Human Milk Short-Chain Fatty Acid Composition is Associated with Adiposity Outcomes in Infants

Philippa M. Prentice, Marieke H. Schoemaker, Jacques Vervoort, Kasper Hettinga, Tim T. Lambers, Eric A.F. van Tol, Carlo L. Acerini, Laurentya Olga, Clive J. Petry, Ieuan A. Hughes, Albert Koulman, Ken K. Ong, David B. Dunger

Research output: Contribution to journalArticleAcademicpeer-review

Abstract

BACKGROUND: Presumed benefits of human milk (HM) in avoiding rapid infancy weight gain and later obesity could relate to its nutrient composition. However, data on breast milk composition and its relation with growth are sparse. OBJECTIVE: We investigated whether short-chain fatty acids (SCFAs), known to be present in HM and linked to energy metabolism, are associated with infancy anthropometrics. METHODS: In a prospective birth cohort, HM hindmilk samples were collected from 619 lactating mothers at 4-8 wk postnatally [median (IQR) age: 33.9 (31.3-36.5) y, body mass index (BMI) (kg/m2): 22.8 (20.9-25.2)]. Their offspring, born at 40.1 (39.1-41.0) wk gestation with weight 3.56 (3.22-3.87) kg and 51% male, were assessed with measurement of weight, length, and skinfold thickness at ages 3, 12, and 24 mo, and transformed to age- and sex-adjusted z scores. HM SCFAs were measured by 1H-nuclear magnetic resonance spectroscopy (NMR) and GC-MS. Multivariable linear regression models were conducted to analyze the relations between NMR HM SCFAs and infancy growth parameters with adjustment for potential confounders. RESULTS: NMR peaks for HM butyrate, acetate, and formic acid, but not propionate, were detected. Butyrate peaks were 17.8% higher in HM from exclusively breastfeeding mothers than mixed-feeding mothers (P = 0.003). HM butyrate peak values were negatively associated with changes in infant weight (standardized B  = -0.10, P = 0.019) and BMI (B = -0.10, P = 0.018) between 3 and 12 mo, and negatively associated with BMI (B = -0.10, P = 0.018) and mean skinfold thickness (B = -0.10, P = 0.049) at age 12 mo. HM formic acid peak values showed a consistent negative association with infant BMI at all time points (B < = -0.10, P < = 0.014), whereas HM acetate was negatively associated with skinfold thickness at 3 mo (B = -0.10, P = 0.028) and 24 mo (B = -0.10, P = 0.036). CONCLUSIONS: These results suggest that HM SCFAs play a beneficial role in weight gain and adiposity during infancy. Further knowledge of HM SCFA function may inform future strategies to support healthy growth.

LanguageEnglish
Pages716-722
JournalThe Journal of Nutrition
Volume149
Issue number5
DOIs
Publication statusPublished - May 2019

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Volatile Fatty Acids
Adiposity
Human Milk
formic acid
Skinfold Thickness
Butyrates
Body Mass Index
Magnetic Resonance Spectroscopy
Mothers
Weights and Measures
Weight Gain
Linear Models
Acetates
Growth
Propionates
Breast Feeding
Energy Metabolism
Obesity

Keywords

  • breast milk
  • growth
  • lipids
  • nutrition
  • short chain fatty acids
  • weight

Cite this

Prentice, Philippa M. ; Schoemaker, Marieke H. ; Vervoort, Jacques ; Hettinga, Kasper ; Lambers, Tim T. ; van Tol, Eric A.F. ; Acerini, Carlo L. ; Olga, Laurentya ; Petry, Clive J. ; Hughes, Ieuan A. ; Koulman, Albert ; Ong, Ken K. ; Dunger, David B. / Human Milk Short-Chain Fatty Acid Composition is Associated with Adiposity Outcomes in Infants. In: The Journal of Nutrition. 2019 ; Vol. 149, No. 5. pp. 716-722.
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abstract = "BACKGROUND: Presumed benefits of human milk (HM) in avoiding rapid infancy weight gain and later obesity could relate to its nutrient composition. However, data on breast milk composition and its relation with growth are sparse. OBJECTIVE: We investigated whether short-chain fatty acids (SCFAs), known to be present in HM and linked to energy metabolism, are associated with infancy anthropometrics. METHODS: In a prospective birth cohort, HM hindmilk samples were collected from 619 lactating mothers at 4-8 wk postnatally [median (IQR) age: 33.9 (31.3-36.5) y, body mass index (BMI) (kg/m2): 22.8 (20.9-25.2)]. Their offspring, born at 40.1 (39.1-41.0) wk gestation with weight 3.56 (3.22-3.87) kg and 51{\%} male, were assessed with measurement of weight, length, and skinfold thickness at ages 3, 12, and 24 mo, and transformed to age- and sex-adjusted z scores. HM SCFAs were measured by 1H-nuclear magnetic resonance spectroscopy (NMR) and GC-MS. Multivariable linear regression models were conducted to analyze the relations between NMR HM SCFAs and infancy growth parameters with adjustment for potential confounders. RESULTS: NMR peaks for HM butyrate, acetate, and formic acid, but not propionate, were detected. Butyrate peaks were 17.8{\%} higher in HM from exclusively breastfeeding mothers than mixed-feeding mothers (P = 0.003). HM butyrate peak values were negatively associated with changes in infant weight (standardized B  = -0.10, P = 0.019) and BMI (B = -0.10, P = 0.018) between 3 and 12 mo, and negatively associated with BMI (B = -0.10, P = 0.018) and mean skinfold thickness (B = -0.10, P = 0.049) at age 12 mo. HM formic acid peak values showed a consistent negative association with infant BMI at all time points (B < = -0.10, P < = 0.014), whereas HM acetate was negatively associated with skinfold thickness at 3 mo (B = -0.10, P = 0.028) and 24 mo (B = -0.10, P = 0.036). CONCLUSIONS: These results suggest that HM SCFAs play a beneficial role in weight gain and adiposity during infancy. Further knowledge of HM SCFA function may inform future strategies to support healthy growth.",
keywords = "breast milk, growth, lipids, nutrition, short chain fatty acids, weight",
author = "Prentice, {Philippa M.} and Schoemaker, {Marieke H.} and Jacques Vervoort and Kasper Hettinga and Lambers, {Tim T.} and {van Tol}, {Eric A.F.} and Acerini, {Carlo L.} and Laurentya Olga and Petry, {Clive J.} and Hughes, {Ieuan A.} and Albert Koulman and Ong, {Ken K.} and Dunger, {David B.}",
year = "2019",
month = "5",
doi = "10.1093/jn/nxy320",
language = "English",
volume = "149",
pages = "716--722",
journal = "The Journal of Nutrition",
issn = "0022-3166",
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Prentice, PM, Schoemaker, MH, Vervoort, J, Hettinga, K, Lambers, TT, van Tol, EAF, Acerini, CL, Olga, L, Petry, CJ, Hughes, IA, Koulman, A, Ong, KK & Dunger, DB 2019, 'Human Milk Short-Chain Fatty Acid Composition is Associated with Adiposity Outcomes in Infants', The Journal of Nutrition, vol. 149, no. 5, pp. 716-722. https://doi.org/10.1093/jn/nxy320

Human Milk Short-Chain Fatty Acid Composition is Associated with Adiposity Outcomes in Infants. / Prentice, Philippa M.; Schoemaker, Marieke H.; Vervoort, Jacques; Hettinga, Kasper; Lambers, Tim T.; van Tol, Eric A.F.; Acerini, Carlo L.; Olga, Laurentya; Petry, Clive J.; Hughes, Ieuan A.; Koulman, Albert; Ong, Ken K.; Dunger, David B.

In: The Journal of Nutrition, Vol. 149, No. 5, 05.2019, p. 716-722.

Research output: Contribution to journalArticleAcademicpeer-review

TY - JOUR

T1 - Human Milk Short-Chain Fatty Acid Composition is Associated with Adiposity Outcomes in Infants

AU - Prentice, Philippa M.

AU - Schoemaker, Marieke H.

AU - Vervoort, Jacques

AU - Hettinga, Kasper

AU - Lambers, Tim T.

AU - van Tol, Eric A.F.

AU - Acerini, Carlo L.

AU - Olga, Laurentya

AU - Petry, Clive J.

AU - Hughes, Ieuan A.

AU - Koulman, Albert

AU - Ong, Ken K.

AU - Dunger, David B.

PY - 2019/5

Y1 - 2019/5

N2 - BACKGROUND: Presumed benefits of human milk (HM) in avoiding rapid infancy weight gain and later obesity could relate to its nutrient composition. However, data on breast milk composition and its relation with growth are sparse. OBJECTIVE: We investigated whether short-chain fatty acids (SCFAs), known to be present in HM and linked to energy metabolism, are associated with infancy anthropometrics. METHODS: In a prospective birth cohort, HM hindmilk samples were collected from 619 lactating mothers at 4-8 wk postnatally [median (IQR) age: 33.9 (31.3-36.5) y, body mass index (BMI) (kg/m2): 22.8 (20.9-25.2)]. Their offspring, born at 40.1 (39.1-41.0) wk gestation with weight 3.56 (3.22-3.87) kg and 51% male, were assessed with measurement of weight, length, and skinfold thickness at ages 3, 12, and 24 mo, and transformed to age- and sex-adjusted z scores. HM SCFAs were measured by 1H-nuclear magnetic resonance spectroscopy (NMR) and GC-MS. Multivariable linear regression models were conducted to analyze the relations between NMR HM SCFAs and infancy growth parameters with adjustment for potential confounders. RESULTS: NMR peaks for HM butyrate, acetate, and formic acid, but not propionate, were detected. Butyrate peaks were 17.8% higher in HM from exclusively breastfeeding mothers than mixed-feeding mothers (P = 0.003). HM butyrate peak values were negatively associated with changes in infant weight (standardized B  = -0.10, P = 0.019) and BMI (B = -0.10, P = 0.018) between 3 and 12 mo, and negatively associated with BMI (B = -0.10, P = 0.018) and mean skinfold thickness (B = -0.10, P = 0.049) at age 12 mo. HM formic acid peak values showed a consistent negative association with infant BMI at all time points (B < = -0.10, P < = 0.014), whereas HM acetate was negatively associated with skinfold thickness at 3 mo (B = -0.10, P = 0.028) and 24 mo (B = -0.10, P = 0.036). CONCLUSIONS: These results suggest that HM SCFAs play a beneficial role in weight gain and adiposity during infancy. Further knowledge of HM SCFA function may inform future strategies to support healthy growth.

AB - BACKGROUND: Presumed benefits of human milk (HM) in avoiding rapid infancy weight gain and later obesity could relate to its nutrient composition. However, data on breast milk composition and its relation with growth are sparse. OBJECTIVE: We investigated whether short-chain fatty acids (SCFAs), known to be present in HM and linked to energy metabolism, are associated with infancy anthropometrics. METHODS: In a prospective birth cohort, HM hindmilk samples were collected from 619 lactating mothers at 4-8 wk postnatally [median (IQR) age: 33.9 (31.3-36.5) y, body mass index (BMI) (kg/m2): 22.8 (20.9-25.2)]. Their offspring, born at 40.1 (39.1-41.0) wk gestation with weight 3.56 (3.22-3.87) kg and 51% male, were assessed with measurement of weight, length, and skinfold thickness at ages 3, 12, and 24 mo, and transformed to age- and sex-adjusted z scores. HM SCFAs were measured by 1H-nuclear magnetic resonance spectroscopy (NMR) and GC-MS. Multivariable linear regression models were conducted to analyze the relations between NMR HM SCFAs and infancy growth parameters with adjustment for potential confounders. RESULTS: NMR peaks for HM butyrate, acetate, and formic acid, but not propionate, were detected. Butyrate peaks were 17.8% higher in HM from exclusively breastfeeding mothers than mixed-feeding mothers (P = 0.003). HM butyrate peak values were negatively associated with changes in infant weight (standardized B  = -0.10, P = 0.019) and BMI (B = -0.10, P = 0.018) between 3 and 12 mo, and negatively associated with BMI (B = -0.10, P = 0.018) and mean skinfold thickness (B = -0.10, P = 0.049) at age 12 mo. HM formic acid peak values showed a consistent negative association with infant BMI at all time points (B < = -0.10, P < = 0.014), whereas HM acetate was negatively associated with skinfold thickness at 3 mo (B = -0.10, P = 0.028) and 24 mo (B = -0.10, P = 0.036). CONCLUSIONS: These results suggest that HM SCFAs play a beneficial role in weight gain and adiposity during infancy. Further knowledge of HM SCFA function may inform future strategies to support healthy growth.

KW - breast milk

KW - growth

KW - lipids

KW - nutrition

KW - short chain fatty acids

KW - weight

U2 - 10.1093/jn/nxy320

DO - 10.1093/jn/nxy320

M3 - Article

VL - 149

SP - 716

EP - 722

JO - The Journal of Nutrition

T2 - The Journal of Nutrition

JF - The Journal of Nutrition

SN - 0022-3166

IS - 5

ER -