European Journal of Nutrition

, Volume 58, Issue 8, pp 3241–3253 | Cite as

Impact of a high-protein diet during lactation on milk composition and offspring in a pig model

  • Alexandra SchutkowskiEmail author
  • Holger Kluge
  • Paula Trotz
  • Gerd Hause
  • Bettina König
  • Monika Wensch-Dorendorf
  • Gabriele I. Stangl
Original Contribution



Early postnatal nutrition not only holds relevance to infant growth, but also determines the risk of developing obesity and chronic diseases such as diabetes type 2 and cardiovascular diseases in adulthood. It is suggested that a high-protein (HP) diet in early childhood can predispose children to obesity. However, data concerning possible alterations in milk composition and the development of the offspring in response to a maternal HP diet are currently not available. To address this question, we conducted a study using pigs as a model organism.


At parturition, sows were assigned to two experimental groups. During lactation, the control group received a diet with a protein content of 16%, whereas the diet of the HP group contained 30% protein. After 28 days of lactation, samples were taken from sows and piglets for the quantification of free amino acids and other metabolites and for histology.


Serum and milk urea showed the most marked differences between the two groups of sows, whereas serum urea concentration in piglets did not differ. Here, we found that the intake of an HP diet changed a series of metabolites in sows, but had only small effects on milk composition and virtually no effects on growth in the offspring. Interestingly, maternal protein intake during lactation shapes the microbiome of the offspring.


From our current study, we conclude that even a very high maternal protein intake throughout lactation has no impact on growth and health parameters of the offspring.


Lactation Pig High protein Milk 



Branched chain amino acid




Crude protein


Free amino acid


High protein


Insulin-like growth factor 1


Least-squares means


Phosphate buffered saline


Compliance with ethical standards

Conflict of interest

The authors have declared no conflicts of interest.

Supplementary material

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Supplementary material 1 (DOCX 34 KB)
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Supplementary material 2 (TIF 2692 KB)
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Supplementary material 3 (TIF 3904 KB)
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Supplementary material 4 (TIF 3469 KB)


  1. 1.
    Koletzko B, Brands B, Poston L et al (2012) Early nutrition programming of long-term health. Proc Nutr Soc 71:371–378. CrossRefPubMedGoogle Scholar
  2. 2.
    Arenz S, Rückerl R, Koletzko B et al (2004) Breast-feeding and childhood obesity-a systematic review. Int J Obes Relat Metab Disord 28:1247–1256. CrossRefPubMedGoogle Scholar
  3. 3.
    Field CJ (2005) The immunological components of human milk and their effect on immune development in infants. J Nutr 135:1–4. CrossRefPubMedGoogle Scholar
  4. 4.
    Michaelsen KF, Skafte L, Badsberg JH et al (1990) Variation in macronutrients in human bank milk: influencing factors and implications for human milk banking. J Pediatr Gastroenterol Nutr 11:229–239CrossRefGoogle Scholar
  5. 5.
    Quinn EA, Largado F, Power M et al (2012) Predictors of breast milk macronutrient composition in Filipino mothers. Am J Hum Biol 24:533–540. CrossRefPubMedGoogle Scholar
  6. 6.
    Tielemans SMAJ, Altorf-van der Kuil W, Engberink MF et al (2013) Intake of total protein, plant protein and animal protein in relation to blood pressure: a meta-analysis of observational and intervention studies. J Hum Hypertens 27:564–571. CrossRefPubMedGoogle Scholar
  7. 7.
    EFSA Panel on Dietetic Products, Nutrition and Allergies (2012) Scientific opinion on dietary reference values for protein. EFSA J 10:2557. CrossRefGoogle Scholar
  8. 8.
    Fleddermann M, Demmelmair H, Grote V et al (2017) Role of selected amino acids on plasma IGF-I concentration in infants. Eur J Nutr 56:613–620. CrossRefPubMedGoogle Scholar
  9. 9.
    Hörnell A, Lagström H, Lande B et al (2013) Protein intake from 0 to 18 years of age and its relation to health: a systematic literature review for the 5th Nordic Nutrition Recommendations. Food Nutr Res 57:21083. CrossRefGoogle Scholar
  10. 10.
    Kanitz E, Otten W, Tuchscherer M et al (2012) High and low protein∶ carbohydrate dietary ratios during gestation alter maternal-fetal cortisol regulation in pigs. PLoS One 7:e52748. CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Metges CC, Görs S, Lang IS et al (2014) Low and high dietary protein:carbohydrate ratios during pregnancy affect materno-fetal glucose metabolism in pigs. J Nutr 144:155–163. CrossRefPubMedGoogle Scholar
  12. 12.
    Liberato SC, Singh G, Mulholland K (2013) Effects of protein energy supplementation during pregnancy on fetal growth: a review of the literature focusing on contextual factors. Food Nutr Res 57:20499. CrossRefGoogle Scholar
  13. 13.
    Thone-Reineke C, Kalk P, Dorn M et al (2006) High-protein nutrition during pregnancy and lactation programs blood pressure, food efficiency, and body weight of the offspring in a sex-dependent manner. Am J Physiol Regul Integr Comp Physiol 291:R1025–R1030. CrossRefPubMedGoogle Scholar
  14. 14.
    Shiell AW, Campbell-Brown M, Haselden S et al (2001) High-meat, low-carbohydrate diet in pregnancy: relation to adult blood pressure in the offspring. Hypertension 38:1282–1288CrossRefGoogle Scholar
  15. 15.
    Koletzko B, Kries R von, Closa R et al (2009) Lower protein in infant formula is associated with lower weight up to age 2 years: a randomized clinical trial. Am J Clin Nutr 89:1836–1845. CrossRefPubMedGoogle Scholar
  16. 16.
    Patro-Gołąb B, Zalewski BM, Kouwenhoven SM et al (2016) Protein concentration in milk formula, growth, and later risk of obesity: a systematic review. J Nutr 146:551–564. CrossRefPubMedGoogle Scholar
  17. 17.
    Gruszfeld D, Weber M, Gradowska K et al (2016) Association of early protein intake and pre-peritoneal fat at five years of age: follow-up of a randomized clinical trial. Nutr Metab Cardiovasc Dis 26:824–832. CrossRefPubMedGoogle Scholar
  18. 18.
    Socha P, Grote V, Gruszfeld D et al (2011) Milk protein intake, the metabolic-endocrine response, and growth in infancy: data from a randomized clinical trial. Am J Clin Nutr 94:1776S–1784S. CrossRefPubMedGoogle Scholar
  19. 19.
    Ketelslegers JM, Maiter D, Maes M et al (1996) Nutritional regulation of the growth hormone and insulin-like growth factor-binding proteins. Horm Res 45:252–257. CrossRefPubMedGoogle Scholar
  20. 20.
    Miller E (1987) The pig as a model for human nutrition. Ann Rev Nutr 7:361–382. CrossRefGoogle Scholar
  21. 21.
    National Research Council (2012) Nutrient requirements of swine, Eleventh revised edition. Animal nutrition series. National Academies Press, WashingtonGoogle Scholar
  22. 22.
    Bassler R (1976) Die chemische Untersuchung von Futtermitteln, Methodenbuch, 3rd edn. VDLUFA-Verl., DarmstadtGoogle Scholar
  23. 23.
    Hara A, Radin NS (1978) Lipid extraction of tissues with a low-toxicity solvent. Anal Biochem 90:420–426CrossRefGoogle Scholar
  24. 24.
    Hoff JL de, Davidson LM, Kritchevsky D (1978) An enzymatic assay for determining free and total cholesterol in tissue. Clin Chem 24:433–435PubMedGoogle Scholar
  25. 25.
    BVL (2006) Amtliche Sammlung von Untersuchungsverfahren nach § 64 LFGB, § 38 TabakerzG, § 28b GenTG: (L). In: Amtliche Sammlung von Untersuchungsverfahren nach § 64 LFGB, § 38 TabakerzG, § 28b GenTG. Beuth Verlag, BerlinGoogle Scholar
  26. 26.
    Teerlink T (1994) Derivatization of posttranslationally modified amino acids. J Chromatogr B Biomed Appl 659:185–207CrossRefGoogle Scholar
  27. 27.
    Schuster R (1988) Determination of amino acids in biological, pharmaceutical, plant and food samples by automated precolumn derivatization and high-performance liquid chromatography. J Chromatogr 431:271–284CrossRefGoogle Scholar
  28. 28.
    Kühne H, Hause G, Grundmann SM et al (2016) Vitamin D receptor knockout mice exhibit elongated intestinal microvilli and increased ezrin expression. Nutr Res 36:184–192. CrossRefPubMedGoogle Scholar
  29. 29.
    Behr M, Humbeck K, Hause G et al (2010) The hemibiotroph Colletotrichum graminicola locally induces photosynthetically active green islands but globally accelerates senescence on aging maize leaves. Mol Plant Microbe Interact 23:879–892. CrossRefPubMedGoogle Scholar
  30. 30.
    Godfrey K, Robinson S, Barker D et al (1996) Maternal nutrition in early and late pregnancy in relation to placental and fetal growth. BMJ 312:410. CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Cucó G, Arija V, Iranzo R et al (2006) Association of maternal protein intake before conception and throughout pregnancy with birth weight. Acta Obstet Gynecol Scand 85:413–421. CrossRefPubMedGoogle Scholar
  32. 32.
    Elliott RF, Vander Noot GW, Gilbreath RL et al (1971) Effect of dietary protein level on composition changes in sow colostrum and milk. J Anim Sci 32:1128–1137. CrossRefPubMedGoogle Scholar
  33. 33.
    Laspiur JP, Burton JL, Weber PSD et al (2009) Dietary protein intake and stage of lactation differentially modulate amino acid transporter mRNA abundance in porcine mammary tissue. J Nutr 139:1677–1684. CrossRefPubMedGoogle Scholar
  34. 34.
    Hansen AV, Strathe AB, Kebreab E et al (2012) Predicting milk yield and composition in lactating sows: a Bayesian approach. J Anim Sci 90:2285–2298. CrossRefPubMedGoogle Scholar
  35. 35.
    Farmer C (2015) The gestating and lactating sow. Wageningen Academic Publishers, Wageningen. CrossRefGoogle Scholar
  36. 36.
    Farmer C, Guan X, Trottier NL (2008) Mammary arteriovenous differences of glucose, insulin, prolactin and IGF-I in lactating sows under different protein intake levels. Domest Anim Endocrinol 34:54–62. CrossRefPubMedGoogle Scholar
  37. 37.
    Guan X, Pettigrew JE, Ku PK et al (2004) Dietary protein concentration affects plasma arteriovenous difference of amino acids across the porcine mammary gland. J Anim Sci 82:2953–2963. CrossRefPubMedGoogle Scholar
  38. 38.
    King RH, Williams IH (1984) The effect of nutrition on the reproductive performance of first-litter sows 2. Protein and energy intakes during lactation. Anim Prod 38:249–256. CrossRefGoogle Scholar
  39. 39.
    Nie C, He T, Zhang W et al (2018) Branched chain amino acids: beyond nutrition metabolism. Int J Mol Sci 19:954. CrossRefPubMedCentralGoogle Scholar
  40. 40.
    Liu Z, Roy NC, Guo Y et al (2016) Human breast milk and infant formulas differentially modify the intestinal microbiota in human infants and host physiology in rats. J Nutr 146:191–199. CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Institute of Agricultural and Nutritional SciencesMartin Luther University Halle-WittenbergHalle (Saale)Germany
  2. 2.BiocenterMartin Luther University Halle-WittenbergHalle (Saale)Germany
  3. 3.Competence Cluster of Cardiovascular Health and Nutrition (nutriCARD)Halle-Jena-LeipzigGermany

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