, and their role in human milk. In Kelly

A. L.

Larsen

L. B.

(Eds.), Agents of Change (pp. 101–126). Springer. https://doi.org/10.1007/978-3-030-55482-8_5

Barrett

N. E.

Grandison

A. S.

Lewis

M. J.

(1999). Contribution of the lactoperoxidase system to the keeping quality of pasteurized milk. Journal of Dairy Research, 66(1), 73–80. https://doi.org/10.1017/S0022029998003252

Chandan

R. C.

Parry

R. M.

Shahani

K. M.

(1965). Purification and some properties of bovine milk lysozyme. Biochimica et Biophysica Acta (BBA) - Enzymology and Biological Oxidation, 110(2), 389–398. https://doi.org/10.1016/S0926-6593(65)80046-7

Christen

Lai

C. T.

Hartmann

P. E.

Geddes

D. T.

(2013). The effect of UV-C pasteurization on bacteriostatic properties and immunological proteins of donor human milk. PloS one, 8(12), e85867. https://doi.org/10.1371/journal.pone.0085867

Contador

Delgado-Adámez

Delgado

F. J.

Cava

Ramírez

(2013). Effect of thermal pasteurisation or high pressure processing on immunoglobulin and leukocyte contents of human milk. International Dairy Journal, 32(1), 1–5. https://doi.org/10.1016/j.idairyj.2013.03.006

Czank

Prime

D. K.

Hartmann

Simmer

Hartmann

P. E.

(2009). Retention of the immunological proteins of pasteurized human milk in relation to pasteurizer design and practice. Pediatric research, 66(4), 374. https://doi.org/10.1203/PDR.0b013e3181b4554a

10.

Ewaschuk

J. B.

Unger

Harvey

O’Connor

D. L.

Field

C. J.

(2011). Effect of pasteurization on immune components of milk: implications for feeding preterm infants. Applied Physiology, Nutrition, and Metabolism, 36(2), 175–182. https://doi.org/10.1139/h11-008

11.

Franch

Audí

Ramírez-Santana

Permanyer

Pérez-Cano

F. J.

Moltó-Puigmartí

(2010). Banked human milk treatment and immunoactive factors content. Comparison with high pressure processing. Proceedings of the Nutrition Society, 69(OCE3), E288. https://doi.org/10.1017/S0029665110000777

12.

Giribaldi

Coscia

Peila

Antoniazzi

Lamberti

Ortoffi

Moro

G. E.

Bertino

Civera

Cavallarin

(2016). Pasteurization of human milk by a benchtop High-Temperature Short-Time device. Innovative Food Science & Emerging Technologies, 36, 228–233. https://doi.org/10.1016/j.ifset.2016.07.004

13.

Gothefors

Marklund

(1975). Lactoperoxidase activity in human milk and in saliva of newborn infants. Infection and Immunity, 11(6), 1210–1215. https://doi.org/10.1016/S0399-077X(76)80011-X

14.

Gutteridge

Tanner

S. J.

Bray

R. C.

(1978). Comparison of the molybdenum centres of native and desulpho xanthine oxidase. The nature of the cyanide-labile sulphur atom and the nature of the proton-accepting group. Biochemical Journal, 175(3), 887. https://doi.org/10.1042/bj1750887

15.

Harrison

(2006). Milk xanthine oxidase: Properties and physiological roles. International Dairy Journal, 16(6), 546–554. https://doi.org/10.1016/j.idairyj.2005.08.016

16.

Hartle

J. C.

Cohen

R. S.

Sakamoto

Barr

D. B.

Carmichael

S. L.

(2018). Chemical contaminants in raw and pasteurized human milk. Journal of Human Lactation, 34(2), 1–10. https://doi.org/10.1177/0890334418759308

17.

Lönnerdal

(2016). Bioactive proteins in human milk: Health, nutrition, and implications for infant formulas. The Journal of Pediatrics, 173, S4–S9. https://doi.org/10.1016/j.jpeds.2016.02.070

18.

Marín

Sánchez

Pérez

M. D.

Puyol

Calvo

(2006). Effect of heat treatment on bovine lactoperoxidase activity in skim milk: Kinetic and thermodynamic analysis. Journal of Food Science, 68(1), 89–93. https://doi.org/10.1111/j.1365-2621.2003.tb14120.x

19.

Mayayo

Montserrat

Ramos

S. J.

Martínez-Lorenzo

M. J.

Calvo

Sánchez

Pérez

M. D.

(2016). Effect of high pressure and heat treatments on IgA immunoreactivity and lysozyme activity in human milk. European Food Research and Technology, 242(6), 891–898. https://doi.org/10.1007/s00217-015-2595-7

20.

Meng

F. Y.

Uniacke-Lowe

Ryan

A. C.

Kelly

A. L.

(2021). The composition and physico-chemical properties of human milk: A review. Trends in Food Science & Technology, 112, 608–621. https://doi.org/10.1016/j.tifs.2021.03.040

21.

Permanyer

Castellote

Ramírez-Santana

Audí

Pérez-Cano

F. J.

Castell

López-Sabater

M. C.

Franch

. (2010). Maintenance of breast milk immunoglobulin A after high-pressure processing. Journal of Dairy Science, 93(3), 877–883. https://doi.org/10.3168/jds.2009-2643

22.

Perrin

M. T.

Fogleman

A. D.

Newburg

D. S.

Allen

J. C.

(2017). A longitudinal study of human milk composition in the second year postpartum: Implications for human milk banking. Maternal and Child Nutrition, 13(1), Article e12239. https://doi.org/10.1111/mcn.12239

23.

Picaud

J.-C.

Buffin

(2017). Human milk—Treatment and quality of banked human milk. Clinics in Perinatology, 44(1), 95–119. https://doi.org/10.1016/j.clp.2016.11.003

24.

Rai

Adelman

A. S.

Zhuang

Rai

G. P.

Boettcher

Lönnerdal

(2014). Longitudinal changes in lactoferrin concentrations in human milk: A global systematic review. Critical Reviews in Food Science and Nutrition, 54(12), 1539–1547. https://doi.org/10.1080/10408398.2011.642422

25.

Sousa

S. G.

Delgadillo

Saraiva

J. A.

(2014). Effect of thermal pasteurisation and high-pressure processing on immunoglobulin content and lysozyme and lactoperoxidase activity in human colostrum. Food Chemistry, 151, 79–85. https://doi.org/10.1016/j.foodchem.2013.11.024

26.

Sweeney

E. L.

Al-Shehri

S. S.

Cowley

D. M.

Liley

H. G.

Bansal

Charles

B. G.

Shaw

P. N.

Duley

J. A.

Knox

C. L.

(2018). The effect of breastmilk and saliva combinations on the in vitro growth of oral pathogenic and commensal microorganisms. Scientific Reports, 8(1), Article 15112. https://doi.org/10.1038/s41598-018-33519-3

27.

Trujillo

A. J.

Pozo

P. I.

Guamis

(2007). Effect of heat treatment on lactoperoxidase activity in caprine milk. Small Ruminant Research, 67(2), 243–246. https://doi.org/10.1016/j.smallrumres.2005.10.013

28.

Tully

D. B.

Jones

Tully

M. R.

(2001). Donor milk: What’s in it and what’s not. Journal of Human Lactation, 17(2), 152–155. https://doi.org/10.1177/089033440101700212

29.

Viazis

Farkas

B. E.

Allen

J. C.

(2007). Effects of high-pressure processing on Immunoglobulin A and lysozyme activity in human milk. Journal of Human Lactation, 23(3), 253–261. https://doi.org/10.1177/0890334407303945

30.

Weaver

L. T.

Arthur

H. M. L.

Bunn

J. E. G.

Thomas

J. E.

(1998). Human milk IgA concentrations during the first year of lactation. Archives of Disease in Childhood, 78(3), 235. https://doi.org/10.1136/adc.78.3.235

31.

Zhang

Lee

N. A.

Duley

J. A.

Cowley

D. M.

Shaw

P. N.

Bansal

(2022). Comparing the effects of hydrostatic high-pressure processing vs holder pasteurisation on the microbial, biochemical and digestion properties of donor human milk. Food Chemistry, 373, Article 131545. https://doi.org/10.1016/j.foodchem.2021.131545

32.

Zou

Bauland

Hewavitharana

A. K.

Al-Shehri

S. S.

Duley

J. A.

Cowley

D. M.

Koorts

Shaw

P. N.

Bansal

(2021). A sensitive, high-throughput fluorescent method for the determination of lactoperoxidase activities in milk and comparison in human, bovine, goat and camel milk. Food Chemistry, 339, Article 128090. https://doi.org/10.1016/j.foodchem.2020.128090

33.

Zou

Pury

B. D.

Hewavitharana

A. K.

Al-Shehri

S. S.

Bansal

(2020). A sensitive and high-throughput fluorescent method for determination of oxidase activities in human, bovine, goat and camel milk. Food Chemistry, 336, Article 127689. https://doi.org/10.1016/j.foodchem.2020.127689