Overweight modifies the nutritional composition of human milk? A systematic review

Oliveira, Elissa; Marano, Daniele; Amaral, Yasmin Notarbartolo di Villarosa do; Abranches, Andrea; Soares, Fernanda Valente Mendes; Moreira, Maria Elisabeth Lopes

doi:10.1590/1413-812320202510.29902018

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REVIEW • Ciênc. saúde coletiva 25 (10) • Oct 2020 • https://doi.org/10.1590/1413-812320202510.29902018 copy

Overweight modifies the nutritional composition of human milk? A systematic review

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Abstract

This paper aims to identify the association between overweight and the nutritional composition of human milk. A systematic review was performed by searching on PubMed, Virtual Health Library (BVS), EMBASE, Web of Science, and SCOPUS databases, from May to June 2018, using keywords “Human Milk” AND “Overweight” OR “Obesity” OR “Body Mass Index”. The bibliographic search returned 435 papers after the duplicates were removed. Of this total, 12 papers were selected for abstract reading, and nine works were incorporated into this systematic review. Eight papers showed that overweight increased the total concentration of lipids or glucose or macronutrient fractions, and only one study found no association between overweight and the nutritional composition of human milk. Most works selected evidenced that obesity changed the total concentration of lipids and their fractions. Thus, we recommend that women’s weight and height be evaluated in the pregestational visit to identify and monitor nutritional deviations, contributing to weight adequacy before pregnancy and assisting in the production of milk with adequate nutritional composition.

Key words
Overweight; Human milk; Nutritional Composition; Systematic Review

Author	Year	Type of study	Country	Sample n total and n by group	Follow-up losses	Age (years)	Ethnic groups	Anthropometric assessment indicators	Mean pregestational body mass index (Kg/m²2 Fujimori M, França EL, Fiorin V, Morais TC, Honorio-França AC, Abreu LC. Changes in the biochemical and immunological components of serum and colostrum of overweight and obese mothers. BMC Pregnancy Childbirth 2015; 15:166-174)	Eligibility criteria	Exclusion criteria
Marín et al.¹⁵15 Marín MC, Sanjurjo A, Rodrigo MA, Alaniz MJ. Long-chain polyunsaturated fatty acids in breast milk in La Plata, Argentina: relationship with maternal nutritional status. Prostaglandins Leukot Essent Fatty Acids 2005; 73(5):355-360.	2005	Cross-sectional	Argentina	46 21 eutrophic, 16 overweight, 9 obese	No losses	16-39	NI	Weight, height, BMI	NI	Women who gave birth to healthy full-term babies (38-42 weeks of gestational age)	NI
Storck Lindholm et al.¹⁹19 Storck Lindholm E, Strandvik B, Altman D, Möller A, Palme Kilander C. Different fatty acid pattern in breast milk of obese compared to normal-weight mothers. Prostaglandins Leukot Essent Fatty Acids 2013; 88(3):211-217.	2013	Cohort/ intervention	Sweden	82 41 eutrophic, 41 obese, of which 29 were part of the intervention group	No losses	Eutrophic: 32.07 ± 4.1¹ 1 Mean data; Obese without intervention: 30.5 ± 5.7¹ 1 Mean data; Obese with intervention: 32.17 ± 3.7¹ 1 Mean data;	NI	Pregestational and gestational BMI (32 and 36 weeks)	Eutrophic: 22 ± 1.8¹ 1 Mean data; Obese without intervention: 35 ± 3.8¹ 1 Mean data; Obese with intervention: 36 ± 5.0¹ 1 Mean data;	NI	Premature birth (<37 weeks), multiple pregnancies and/or babies with major malformations
Mäkelä et al.¹⁶16 Mäkelä J, Linderborg K, Niinikoski H, Yang B, Lagström H. Breast milk fatty acid composition differs between over-weight and normal weight women: the STEPS Study. Eur J Nutr 2013; 52(2):727-735.	2013	Cross-sectional	Finland	163 49 eutrophic, 51 overweight	No losses	Eutrophic: 29.7 (3.6) ¹ 1 Mean data; Overweight: 31.0 (5.0) ¹ 1 Mean data;	NI	Pregestational BMI	Eutrophic: 20.9 (2.1) ¹ 1 Mean data; Overweight: 29.7 (3.3) ¹ 1 Mean data;	NI	NI
Linderborg et al.¹⁷17 Linderborg KM, Kalpio M, Mäkelä J, Niinikoski H, Kallio HP, Lagström H. Tandem mass spectrometric analysis of human milk triacylglycerols from normal weight and overweight mothers on different diets. Food Chem 2014; 146:583-590.	2014	Cross-sectional	Finland	40 Eutrophic with recommended food choices Eutrophic with non-recommended food choices Overweight with recommended food choices Overweight with non-recommended food choices	No losses	30.01 ± 3.96¹ 1 Mean data;	NI	Pregestational BMI	Eutrophic with adequate food choices: 20.81 ± 1.69¹ 1 Mean data; Eutrophic with inadequate food choices: 21.41 ± 2.31¹ 1 Mean data; Overweight with adequate food choices: 29.79 ± 2.85¹ 1 Mean data; Overweight with inadequate food choices: 31.22 ± 4.25¹ 1 Mean data;	NI	NI
Fujimori et al.²2 Fujimori M, França EL, Fiorin V, Morais TC, Honorio-França AC, Abreu LC. Changes in the biochemical and immunological components of serum and colostrum of overweight and obese mothers. BMC Pregnancy Childbirth 2015; 15:166-174	2015	Cross-sectional	Brazil	68 25 eutrophic, 24 overweight, 19 obese	No losses	Eutrophic: 25.0 (18-37) ² 2 Median data; NI = No information. Overweight: 24.1 (18-37) ² 2 Median data; NI = No information. Obese: 26.8 (21-38)² 2 Median data; NI = No information.	NI	Pregestational BMI	Eutrophic: 21.4 (18.4 - 24.4) ² 2 Median data; NI = No information. Overweight: 26.6 (25.2 - 28.6) ² 2 Median data; NI = No information. Obese: 34.7 (30.1 - 47.9) ² 2 Median data; NI = No information.	Women with breasts without fissures on nipples or mastitis; who were exclusively breastfeeding their babies	Multiple pregnancies, fetal malformation and births before the 37th gestational week
Panagos et al.¹⁸18 Panagos PG, Vishwanathan R, Penfield-Cyr A, Matthan NR, Shivappa N, Wirth MD, Hebert JR, Sen S. Breastmilk from obese mothers has pro-inflammatory properties and decreased neuroprotective factors. J Perinatol 2016; 36(4):284-290.	2016	Cohort	USA	42 21 eutrophic, 21 obese	No losses to evaluate the nutritional composition of milk	Eutrophic: 31 ± 3.7¹ 1 Mean data; Obese: 30 ± 5.7¹ 1 Mean data;	Multiethnic (Hispanic, Caucasian, African American, and Asian)	Weight, height and pregestational BMI	Eutrophic: 22 (1.9) ¹ 1 Mean data; Obese: 35 (4.0) ¹ 1 Mean data;	Recruited at the Tufts Medical Center. Visits between 34 and 40 weeks of gestational age. Women who planned to offer breast milk as the main form of nutrition for their babies and were willing to provide a sample of human milk on a study visit between 4 and 10 weeks postpartum	Childbirth before 35 weeks of gestational age, multiple pregnancy, tobacco use, intrauterine growth restriction, fetal abnormalities, stillbirth.
De Luca et al.⁴4 De Luca A, Frasquet-Darrieux M, Gaud MA, Christin P, Boquien CY, Millet C, Herviou M, Darmaun D, Robins RJ, In-grand P, Hankard R. Higher Leptin but Not Human Milk Macronutrient Concentration Distinguishes Normal-Weight from Obese Mothers at 1-Month Postpartum. PLoS One 2016; 11(12):e0168568	2016	Cross-sectional	France	100 50 eutrophic, 50 obese	No losses	Eutrophic 30.1 ± 4.2¹ 1 Mean data; Obese 30.2 ± 4.7¹ 1 Mean data;	NI	Weight, height and BMI	Eutrophic: 21.6 ± 1.4¹ 1 Mean data; Obese: 34.3 ± 3.9¹ 1 Mean data;	Continuous breastfeeding up to 1 month	Pre-existing chronic or gestational disease, smoking during pregnancy, twin pregnancy, prematurity, low birth weight or hospitalization in the neonatal period
Young et al.³3 Young BE, Patinkin Z, Palmer C, de la Houssaye B, Barbour LA, Hernandez T, Friedman JE, Krebs NF. Human Milk Insulin is Related to Maternal Plasma Insulin and BMI - But other Components of Human Milk do not Differ by BMI. Eur J Clin Nutr 2017; 71(9):1094-1100.	2017	Cohort	USA	48 26 eutrophic, 22 overweight	No losses	Eutrophic 30.8 ± 2.6¹ 1 Mean data; Obese 30.3 ± 3.9¹ 1 Mean data;	NI	Pregestational BMI	Eutrophic: 21.4 ± 2.0¹ 1 Mean data; Obese: 30.4 ± 4.2¹ 1 Mean data;	Maternal age 21 to 36 years, with pregestational BMI from 17.0 to 39.9 kg / m²2 Fujimori M, França EL, Fiorin V, Morais TC, Honorio-França AC, Abreu LC. Changes in the biochemical and immunological components of serum and colostrum of overweight and obese mothers. BMC Pregnancy Childbirth 2015; 15:166-174, single fetus, planning to breastfeed exclusively for at least four months, healthy, delivery at the study hospital	Women with chronic medical conditions requiring treatment, such as cardiopulmonary, rheumatological or kidney disease or pre-existing diabetes, gestational diabetes, pre-eclampsia or premature birth
Hahn et al.²⁰20 Hahn WH, Jeong T, Park S, Song S, Kang NM. Content fat and calorie of human milk is affected by interactions between maternal age and body mass index. J Matern Fetal Neonatal Med 2018; 31(10):1385-1388.	2017	Cross-sectional	South Korea	80 20 eutrophic among 20 years, 20 eutrophic among 30 years, 20 Overweight among 20 years and 20 Overweight among 30 years	NI	Eutrophic > 20 and < 30 Obese > 30	NI	BMI	NI	Mothers who exclusively breastfed, gave birth to a healthy baby, without any breast diseases including inflammatory diseases, started to breastfeed from the first day of delivery and children with normal weight at birth, head circumference and birth height	Mothers with a disease including gestational diabetes mellitus and hypertensive diseases

Author	Nutritional content analyzed	Method used to assess the composition of human milk	Milk evaluation period	Moment of evaluation of human milk (colostrum, transitional, mature)	Confounding factors controlled in the analysis	Main results
Marín et al.¹⁵15 Marín MC, Sanjurjo A, Rodrigo MA, Alaniz MJ. Long-chain polyunsaturated fatty acids in breast milk in La Plata, Argentina: relationship with maternal nutritional status. Prostaglandins Leukot Essent Fatty Acids 2005; 73(5):355-360.	Lipid (fatty acids) and protein	Total lipids: Folch Fatty acids: gas chromatography Protein: Lowry et al.	1 and 3 months	Mature³ 1 Colostro: Até 5 dias após o parto;	NI	The human milk protein was not modified by the woman's nutritional status. There was a higher concentration of total lipids, linoleic acid, polyunsaturated fatty acids (omega 6) among obese puerperae.
Storck Lindholm et al.¹⁹19 Storck Lindholm E, Strandvik B, Altman D, Möller A, Palme Kilander C. Different fatty acid pattern in breast milk of obese compared to normal-weight mothers. Prostaglandins Leukot Essent Fatty Acids 2013; 88(3):211-217.	Lipid (fatty acids)	Fatty acids: gas and liquid chromatography	3 days, 10 days, 1 month and 2 months		NI	The concentrations of omega 6 in human milk were higher in eutrophic women on the third day after birth, and omega 3 was lower in obese women without intervention. The proportion of omega 6/omega 3 was higher in the milk of obese women without intervention compared to the other two groups. Obese mothers with dietary monitoring had concentrations of polyunsaturated fatty acids close to those of eutrophic ones.
Mäkelä et al.¹⁶16 Mäkelä J, Linderborg K, Niinikoski H, Yang B, Lagström H. Breast milk fatty acid composition differs between over-weight and normal weight women: the STEPS Study. Eur J Nutr 2013; 52(2):727-735.	Lipid (fatty acids)	Fatty acids: gas chromatography	3 months	Mature³ 1 Colostro: Até 5 dias após o parto;	Maternal diet	Overweight women had significantly more saturated fatty acids and lower omega 3 when compared to eutrophic mothers. Moreover, the proportion of unsaturated and saturated fatty acids was significantly lower, and the proportion of omega 6 to omega 3 was higher in overweight women.
Linderborg et al.¹⁷17 Linderborg KM, Kalpio M, Mäkelä J, Niinikoski H, Kallio HP, Lagström H. Tandem mass spectrometric analysis of human milk triacylglycerols from normal weight and overweight mothers on different diets. Food Chem 2014; 146:583-590.	Lipid (fatty acids and triglycerides)	Fatty acids: gas chromatography	3 months	Mature³ 1 Colostro: Até 5 dias após o parto;	NI	Eutrophic puerperae with recommended dietary choices had more linoleic acid and less diacylglycerol fragments in milk compared to eutrophic puerperae with non-recommended food choices.
Fujimori et al.²2 Fujimori M, França EL, Fiorin V, Morais TC, Honorio-França AC, Abreu LC. Changes in the biochemical and immunological components of serum and colostrum of overweight and obese mothers. BMC Pregnancy Childbirth 2015; 15:166-174	Lipid (cholesterol, triglycerides), glucose and protein	Total lipids: Enzymatic colorimetric method Glucose: Enzymatic system Protein: Biuret colorimetric method	48-72 hours postpartum	Colostrum¹ 1 Dados de média;	Maternal age, gestational age at delivery, smoking, high blood pressure, pre-gestational body mass index, pre-gestational diabetes and gestational diabetes	Increased calories, fat, and glucose were found in the colostrum of obese women. Protein concentration was similar between groups.
Panagos et al.¹⁸18 Panagos PG, Vishwanathan R, Penfield-Cyr A, Matthan NR, Shivappa N, Wirth MD, Hebert JR, Sen S. Breastmilk from obese mothers has pro-inflammatory properties and decreased neuroprotective factors. J Perinatol 2016; 36(4):284-290.	Lipids, lactose, protein	Total lipids, lactose and protein: Julie Z7 Automatic MilkoScope equipment by ultrasound technique Fatty acids: modified Folch method, followed by saponification and methylation	2 months	Mature³ 1 Colostro: Até 5 dias após o parto;	NI	The mature milk of obese mothers had a lower amount of omega 3. However, there was no association between pre-gestational BMI, caloric density and macronutrients in human milk.
De Luca et al.⁴4 De Luca A, Frasquet-Darrieux M, Gaud MA, Christin P, Boquien CY, Millet C, Herviou M, Darmaun D, Robins RJ, In-grand P, Hankard R. Higher Leptin but Not Human Milk Macronutrient Concentration Distinguishes Normal-Weight from Obese Mothers at 1-Month Postpartum. PLoS One 2016; 11(12):e0168568	Protein (amino acids)	Free amino acids: ultra-performance liquid chromatography and tandem mass spectrometry	1 month	Mature³ 1 Colostro: Até 5 dias após o parto;	NI	The amount of branched-chain amino acids was 20% higher in the mature milk of obese puerperae and 30% concerning tyrosine.
Young et al.³3 Young BE, Patinkin Z, Palmer C, de la Houssaye B, Barbour LA, Hernandez T, Friedman JE, Krebs NF. Human Milk Insulin is Related to Maternal Plasma Insulin and BMI - But other Components of Human Milk do not Differ by BMI. Eur J Clin Nutr 2017; 71(9):1094-1100.	Lipids, lactose, protein, calorie	Lipid: creamatocrit; Lactose: enzymatic digestion Protein: modified version of the Bradford method	2 weeks, 1,2,3,4 months	Transição² 2 Dados de mediana; NI= Não informado. e Maduro³ 3 Mature: > 15 days after delivery. NI = Not Informed. (Anterior e posterior)	NI	There was no association between pregestational BMI and the concentration of lipids, lactose, and protein.
Hahn et al.²⁰20 Hahn WH, Jeong T, Park S, Song S, Kang NM. Content fat and calorie of human milk is affected by interactions between maternal age and body mass index. J Matern Fetal Neonatal Med 2018; 31(10):1385-1388.	Lipids, protein, lactose, calorie	MIRIS	4 weeks	Mature³ 1 Colostro: Até 5 dias após o parto;	Maternal age	The interaction between maternal age and BMI modified milk macronutrients in different ways, according to the different subgroups.

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[1] Collaborations

All authors made substantial contributions to the study’s conception and design, obtaining, analyzing, and interpreting the data, elaborating the paper, and approved the final version of the manuscript.