Top

Published in:

Open Access 01-03-2021 | Enterostomy | Original Contribution

Fatty acid composition of adipose tissue at term indicates deficiency of arachidonic and docosahexaenoic acid and excessive linoleic acid supply in preterm infants

Authors: K. A. Böckmann, A. von Stumpff, W. Bernhard, A. Shunova, M. Minarski, B. Frische, S. Warmann, E. Schleicher, C. F. Poets, A. R. Franz

Published in: European Journal of Nutrition | Issue 2/2021

Abstract

Background

Arachidonic (ARA) and docosahexaenoic acid (DHA) are constitutive to membrane phospholipids, and essential for brain and overall development. ARA/DHA pools in term infants (TI) are built during the third trimester, stored as adipose tissue triglycerides and predominantly distributed via plasma phosphatidylcholine (PC). In preterm infants (PTI), placental ARA/DHA supply is replaced by linoleic-acid (LA)-enriched nutrition. This study aimed to investigate the impact of PTI nutrition, compared to placental supply, on fatty acid composition in adipose tissue and blood.

Methods

Prospective observational study (4/2017–3/2019) in 12 PTI and 3 PTI with enterostomy (PTI/E) (gestational age (GA) < 32 weeks) with surgical intervention at term (± 6 weeks) and 14 TI (GA ≥ 34 weeks, surgical intervention < 2 weeks postnatally). PTI/E were analyzed descriptively only. PC and triglyceride fatty acids were analyzed with tandem mass spectrometry and gas chromatography, respectively. Results were compared between TI and PTI with Wilcoxon Test and shown as median [25th percentile–75th percentile] mol%.

Results

PTI had less ARA in adipose tissue TG (0.77[0.67–0.87]% vs. 1.04[0.95–1.14]%, p = 0.0003) and plasma PC (20.7[18.7–22.8]% vs. 28.3[22.7–33.5]%, p = 0.011) than TI. PTI also had less DHA in adipose tissue TG (0.6[0.4–0.8]% vs. 1.1[0.8–1.4]%, p = 0.006) and plasma PC (6.4[5.6–7.1]% vs. 8.4[7.8–13.1]%, p = 0.002). LA was increased in PTI’s adipose tissue TG (10.0[8.8–12.3]% vs. 3.0[2.5–3.6]%, p < 0.0001) and plasma PC (48.4[44.6–49.6]% vs. 30.6[24.9–35.6]%, p = 0.0002). Similar differences were observed in erythrocyte PC.

Conclusion

In PTI, LA is increased and ARA/DHA decreased in adipose tissue, plasma and erythrocyte lipids as proxies for other tissues, likely caused by PTI nutrition. This may contribute to impaired PTI development.

Available only for authorised users

The AOCS Lipid Library (2017) Plasma lipoproteins—composition, structure and biochemistry. https://lipidlibraryaocsorg/

Martin CR, Dasilva DA, Cluette-Brown JE, Dimonda C, Hamill A, Bhutta AQ, Coronel E, Wilschanski M, Stephens AJ, Driscoll DF, Bistrian BR, Ware JH, Zaman MM, Freedman SD (2011) Decreased postnatal docosahexaenoic and arachidonic acid blood levels in premature infants are associated with neonatal morbidities. J Pediatr 159(5):743–749. https://doi.org/10.1016/j.jpeds.2011.04.039e741–742CrossRefPubMedPubMedCentral

Lauritzen L, Hansen HS, Jorgensen MH, Michaelsen KF (2001) The essentiality of long chain n-3 fatty acids in relation to development and function of the brain and retina. Prog Lipid Res 40(1–2):1–94CrossRef

Mitchell DC, Niu SL, Litman BJ (2003) Enhancement of G protein-coupled signaling by DHA phospholipids. Lipids 38(4):437–443. https://doi.org/10.1007/s11745-003-1081-1CrossRefPubMed

Mitchell DC, Niu SL, Litman BJ (2003) DHA-rich phospholipids optimize G-Protein-coupled signaling. J Pediatr 143(4 Suppl):S80–S86. https://doi.org/10.1067/s0022-3476(03)00405-0CrossRefPubMed

German OL, Monaco S, Agnolazza DL, Rotstein NP, Politi LE (2013) Retinoid X receptor activation is essential for docosahexaenoic acid protection of retina photoreceptors. J Lipid Res 54(8):2236–2246. https://doi.org/10.1194/jlr.M039040CrossRefPubMedPubMedCentral

SanGiovanni JP, Chew EY (2005) The role of omega-3 long-chain polyunsaturated fatty acids in health and disease of the retina. Prog Retin Eye Res 24(1):87–138. https://doi.org/10.1016/j.preteyeres.2004.06.002CrossRefPubMed

Gawrisch K, Soubias O, Mihailescu M (2008) Insights from biophysical studies on the role of polyunsaturated fatty acids for function of G-protein coupled membrane receptors. Prostaglandins Leukot Essent Fatty Acids 79(3–5):131–134. https://doi.org/10.1016/j.plefa.2008.09.002CrossRefPubMedPubMedCentral

Bazan NG (2018) Docosanoids and elovanoids from omega-3 fatty acids are pro-homeostatic modulators of inflammatory responses, cell damage and neuroprotection. Mol Aspects Med 64:18–33. https://doi.org/10.1016/j.mam.2018.09.003CrossRefPubMedPubMedCentral

10.

Jun B, Mukherjee PK, Asatryan A, Kautzmann MA, Heap J, Gordon WC, Bhattacharjee S, Yang R, Petasis NA, Bazan NG (2017) Elovanoids are novel cell-specific lipid mediators necessary for neuroprotective signaling for photoreceptor cell integrity. Sci Rep 7(1):5279. https://doi.org/10.1038/s41598-017-05433-7CrossRefPubMedPubMedCentral

11.

Clandinin MT, Chappell JE, Heim T, Swyer PR, Chance GW (1981) Fatty acid utilization in perinatal de novo synthesis of tissues. Early Hum Dev 5(4):355–366. https://doi.org/10.1016/0378-3782(81)90016-5CrossRefPubMed

12.

Axelrod J (1990) Receptor-mediated activation of phospholipase A2 and arachidonic acid release in signal transduction. Biochem Soc Trans 18(4):503–507CrossRef

13.

Ordway RW, Singer JJ, Walsh JV Jr (1991) Direct regulation of ion channels by fatty acids. Trends Neurosci 14(3):96–100CrossRef

14.

Innis SM, Adamkin DH, Hall RT, Kalhan SC, Lair C, Lim M, Stevens DC, Twist PF, Diersen-Schade DA, Harris CL, Merkel KL, Hansen JW (2002) Docosahexaenoic acid and arachidonic acid enhance growth with no adverse effects in preterm infants fed formula. J Pediatr 140(5):547–554. https://doi.org/10.1067/mpd.2002.123282CrossRefPubMed

15.

Piomelli D (1994) Eicosanoids in synaptic transmission. Crit Rev Neurobiol 8(1–2):65–83PubMed

16.

Rau GA, Vieten G, Haitsma JJ, Freihorst J, Poets C, Ure BM, Bernhard W (2004) Surfactant in newborn compared with adolescent pigs: adaptation to neonatal respiration. Am J Respir Cell Mol Biol 30(5):694–701. https://doi.org/10.1165/rcmb.2003-0351OCCrossRefPubMed

17.

Dombrowsky H, Clark GT, Rau GA, Bernhard W, Postle AD (2003) Molecular species compositions of lung and pancreas phospholipids in the cftr(tm1HGU/tm1HGU) cystic fibrosis mouse. Pediatr Res 53(3):447–454. https://doi.org/10.1203/01.pdr.0000049937.30305.8aCrossRefPubMed

18.

Bernhard W, Haagsman HP, Tschernig T, Poets CF, Postle AD, van Eijk ME, von der Hardt H (1997) Conductive airway surfactant: surface-tension function, biochemical composition, and possible alveolar origin. Am J Respir Cell Mol Biol 17(1):41–50. https://doi.org/10.1165/ajrcmb.17.1.2594CrossRefPubMed

19.

Bernhard W, Hoffmann S, Dombrowsky H, Rau GA, Kamlage A, Kappler M, Haitsma JJ, Freihorst J, von der Hardt H, Poets CF (2001) Phosphatidylcholine molecular species in lung surfactant: composition in relation to respiratory rate and lung development. Am J Respir Cell Mol Biol 25(6):725–731. https://doi.org/10.1165/ajrcmb.25.6.4616CrossRefPubMed

20.

Bernhard W, Maas C, Shunova A, Mathes M, Bockmann K, Bleeker C, Vek J, Poets CF, Schleicher E, Franz AR (2018) Transport of long-chain polyunsaturated fatty acids in preterm infant plasma is dominated by phosphatidylcholine. Eur J Nutr 57(6):2105–2112. https://doi.org/10.1007/s00394-017-1484-1CrossRefPubMed

21.

Svennerholm L (1968) Distribution and fatty acid composition of phosphoglycerides in normal human brain. J Lipid Res 9(5):570–579CrossRef

22.

Makrides M, Neumann MA, Byard RW, Simmer K, Gibson RA (1994) Fatty acid composition of brain, retina, and erythrocytes in breast- and formula-fed infants. Am J Clin Nutr 60(2):189–194. https://doi.org/10.1093/ajcn/60.2.189CrossRefPubMed

23.

Haggarty P (2010) Fatty acid supply to the human fetus. Annu Rev Nutr 30:237–255. https://doi.org/10.1146/annurev.nutr.012809.104742CrossRefPubMed

24.

Bernhard W, Raith M, Koch V, Kunze R, Maas C, Abele H, Poets CF, Franz AR (2014) Plasma phospholipids indicate impaired fatty acid homeostasis in preterm infants. Eur J Nutr 53(7):1533–1547. https://doi.org/10.1007/s00394-014-0658-3CrossRefPubMed

25.

Farquharson J, Cockburn F, Patrick WA, Jamieson EC, Logan RW (1993) Effect of diet on infant subcutaneous tissue triglyceride fatty acids. Arch Dis Child 69(5):589–593CrossRef

26.

Bernhard W, Poets CF, Franz AR (2019) Choline and choline-related nutrients in regular and preterm infant growth. Eur J Nutr 58(3):931–945. https://doi.org/10.1007/s00394-018-1834-7CrossRefPubMed

27.

Pynn CJ, Henderson NG, Clark H, Koster G, Bernhard W, Postle AD (2011) Specificity and rate of human and mouse liver and plasma phosphatidylcholine synthesis analyzed in vivo. J Lipid Res 52(2):399–407. https://doi.org/10.1194/jlr.D011916CrossRefPubMedPubMedCentral

28.

Maas C, Poets CF, Franz AR (2015) Avoiding postnatal undernutrition of VLBW infants during neonatal intensive care: evidence and personal view in the absence of evidence. Arch Dis Child Fetal Neonatal Ed 100(1):F76–F81. https://doi.org/10.1136/archdischild-2014-306195CrossRefPubMed

29.

Agostoni C, Buonocore G, Carnielli VP, De Curtis M, Darmaun D, Decsi T, Domellof M, Embleton ND, Fusch C, Genzel-Boroviczeny O, Goulet O, Kalhan SC, Kolacek S, Koletzko B, Lapillonne A, Mihatsch W, Moreno L, Neu J, Poindexter B, Puntis J, Putet G, Rigo J, Riskin A, Salle B, Sauer P, Shamir R, Szajewska H, Thureen P, Turck D, van Goudoever JB, Ziegler EE (2010) Enteral nutrient supply for preterm infants: commentary from the European Society of Paediatric Gastroenterology, Hepatology and Nutrition Committee on Nutrition. J Pediatr Gastroenterol Nutr 50(1):85–91. https://doi.org/10.1097/MPG.0b013e3181adaee0CrossRefPubMed

30.

Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37(8):911–917. https://doi.org/10.1139/o59-099CrossRefPubMed

31.

Maas C, Franz AR, Shunova A, Mathes M, Bleeker C, Poets CF, Schleicher E, Bernhard W (2017) Choline and polyunsaturated fatty acids in preterm infants’ maternal milk. 56(4):1733–1742. https://doi.org/10.1007/s00394-016-1220-2CrossRef

32.

Raith M, Schaal K, Koslowski R, Fehrenbach H, Poets CF, Schleicher E, Bernhard W (2012) Effects of recombinant human keratinocyte growth factor on surfactant, plasma, and liver phospholipid homeostasis in hyperoxic neonatal rats. J Appl Physiol 112(8):1317–1328. https://doi.org/10.1152/japplphysiol.00887.2011CrossRefPubMed

33.

Pynn CJ, Picardi MV, Nicholson T, Wistuba D, Poets CF, Schleicher E, Perez-Gil J, Bernhard W (2010) Myristate is selectively incorporated into surfactant and decreases dipalmitoylphosphatidylcholine without functional impairment. Am J Physiol Regul Integr Comp Physiol 299(5):R1306–R1316. https://doi.org/10.1152/ajpregu.00380.2010CrossRefPubMed

34.

Bernhard W, Raith M, Koch V, Maas C, Abele H, Poets CF, Franz AR (2016) Developmental changes in polyunsaturated fetal plasma phospholipids and feto-maternal plasma phospholipid ratios and their association with bronchopulmonary dysplasia. Eur J Nutr 55(7):2265–2274. https://doi.org/10.1007/s00394-015-1036-5CrossRefPubMed

35.

Lapillonne A, Jensen CL (2009) Reevaluation of the DHA requirement for the premature infant. Prostaglandins Leukot Essent Fatty Acids 81(2–3):143–150. https://doi.org/10.1016/j.plefa.2009.05.014CrossRefPubMed

36.

Innis SM (2005) Essential fatty acid transfer and fetal development. Placenta 26:S70–S75. https://doi.org/10.1016/j.placenta.2005.01.005CrossRefPubMed

37.

Liefaard G, Heineman E, Molenaar JC, Tibboel D (1995) Prospective evaluation of the absorptive capacity of the bowel after major and minor resections in the neonate. J Pediatr Surg 30(3):388–391. https://doi.org/10.1016/0022-3468(95)90038-1CrossRefPubMed

38.

Bernhard W, Bockmann K, Maas C, Mathes M, Hovelmann J, Shunova A, Hund V, Schleicher E, Poets CF, Franz AR (2019) Combined choline and DHA supplementation: a randomized controlled trial. Eur J Nutr. https://doi.org/10.1007/s00394-019-01940-7CrossRefPubMed

39.

Alshweki A, Munuzuri AP, Bana AM, de Castro MJ, Andrade F, Aldamiz-Echevarria L, de Pipaon MS, Fraga JM, Couce ML (2015) Effects of different arachidonic acid supplementation on psychomotor development in very preterm infants; a randomized controlled trial. Nutr J 14:101. https://doi.org/10.1186/s12937-015-0091-3CrossRefPubMedPubMedCentral

40.

Delplanque B, Gibson R, Koletzko B, Lapillonne A, Strandvik B (2015) Lipid quality in infant nutrition: current knowledge and future opportunities. J Pediatr Gastroenterol Nutr 61(1):8–17. https://doi.org/10.1097/mpg.0000000000000818CrossRefPubMedPubMedCentral

41.

Commission E (2016) Commission Delegated Regulation (EU) 2016/127 of 25 September 2015 supplementing Regulation (EU) No 609/2013 of the European Parliament and of the Council as regards the specific compositional and information requirements for infant formula and follow-on formula and as regards requirements on information relating to infant and young child feeding. Off J Eur Union:(L 25/21):21–29

42.

Koletzko B, Bergmann K, Brenna JT, Calder PC, Campoy C, Clandinin MT, Colombo J, Daly M, Decsi T, Demmelmair H, Domellof M, FidlerMis N, Gonzalez-Casanova I, van Goudoever JB, Hadjipanayis A, Hernell O, Lapillonne A, Mader S, Martin CR, Matthaus V, Ramakrishan U, Smuts CM, Strain SJJ, Tanjung C, Tounian P, Carlson SE (2020) Should formula for infants provide arachidonic acid along with DHA? A position paper of the European Academy of Paediatrics and the Child Health Foundation. Am J Clin Nutr 111(1):10–16. https://doi.org/10.1093/ajcn/nqz252CrossRefPubMed

43.

Christoph Bührer RE, Frank Jochum, Hermann Kalhoff, Antje Körner, Berthold Koletzko, Burkhard Lawrenz, Walter Mihatsch, Silvia Rudloff, Klaus-Peter Zimmer &, V.) EdDGfK-uJDe (2020) Sollen Säuglingsnahrungen sowohl Docosahexaensäure als auch Arachidonsäure enthalten? Monatsschrift Kinderheilkunde March 24

44.

Collins CT, Gibson RA, Makrides M, McPhee AJ, Sullivan TR, Davis PG, Thio M, Simmer K, Rajadurai VS (2016) The N3RO trial: a randomised controlled trial of docosahexaenoic acid to reduce bronchopulmonary dysplasia in preterm infants < 29 weeks’ gestation. BMC Pediatr 16:72. https://doi.org/10.1186/s12887-016-0611-0CrossRefPubMedPubMedCentral

Title: Fatty acid composition of adipose tissue at term indicates deficiency of arachidonic and docosahexaenoic acid and excessive linoleic acid supply in preterm infants
Authors: K. A. Böckmann
A. von Stumpff
W. Bernhard
A. Shunova
M. Minarski
B. Frische
S. Warmann
E. Schleicher
C. F. Poets
A. R. Franz
Publication date: 01-03-2021
Publisher: Springer Berlin Heidelberg
Keywords: Enterostomy
Nutrition
Enterostomy
Published in: European Journal of Nutrition / Issue 2/2021
Print ISSN: 1436-6207
Electronic ISSN: 1436-6215
DOI: https://doi.org/10.1007/s00394-020-02293-2

Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Pediatric Cardiology Video

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

Cardiopulmonary Comorbidity Video

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Valvular Heart Disease Video

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Heart Failure Video

Watch this official video from ACC.24. Dr. Biykem Bozkurt discuss last year's major advances in heart failure and cardiomyopathies.

ACC 2024 Congress Coverage

Heart Failure Video

Year in Review: Heart failure and cardiomyopathies

Watch now

Watch this official video from ACC.24. Dr. Biykem Bozkurt discuss last year's major advances in heart failure and cardiomyopathies.

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

16-04-2024 Type 2 Diabetes News

Incentivised to exercise

11-04-2024 Lifestyle Modifications News

New intervention for STEMI-related cardiogenic shock

10-04-2024 Myocardial Infarction News

» View more highlights on the ACC 2024 congress hub page

Image Credits

STEP AAG HeroTeaserCollection image/© Tarek / Generated with AI / Stock.adobe.com, ACC 2024 Pediatric and Congenital Heart Disease: Year in Review/© 2024 American College of Cardiology, ACC 2024 Pulmonary Vascular Disease: Year in Review/© 2024 American College of Cardiology, ACC 2024 Valvular Heart Disease: Year in Review/© 2024 American College of Cardiology, ACC 2024 HF and Cardiomyopathies: Year in Review/© 2024 American College of Cardiology, Woman out walking/© Seventyfour / stock.adobe.com (symbolic image with model), Woman checking smartwatch /© saltdium / stock.adobe.com (symbolic image with model), Cardiac catheterization/© Damian / stock.adobe.com

At a glance: The STEP trials

Springer Medicine

Abstract

Background

Methods

Results

Conclusion

Please log in to get access to this content

Other articles of this Issue 2/2021

Depressive symptoms, fruit and vegetables consumption and urinary 3-indoxylsulfate concentration: a nested case–control study in the French Nutrinet-Sante cohort

Synergetic responses of intestinal microbiota and epithelium to dietary inulin supplementation in pigs

Breast milk n-3 long-chain polyunsaturated fatty acids and blood pressure: an individual participant meta-analysis

Caribbean nutrition transition: what can we learn from dietary patterns in the French West Indies?

Hesperidin ameliorates signs of the metabolic syndrome and cardiac dysfunction via IRS/Akt/GLUT4 signaling pathway in a rat model of diet-induced metabolic syndrome

Cardiometabolic risk profile and diet quality among internal migrants in Brazil: a population-based study

Highlights from the ACC 2024 Congress

ACC 2024 Congress Coverage