Does Fetal Growth Adequacy Affect the Nutritional Composition of Mothers' Milk?: A Historical Cohort Study

Abstract

Objective The study aimed to assess the association between intrauterine growth of preterm infants and energy and macronutrient contents in their mothers' milk.

Study Design A historical cohort of mothers of preterm infants was assessed according to offspring's intrauterine growth. Fetal growth restriction (FGR) was defined as small-for-gestational age or appropriate for gestational age with fetal growth deceleration. During the first 4 weeks after delivery, the composition of daily pool samples of mothers' milk was measured by using a mid-infrared human milk analyzer. Explanatory models for milk energy, true protein, total carbohydrate, and fat contents were obtained by generalized additive mixed effects regression models.

Results In total, 127 milk samples were analyzed from 73 mothers who delivered 92 neonates. Energy content was significantly higher in mothers with chronic hypertension (average: +6.28 kcal/dL; 95% confidence interval [CI]: 0.54–12.01; p = 0.034) and for extremely preterm compared with very preterm infants (average: +5.95 kcal/dL; 95% CI: 2.16–9.73; p = 0.003), and weakly associated with single pregnancies (average: +3.38 kcal/dL; 95% CI: 0.07–6.83; p = 0.057). True protein content was significantly higher in mothers with chronic hypertension (average: +0.91 g/dL; 95% CI: 0.63–1.19; p < 0.001) and with hypertension induced by pregnancy (average: +0.25 g/dL, 95% CI: 0.07–0.44; p = 0.007), and for extremely preterm compared with very and moderate preterm infants (average: +0.19; 95% CI: 0.01–0.38; p = 0.043 and +0.28 g/dL; 95% CI: 0.05–0.51; p = 0.017, respectively). Fat content was weakly and negatively associated with FGR, both in SGA infants and AGA infants with fetal growth deceleration (average: −0.44 g/dL; 95% CI: −0.92 to −0.05; p = 0.079 and average: −0.36 g/dL; 95% CI: −0.74 to −0.02; p = 0.066, respectively).

Conclusion Energy and macronutrient contents in mothers' milk of preterm infants was significantly and positively associated with the degree of prematurity and hypertension. The hypothesis that the composition of milk is associated with FGR was not demonstrated.

Key Points

• Energy and protein are higher for more immature infants.

• Energy and/or protein is higher in hypertension.

• Fat may be lower for infants with intrauterine growth restriction.

Keywords

fetal growth restriction - maternal hypertension - mothers' milk composition - prematurity - twin pregnancy

• References

• 1 Victora CG, Bahl R, Barros AJ. et al; Lancet Breastfeeding Series Group. Breastfeeding in the 21st century: epidemiology, mechanisms, and lifelong effect. Lancet 2016; 387 (10017): 475-490
• 2 de Halleux V, Pieltain C, Senterre T. et al. Growth benefits of own mother's milk in preterm infants fed daily individualized fortified human milk. Nutrients 2019; 11 (04) 11
• 3 Bauer J, Gerss J. Longitudinal analysis of macronutrients and minerals in human milk produced by mothers of preterm infants. Clin Nutr 2011; 30 (02) 215-220
• 4 Chung MY. Factors affecting human milk composition. Pediatr Neonatol 2014; 55 (06) 421-422
• 5 Bhatia J. Human milk for preterm infants and fortification. Nestle Nutr Inst Workshop Ser 2016; 86: 109-119
• 6 Macedo I, Pereira-da-Silva L, Cardoso M. The fortification method relying on assumed human milk composition overestimates the actual energy and macronutrient intakes in very preterm infants. Matern Health Neonatol Perinatol 2018; 4: 22
• 7 Arslanoglu S, Boquien CY, King C. et al. Fortification of human milk for preterm infants: update and recommendations of the European Milk Bank Association (EMBA) Working Group on Human Milk Fortification. Front Pediatr 2019; 7: 76
• 8 Polberger S, Räihä NCR, Juvonen P, Moro GE, Minoli I, Warm A. Individualized protein fortification of human milk for preterm infants: comparison of ultrafiltrated human milk protein and a bovine whey fortifier. J Pediatr Gastroenterol Nutr 1999; 29 (03) 332-338
• 9 Gidrewicz DA, Fenton TR. A systematic review and meta-analysis of the nutrient content of preterm and term breast milk. BMC Pediatr 2014; 14: 216
• 10 Mimouni FB, Lubetzky R, Yochpaz S, Mandel D. Preterm human milk macronutrient and energy composition: a systematic review and meta-analysis. Clin Perinatol 2017; 44 (01) 165-172
• 11 Arsić A, Vučić V, Prekajski N. et al. Different fatty acid composition of serum phospholipids of small and appropriate for gestational age preterm infants and of milk from their mothers. Hippokratia 2012; 16 (03) 230-235
• 12 Fares S, Sethom MM, Hammami MB. et al. Increased docosahexaenoic acid and n-3 polyunsaturated fatty acids in milk from mothers of small for gestational age preterm infants. Prostaglandins Leukot Essent Fatty Acids 2018; 135: 42-46
• 13 Domany KA, Mandel D, Kedem MH, Lubetzky R. Breast milk fat content of mothers to small-for-gestational-age infants. J Perinatol 2015; 35 (06) 444-446
• 14 Santiago LTC, Meira Júnior JD, Freitas NA, Kurokawa CS, Rugolo LMSS. Colostrum fat and energy content: effect of gestational age and fetal growth. Rev Paul Pediatr 2018; 36 (03) 286-291
• 15 Clark RH, Olsen IE, Spitzer AR. Assessment of neonatal growth in prematurely born infants. Clin Perinatol 2014; 41 (02) 295-307
• 16 Norris T, Johnson W, Farrar D, Tuffnell D, Wright J, Cameron N. Small-for-gestational age and large-for-gestational age thresholds to predict infants at risk of adverse delivery and neonatal outcomes: are current charts adequate? An observational study from the Born in Bradford cohort. BMJ Open 2015; 5 (03) e006743
• 17 Gardosi J. Preterm standards for fetal growth and birthweight. Acta Paediatr 2017; 106 (09) 1383-1384
• 18 Beune IM, Bloomfield FH, Ganzevoort W. et al. Consensus based definition of growth restriction in the newborn. J Pediatr 2018; 196: 71-76.e1
• 19 Goldberg DL, Becker PJ, Brigham K. et al. Identifying malnutrition in preterm and neonatal populations: recommended indicators. J Acad Nutr Diet 2018; 118 (09) 1571-1582
• 20 Czosnykowska-Łukacka M, Królak-Olejnik B, Orczyk-Pawiłowicz M. Breast milk macronutrient components in prolonged lactation. Nutrients 2018; 10 (12) 1893
• 21 de Halleux V, Rigo J. Variability in human milk composition: benefit of individualized fortification in very-low-birth-weight infants. Am J Clin Nutr 2013; 98 (02) 529S-535S
• 22 Engle WA. American Academy of Pediatrics Committee on Fetus and Newborn. Age terminology during the perinatal period. Pediatrics 2004; 114 (05) 1362-1364
• 23 Tucker J, McGuire W. Epidemiology of preterm birth. BMJ 2004; 329 (7467): 675-678
• 24 Fenton TR, Kim JH. A systematic review and meta-analysis to revise the Fenton growth chart for preterm infants. BMC Pediatr 2013; 13: 59
• 25 Hadlock FP, Harrist RB, Martinez-Poyer J. In utero analysis of fetal growth: a sonographic weight standard. Radiology 1991; 181 (01) 129-133
• 26 Sotiriadis A, Eleftheriades M, Chatzinikolaou F, Hassiakos D, Chrousos GP, Pervanidou P. National curves of foetal growth in singleton foetuses of Greek origin. Eur J Clin Invest 2016; 46 (05) 425-433
• 27 Mack LR, Tomich PG. Gestational diabetes: diagnosis, classification, and clinical care. Obstet Gynecol Clin North Am 2017; 44 (02) 207-217
• 28 Brown MA, Magee LA, Kenny LC. et al; International Society for the Study of Hypertension in Pregnancy (ISSHP). Hypertensive disorders of pregnancy: ISSHP classification, diagnosis, and management recommendations for international practice. Hypertension 2018; 72 (01) 24-43
• 29 American College of Obstetricians and Gynecologists, Task Force on Hypertension in Pregnancy. Hypertension in pregnancy. Report of the American College of Obstetricians and Gynecologists' Task Force on Hypertension in Pregnancy. Obstet Gynecol 2013; 122 (05) 1122-1131
• 30 Bland M. An introduction to medical statistics. 3rd ed.. Oxford: Oxford University Press; 2000
• 31 Phattraprayoon N, Kraisonsin N, Kanjanapattanakul W. Comparison of breast milk compositions among mothers delivering small-for-gestational age, appropriate-for-gestational age, and large-for-gestational age infants. Breastfeed Med 2018; 13 (09) 627-630
• 32 Ernst SA, Brand T, Reeske A, Spallek J, Petersen K, Zeeb H. Care-related and maternal risk factors associated with the antenatal nondetection of intrauterine growth restriction: a case-control study from Bremen, Germany. BioMed Res Int 2017; 2017: 1746146
• 33 Larsson A, Ottosson P, Törnqvist C, Olhager E. Body composition and growth in full-term small for gestational age and large for gestational age Swedish infants assessed with air displacement plethysmography at birth and at 3-4 months of age. PLoS One 2019; 14 (05) e0207978
• 34 Hong YH, Chung S. Small for gestational age and obesity related comorbidities. Ann Pediatr Endocrinol Metab 2018; 23 (01) 4-8
• 35 Embleton ND. Optimal protein and energy intakes in preterm infants. Early Hum Dev 2007; 83 (12) 831-837
• 36 Dizdar EA, Sari FN, Degirmencioglu H. et al. Effect of mode of delivery on macronutrient content of breast milk. J Matern Fetal Neonatal Med 2014; 27 (11) 1099-1102
• 37 Argov-Argaman N, Mandel D, Lubetzky R. et al. Human milk fatty acids composition is affected by maternal age. J Matern Fetal Neonatal Med 2017; 30 (01) 34-37
• 38 Galante L, Milan AM, Reynolds CM, Cameron-Smith D, Vickers MH, Pundir S. Sex-specific human milk composition: the role of infant sex in determining early life nutrition. Nutrients 2018; 10 (09) 10
• 39 Léké A, Grognet S, Deforceville M. et al. Macronutrient composition in human milk from mothers of preterm and term neonates is highly variable during the lactation period. Clin Nutr Exp 2019; 26: 59-72
• 40 Maly J, Burianova I, Vitkova V, Ticha E, Navratilova M, Cermakova E. PREMATURE MILK study group. Preterm human milk macronutrient concentration is independent of gestational age at birth. Arch Dis Child Fetal Neonatal Ed 2019; 104 (01) F50-F56
• 41 Hill PD, Aldag JC, Chatterton RT, Zinaman M. Comparison of milk output between mothers of preterm and term infants: the first 6 weeks after birth. J Hum Lact 2005; 21 (01) 22-30
• 42 Whitford HM, Wallis SK, Dowswell T, West HM, Renfrew MJ. Breastfeeding education and support for women with twins or higher order multiples. Cochrane Database Syst Rev 2017; 2: CD012003
• 43 Saint L, Maggiore P, Hartmann PE. Yield and nutrient content of milk in eight women breast-feeding twins and one woman breast-feeding triplets. Br J Nutr 1986; 56 (01) 49-58
• 44 Keikha M, Bahreynian M, Saleki M, Kelishadi R. Macro- and micronutrients of human milk composition: are they related to maternal diet? A comprehensive systematic review. Breastfeed Med 2017; 12 (09) 517-527
• 45 Bachour P, Yafawi R, Jaber F, Choueiri E, Abdel-Razzak Z. Effects of smoking, mother's age, body mass index, and parity number on lipid, protein, and secretory immunoglobulin A concentrations of human milk. Breastfeed Med 2012; 7 (03) 179-188
• 46 Dangat K, Upadhyay D, Kilari A. et al. Altered breast milk components in preeclampsia; An in-vitro proton NMR spectroscopy study. Clin Chim Acta 2016; 463: 75-83
• 47 Napierala M, Mazela J, Merritt TA, Florek E. Tobacco smoking and breastfeeding: effect on the lactation process, breast milk composition and infant development. A critical review. Environ Res 2016; 151: 321-338
• 48 Shapira D, Mandel D, Mimouni FB. et al. The effect of gestational diabetes mellitus on human milk macronutrients content. J Perinatol 2019; 39 (06) 820-823
• 49 Amaral YNDVD, Rocha DM, Silva LMLD, Soares FVM, Moreira MEL. Do maternal morbidities change the nutritional composition of human milk? A systematic review. Cien Saude Colet 2019; 24 (07) 2491-2498
• 50 Buca D, Pagani G, Rizzo G. et al. Outcome of monochorionic twin pregnancy with selective intrauterine growth restriction according to umbilical artery Doppler flow pattern of smaller twin: systematic review and meta-analysis. Ultrasound Obstet Gynecol 2017; 50 (05) 559-568
• 51 Podymow T, August P. Postpartum course of gestational hypertension and preeclampsia. Hypertens Pregnancy 2010; 29 (03) 294-300