Gut wall integrity in exclusively breastfed vs. formula-fed infants

Main Article Content

Nur Hayati
Muzal Kadim
Irawan Mangunatmadja
Soepardi Soedibyo
Evita Bermansyah Ifran
Hikari Ambara Sjakti


Background Breast milk has bioactive substances that modulate gastrointestinal maturation and maintain mucosal integrity of the gut in infants. Markers that are both non-invasive and reliable, such as fecal alpha-1 antitrypsin (AAT), calprotectin, and secretory immunoglobulin A (sIgA) have been used to assess gut integrity in adults. Higher AAT levels may imply greater enteric protein loss due to increase intestinal permeability of immaturity gut.

Objective To assess and compare gut integrity of exclusively breastfed (BF) and exclusively formula fed (FF) infants aged 4-6 months.

Methods Subjects were 80 healthy infants (BF=40; FF=40), aged 4-6 months who visited the Pediatric Polyclinic at St. Carolus Hospital, and lived in Pasar Minggu or Cempaka Putih Districts, Jakarta. The fecal AAT was analyzed by an ELISA method. Mann-Whitney and unpaired T-test were used to analyze possible correlations between feeding type and gut integrity.

Results The BF group had significantly higher mean fecal AAT than the FF group (P=0.02). Median sIgA levels were not significantly different between groups (P=0.104). The FF group had a higher mean fecal calprotectin level but this difference was also not significant (P=0.443). There was a significant correlation between breastfeeding and mean fecal AAT level (P=0.02), but no significant correlation with calprotectin (P=0.65) or sIgA (P=0.26).

Conclusion The breastfed group shows better mucosal integrity compared to the formula fed group. Higher mean fecal AAT level in the BF group is related to the AAT content of breast milk. Therefore AAT content of BF group is actually lower than formula fed group which shows greater mucosal integrity in BF group.

Article Details

How to Cite
Hayati N, Kadim M, Mangunatmadja I, Soedibyo S, Ifran E, Sjakti H. Gut wall integrity in exclusively breastfed vs. formula-fed infants. PI [Internet]. 31Aug.2016 [cited 21Jul.2019];56(4):199-04. Available from:
Received 2016-10-03
Accepted 2016-10-03
Published 2016-08-31


1. Diehl-Jones WL, Askin DF. Nutritional modulation of neonatal outcomes. AACN Clin Issues. 2004;15:83-96.
2. Hegar B, Sahetapy M. Air susu ibu dan kesehatan saluran cerna. In: Hegar B, Suradi R, Hendarto A, Partiwi IGA, editors. Bedah ASI. 1st ed. Jakarta: Balai Penerbit FKUI; 2008. p. 57-67.
3. American Academy of Pediatrics Work Group on Breastfeed ing. Breastfeeding and the use of human milk. Pediatrics. 1997;100:1035-9.
4. Besar DS, Eveline PN. Air susu ibu dan hak bayi. In: Hegar B, Suradi R, Hendarto A, Partiwi IGA, editors. Bedah ASI. 1st ed. Jakarta: Balai Penerbit FKUI; 2008. p. 1-16.
5. Hegar B. Nilai menyusui. In: Suradi R, Hegar B, Partiwi IGA, Marzuki AN, Ananta Y, penyunting. Indonesia menyusui. 1st ed. Jakarta: IDAI; 2010 . p. 1-12.
6. Goldman AS. Modulation of the gastrointestinal tract of infants by human milk. Interfaces and interactions. An evolutionary perspective. J Nutr. 2000;130:426S-31S.
7. Colome G, Sierra C, Blasco J, Garcia MV, Valverde E, Sanchez E. Intestinal permeability in different feedings in infancy. Acta Paediatr. 2007;96:69-72.
8. L Le Huero-Luron, Blat S, Boudry G. Breast- vs. formula feeding: impacts on the digestive tract and immediate and long-term health effects. Nutr Res Rev. 2010;23:23-36.
9. Szczawinska-Poplonyk A. Development of mucosal immunity in children: a rationale for sublingual immunotherapy? J Allergy. 2012;10:1-7.
10. Osontokun B, Kocoshis SA. Anatomy and physiology of the small and large intestine. In: Wyllie Hym JS, Kay M, editors. Pediatric gastrointestinal and liver disease, patophysiology, diagnosis, management. 3rd ed. Philadelphia: Elsivier Inc; 2006. p. 5-6.
11. Derikx JPM, Luyer MDP, Heineman EH, Buurman WA. Non-invasive markers of gut wall integrity in health and disease. World J Gastroenterol. 2010;16:5272-79.
12. Oswari H, Prayitno L, Dwipoerwantoro PG, Firmansyah A, Makrides M, Lawley B, et al. Comparison of stool microbiota composition, stool alpha 1-antitrypsin and calprotectin concentrations, and diarrhoeal morbidity of Indonesian infants fed breast milk or probiotic/prebiotic-supplemented formula. J Paediatr Child Health. 2013;49:1032-9.
13. Woodruff C, Fabacher D, Latham C. Fecal alpha 1-antitrypsin and infant feeding. J Pediatr. 1985;106:228-32.
14. Thomas DW, McGilligan KM, Carlson M, Azen SP, Eisenberg LD, Lieberman HM, et al. Fecal alpha 1-antitrypsin and hemoglobin excretion in healthy human milk-, formula-, cow’s milk-fed infants. Pediatrics. 1986;78:305-12.
15. Davidson LA, Lonnerdal B. Fecal alpha 1-antitrypsin in breastfed infants is derived from human milk and is not indicative of enteric protein loss. Acta Paediatr. 1990;79:137-41.
16. Compeotto F, Butel MJ, Kalach N, Derrieux S, Aubert-Jacquin C, Barbot L, et al. High faecal calprotectin concentrations in newborn infants. Arch Dis Child Fetal Neonatal Ed. 2004;89:F353-5.
17. Rosti L, Braga M, Fulcieri C, Sammarco G, Manenti B, Costa E. Formula milk feeding does not increase the release of the inflammatory marker calprotectin, compared to human milk. Pediatr Med Chir. 2011;33:178-81.
18. Strygler B, Nicar MJ, Santangelo WC, Porter JL, Fordtran JS. Alpha 1-antitrypsin excretion in stool in normal subjects and in patients with gastrointestinal disorders. Gastroenterology. 1990;99:1380-7.
19. Bode L. Recent advances on structure, metabolism, and function of human milk oligosaccharides. J Nutr. 2006;136:2127-30.
20. Gopal PK, Gill HS. Oligosaccharides and glycoconjugates in bovine milk and colostrum. Br J Nutr. 2000;84S:69-74.
21. Bakker-Zierikzee AM, Alles MS, Knol J, Kok FK, Tolboom JJ, Bindels JG. Effects of infant formula containing a mixture of galacto- and fructo-oligosaccharides or viable Bifidobacterium animalis on the intestinal microflora during the first 4 months of life. Br J Nutr. 2005;94:783-90.
22. Fagerhol MK. Calprotectin, a faecal marker of organic gastrointestinal abnormality. Lancet. 2000;356:1783-4.
23. Munasir Z, Kurniati N. ASI dan kekebalan tubuh. In: Hegar B, Suradi R, Hendarto A, Partiwi IGA, editors. Bedah ASI. 1st ed. Jakarta: Balai Penerbit FKUI; 2008. p. 69-81.
24. Maruyama K, Hida M, Kohgo T, Fukunaga Y. Changes in salivary and fecal secretory IgA in infants under different feeding regimen. Pediatr Int. 2009;51:342-5.
25. Kuitunen M, Savilahti E. Mucosal IgA, mucosal cow’s milk antibodies, serum cow’s milk antibodies and gastrointestinal permeability in infants. Pediatr Allergy Immunol. 1995; 6:30-5.
26. Hofman LF, Le T. Preliminary pediatric reference range for secretory IgA in saliva using an enzyme immunoassay. Clin Chem. 2002;48:A169-77.
27. Gomela TL. Assessment of gestational age. In: Gomella TL, Cunningham MD, Eyal FG, editors. Neonatology management, procedures, on-call problems, diseases, and drugs. 6th ed. New York: McGraw Hill; 2009. p. 23-31.