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Meta-Analysis
. 2018 Oct 19;10(10):CD003664.
doi: 10.1002/14651858.CD003664.pub6.

Infant formulas containing hydrolysed protein for prevention of allergic disease

David A Osborn  1 , John Kh Sinn, Lisa J Jones
Affiliations
Meta-Analysis

Infant formulas containing hydrolysed protein for prevention of allergic disease

David A Osborn et al. Cochrane Database Syst Rev. .

Abstract

Background: Infant formulas containing hydrolysed proteins have been widely advocated for preventing allergic disease in infants, in place of standard cow's milk formula (CMF). However, it is unclear whether the clinical trial evidence supports this.

Objectives: To compare effects on allergic disease when infants are fed a hydrolysed formula versus CMF or human breast milk. If hydrolysed formulas are effective, to determine what type of hydrolysed formula is most effective, including extensively or partially hydrolysed formula (EHF/PHF). To determine whether infants at low or high risk of allergic disease, and whether infants receiving early short-term (first few days after birth) or prolonged formula feeding benefit from hydrolysed formulas.

Search methods: We searched the Cochrane Central Register of Controlled Trials (CENTRAL 2017, Issue 11), MEDLINE (1948 to 3 November 2017), and Embase (1974 to 3 November 2017). We also searched clinical trials databases, conference proceedings, and the reference lists of retrieved articles and previous reviews for randomised controlled trials and quasi-randomised trials.

Selection criteria: We searched for randomised and quasi-randomised trials that compared use of a hydrolysed formula versus human milk or CMF. Outcomes with ≥ 80% follow-up of participants from eligible trials were eligible for inclusion.

Data collection and analysis: Two review authors independently selected trials, assessed trial quality and extracted data from the included studies. Fixed-effect analyses were performed. The treatment effects were expressed as risk ratio (RR) and risk difference (RD) with 95% confidence intervals and quality of evidence using the GRADE quality of evidence approach. The primary outcome was all allergic disease (including asthma, atopic dermatitis, allergic rhinitis and food allergy).

Main results: A total of 16 studies were included.Two studies assessed the effect of three to four days infant supplementation with an EHF while in hospital after birth versus pasteurised human milk feed. A single study enrolling 90 infants reported no difference in all allergic disease (RR 1.43, 95% CI 0.38 to 5.37) or any specific allergic disease up to childhood including cow's milk allergy (CMA) (RR 7.11, 95% CI 0.35 to 143.84). A single study reported no difference in infant CMA (RR 0.87, 95% CI 0.52 to 1.46; participants = 3559). Quality of evidence was assessed as very low for all outcomes.No eligible trials compared prolonged hydrolysed formula versus human milk feeding.Two studies assessed the effect of three to four days infant supplementation with an EHF versus a CMF. A single study enrolling 90 infants reported no difference in all allergic disease (RR 1.37, 95% CI 0.33 to 5.71; participants = 77) or any specific allergic disease including CMA up to childhood. A single study reported a reduction in infant CMA of borderline significance (RR 0.62, 95% CI 0.38 to 1.00; participants = 3473). Quality of evidence was assessed as very low for all outcomes.Twelve studies assessed the effect of prolonged infant feeding with a hydrolysed formula compared with a CMF. The data showed no difference in all allergic disease in infants (typical RR 0.88, 95% CI 0.76 to 1.01; participants = 2852; studies = 8) and children (typical RR 0.85, 95% CI 0.69 to 1.05; participants = 950; studies = 2), and no difference in any specific allergic disease including infant asthma (typical RR 0.57, 95% CI 0.31 to 1.04; participants = 318; studies = 4), eczema (typical RR 0.93, 95% CI 0.79 to 1.09; participants = 2896; studies = 9), rhinitis (typical RR 0.52, 95% CI 0.14 to 1.85; participants = 256; studies = 3), food allergy (typical RR 1.42, 95% CI 0.87 to 2.33; participants = 479; studies = 2), and CMA (RR 2.31, 95% CI 0.24 to 21.97; participants = 338; studies = 1). Quality of evidence was assessed as very low for all outcomes.

Authors' conclusions: We found no evidence to support short-term or prolonged feeding with a hydrolysed formula compared with exclusive breast feeding for prevention of allergic disease. Very low-quality evidence indicates that short-term use of an EHF compared with a CMF may prevent infant CMA. Further trials are recommended before implementation of this practice.We found no evidence to support prolonged feeding with a hydrolysed formula compared with a CMF for prevention of allergic disease in infants unable to be exclusively breast fed.

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Conflict of interest statement

Review authors DO and JS have been invited speakers at industry‐organised scientific meetings. Neither has accepted an honorarium. LJ has no conflicts of interest to declare.

Figures

1
1
Study flow diagram: review update.
2
2
'Risk of bias' graph: review authors' judgements about each risk of bias item presented as percentages across all included studies.
3
3
'Risk of bias' summary: review authors' judgements about each risk of bias item for each included study.
4
4
Funnel plot of comparison: 4 Prolonged feeding: hydrolysed formula versus cow's milk formula, outcome: 4.1 All allergic disease.
5
5
Funnel plot of comparison: 4 Prolonged feeding: hydrolysed formula versus cow's milk formula, outcome: 4.3 Eczema.
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    1. Fukushima Y, Iwamoto K, Takeuchi‐Nakashima A, Akamatsu N, Fujino‐Numata N, Yoshikoshi M, et al. Preventive effect of whey hydrolysate formulas for mothers and infants against allergy development in infants for the first 2 years. Journal of Nutritional Science and Vitaminology 1997;43(3):397‐411. [PUBMED: 9268927] - PubMed
Giovannini 1994 {published data only}
    1. Giovannini M, Agostoni C, Fiocchi A, Bellu R, Trojan S, Riva E. Antigen‐reduced infant formulas versus human milk: growth and metabolic parameters in the first 6 months of life. Journal of the American College of Nutrition 1994;13(4):357‐63. [PUBMED: 7963141] - PubMed
Halken 1992 {published data only}
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Hartman 1994 {unpublished data only}
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Hattevig 1989 {published data only}
    1. Hattevig G, Kjellman B, Sigurs N, Bjorksten B, Kjellman NI. Effect of maternal avoidance of eggs, cow's milk and fish during lactation upon allergic manifestations in infants. Clinical and Experimental Allergy 1989;19(1):27‐32. [PUBMED: 2702510] - PubMed
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Keller 1996 {published data only}
    1. Keller KM, Burgin‐Wolff A, Lippold R, Wirth S, Lentze MJ. The diagnostic significance of IgG cow's milk protein antibodies re‐evaluated. European Journal of Pediatrics 1996;155(4):331‐7. [PUBMED: 8777930] - PubMed
Knip 2010 {published data only}
    1. Hyytinen M, Savilahti E, Virtanen SM, Harkonen T, Ilonen J, Luopajarvi K, et al. Finnish TRIGR Pilot Study Group. Avoidance of cow's milk‐based formula for at‐risk infants does not reduce development of celiac disease: a randomized controlled trial. Gastroenterology 2017;153(4):961‐70.e3. - PubMed
    1. Knip M, Virtanen SM, Seppa K, Ilonen J, Savilahti E, Vaarala O, et al. Finnish TRIGR Study Group. Dietary intervention in infancy and later signs of beta‐cell autoimmunity. New England Journal of Medicine 2010;363(20):1900‐8. [DOI: 10.1056/NEJMoa1004809; PUBMED: 21067382] - DOI - PMC - PubMed
Knip 2011 {published data only}
    1. Knip M, Akerblom HK, Becker D, Dosch HM, Dupre J, Fraser W, et al. TRIGR Study Group. Hydrolyzed infant formula and early beta‐cell autoimmunity: a randomized clinical trial. JAMA 2014;311(22):2279‐87. [DOI: 10.1001/jama.2014.5610; PUBMED: 24915259] - DOI - PMC - PubMed
    1. Knip M, Virtanen SM, Becker D, Dupre J, Krischer JP, Akerblom HK, TRIGR Study Group. Early feeding and risk of type 1 diabetes: experiences from the Trial to Reduce Insulin‐dependent diabetes mellitus in the Genetically at Risk (TRIGR). American Journal of Clinical Nutrition 2011;94(6 Suppl):1814S‐20S. [DOI: 10.3945/ajcn.110.000711; PUBMED: 21653795] - DOI - PMC - PubMed
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    1. TRIGR Study Group, Akerblom HK, Krischer J, Virtanen SM, Berseth C, Becker D, Dupre J, et al. The trial to reduce IDDM in the genetically at risk (TRIGR) study: recruitment, intervention and follow‐up. Diabetologia 2011;54(3):627‐33; Erratum in: Diabetologia. 2011;54(8):2210. [DOI: 10.1007/s00125-010-1964-9; NCT00179777; PUBMED: 21153533] - DOI - PMC - PubMed
Kuo 2011 {published data only}
    1. Kuo HC, Liu CA, Ou CY, Hsu TY, Wang CL, Huang HC, et al. Partial protein‐hydrolyzed infant formula decreased food sensitization but not allergic diseases in a prospective birth cohort study. International Archives of Allergy and Immunology 2011;154(4):310‐7. [DOI: 10.1159/000321823; PUBMED: 20975282] - DOI - PubMed
Lasekan 2006 {published data only}
    1. Lasekan JB, Koo WW, Walters J, Neylan M, Luebbers S. Growth, tolerance and biochemical measures in healthy infants fed a partially hydrolyzed rice protein‐based formula: a randomized, blinded, prospective trial. Journal of the American College of Nutrition 2006;25(1):12‐9. [PUBMED: 16522927] - PubMed
Lucassen 2000 {published data only}
    1. Lucassen PL, Assendelft WJ, Gubbels JW, Eijk JT, Douwes AC. Infantile colic: crying time reduction with a whey hydrolysate. A double‐blind, randomized, placebo‐controlled trial. Pediatrics 2000;106(6):1349‐54. [PUBMED: 11099588] - PubMed
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    1. Maggio L, Zuppa AA, Sawatzki G, Valsasina R, Schubert W, Tortorolo G. Higher urinary excretion of essential amino acids in preterm infants fed protein hydrolysates. Acta Paediatrica 2005;94(1):75‐84. [PUBMED: 15858965] - PubMed
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Martinez‐Valverde 1993 {unpublished data only}
    1. Martinenez‐Valverde A, Aljma‐Garcia JM. Study and evaluation of serum IgE and specific total IgE against alpha‐lactalbumin, beta‐lactoglobulin and casein with hypoallergenic formulas (HA) and other types of feeding [Thesis]. Spain: Universidad de Malaga, 1993.
Medjad‐Guillou 1992 {published data only}
    1. Medjad‐Guillou N, Henocq A, Arnaud‐Battandier F. Does the hydrolysis of proteins change the acceptability and the digestive tolerance of milk for infants? The results of a comparative and randomized prospective study. Annales de Pediatrie 1992;39(3):202‐6. [PUBMED: 1570949] - PubMed
Mennella 2011a {published data only}
    1. Mennella JA, Castor SM. Sensitive period in flavor learning: effects of duration of exposure to formula flavors on food likes during infancy. Clinical Nutrition 2012;31(6):1022‐5. [DOI: 10.1016/j.clnu.2012.05.005; PUBMED: 22652361] - DOI - PMC - PubMed
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NCT01987154 {published data only}
    1. NCT01987154. Tolerance of an extensively hydrolyzed protein infant formula versus a premature infant formula. clinicaltrials.gov/show/NCT01987154 (first received 19 November 2013).
Nentwich 2003 {published data only}
    1. Nentwich I, Pazdirkova A, Koberska I, Pokojska E, Szepfalusi Z, Lokaj J. Cow milk‐specific humoral and cellular immune response in infants with high risk of atopy under feeding a whey hydrolysate infant formula. Klinische Padiatrie 2003;215(5):275‐9. [DOI: 10.1055/s-2003-42664; PUBMED: 14520590] - DOI - PubMed
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Odelram 1996 {published data only}
    1. Odelram H, Vanto T, Jacobsen L, Kjellman NI. Whey hydrolysate compared with cow's milk‐based formula for weaning at about 6 months of age in high allergy‐risk infants: effects on atopic disease and sensitization. Allergy 1996;51(3):192‐5. [PUBMED: 8781676] - PubMed
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    1. Paronen J, Knip M, Savilahti E, Virtanen SM, Ilonen J, Akerblom HK, et al. Effect of cow's milk exposure and maternal type 1 diabetes on cellular and humoral immunization to dietary insulin in infants at genetic risk for type 1 diabetes. Finnish Trial to Reduce IDDM in the Genetically at Risk Study Group. Diabetes 2000;49(10):1657‐65. [PUBMED: 11016449] - PubMed
Pauls 1996 {published data only}
    1. Pauls J, Bauer K, Versmold H. Randomized controlled trial of formulas with hydrolyzed versus non‐hydrolyzed protein for starting enteral feedings in preterm infants <1500g body weight. Journal of Pediatric Gastroenterology and Nutrition 1996;22:450 (abstract 164).
Picaud 2001 {published data only}
    1. Picaud JC, Lapillonne A, Rigo J, Normand S, Reygrobellet B, Claris O, et al. Nitrogen utilization and bone mineralization in very low birth weight infants fed partially hydrolyzed preterm formula. Seminars in Perinatology 2002;26(6):439‐46; Retraction in: Seminars in Perinatology 2013; 37(2):138. [PUBMED: 12537316] - PubMed
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Porch 1998 {published data only}
    1. Porch MC, Shahane AD, Leiva LE, Elston RC, Sorensen RU. Influence of breast milk, soy or two hydrolyzed formulas on the development of allergic manifestations in infants at risk. Nutrition Research 1998;18(8):1413‐24.
Raupp 1995 {published data only}
    1. Raupp P, Kries R, Gobel C, Fox A, Lemburg P, Schmidt E, et al. Bone density and biochemical parameters of bone mineral metabolism and acid load in preterm infants. Cow's milk formula versus hydrolysed protein preparation. Monatsschr Kinderheilkd 1995;143(7 (Suppl 2)):S140‐6.
Riezzo 2001 {published data only}
    1. Riezzo G, Indrio F, Montagna O, Tripaldi C, Laforgia N, Chiloiro M, et al. Gastric electrical activity and gastric emptying in preterm newborns fed standard and hydrolysate formulas. Journal of Pediatric Gastroenterology and Nutrition 2001;33(3):290‐5. [PUBMED: 11593124] - PubMed
Rigo 1994a {published data only}
    1. Rigo J, Salle BL, Picaud JC, Putet G, Senterre J. Nutritional evaluation of protein hydrolysate formulas. European Journal of Clinical Nutrition 1995;49(Suppl 1):S26‐38. [PUBMED: 8647061] - PubMed
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Rigo 1994b {published data only}
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    1. Savino F, Cresi F, Maccario S, Cavallo F, Dalmasso P, Fanaro S, et al. "Minor" feeding problems during the first months of life: effect of a partially hydrolysed milk formula containing fructo‐ and galacto‐oligosaccharides. Acta Paediatrica Supplement 2003;91(441):86‐90. [PUBMED: 14599049] - PubMed
Savino 2006 {published data only}
    1. Savino F, Palumeri E, Castagno E, Cresi F, Dalmasso P, Cavallo F, et al. Reduction of crying episodes owing to infantile colic: a randomized controlled study on the efficacy of a new infant formula. European Journal of Clinical Nutrition 2006;60(11):1304‐10. [DOI: 10.1038/sj.ejcn.1602457; PUBMED: 16736065] - DOI - PubMed
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    1. Scalabrin D, Berseth C, Marunycz J, Mitmesser S. Long term safety, growth, and health effects of lactobacillus GG (LGG) added to partially and extensively hydrolyzed infant formulas. Allergy: European Journal of Allergy and Clinical Immunology 2009;64(1171):447.
    1. Scalabrin D, Harris C, Johnston WH, Berseth CL. Long‐term safety assessment in children who received hydrolyzed protein formulas with Lactobacillus rhamnosus GG: a 5‐year follow‐up. European Journal of Pediatrics 2017;176(2):217‐24. [DOI: 10.1007/s00431-016-2825-4; PUBMED: 27975116] - DOI - PMC - PubMed
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Schmelzle 2003 {published data only}
    1. Schmelzle H, Wirth S, Skopnik H, Radke M, Knol J, Bockler HM, et al. Randomized double‐blind study of the nutritional efficacy and bifidogenicity of a new infant formula containing partially hydrolyzed protein, a high beta‐palmitic acid level, and nondigestible oligosaccharides. Journal of Pediatric Gastroenterology and Nutrition 2003;36(3):343‐51. [PUBMED: 12604972] - PubMed
Schmidt 1995 {published data only}
    1. Schmidt E, Eden‐Kohler J, Tonkaboni F, Tolle J. Alimentary allergy prevention in infants with increased allergic risk: the effect of different feeding regimens in the first 6 months on atopic manifestations during the first year of life. A large scale feeding trial. Nestle Nutritional Workshop Series. Vol. 34, Baltimore, Maryland: Raven Press, 1995:231‐48.
Schmitz 1992 {published data only}
    1. Schmitz J, Digeon B, Chastang C, Dupouy D, Leroux B, Robillard P, et al. Effects of brief early exposure to partially hydrolyzed and whole cow milk proteins. Journal of Pediatrics 1992;121(5 Pt 2):S85‐9. [PUBMED: 1447639] - PubMed
Schrander 1993 {published data only}
    1. Schrander JJ, Bogart JP, Forget PP, Schrander‐Stumpel CT, Kuijten RH, Kester AD. Cow's milk protein intolerance in infants under 1 year of age: a prospective epidemiological study. European Journal of Pediatrics 1993;152(8):640‐4. [PUBMED: 8404966] - PubMed
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Silva Rey 1996 {unpublished data only}
    1. Silva Rey AL, Garcia G, Nogales A. Preventatibve Effect of a Partially Hydrolyzed Milk Formula [Thesis]. Madrid, Spain, 1996.
Sorensen 2007 {published data only}
    1. Sorensen RU, Inostroza J, Hebal E, Vinet AM, Fierro J. Weaning to a partially hydrolyzed whey formula at three months of age protects against the later development of anti‐cow milk lgE antibodies in comparison to whole cows milk or extensively hydrolyzed whey formulas. Journal of Allergy and Clinical Immunology 2007;119(1):S120.
Staelens 2008 {published data only}
    1. Staelens S, Driessche M, Barclay D, Carrie‐Faessler AL, Haschke F, Verbeke K, et al. Gastric emptying in healthy newborns fed an intact protein formula, a partially and an extensively hydrolysed formula. Clinical Nutrition 2008;27(2):264‐8. [DOI: 10.1016/j.clnu.2007.12.009; PUBMED: 18280619] - DOI - PubMed
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    1. Szajewska H, Albrecht P, Stoinska B, Prochowska A, Gawecka A, Laskowska‐Klita T. Extensive and partial protein hydrolysate preterm formulas: the effect on growth rate, protein metabolism indices, and plasma amino acid concentrations. Journal of Pediatric Gastroenterology and Nutrition 2001;32(3):303‐9. [PUBMED: 11345180] - PubMed
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    1. Vaarala O, Ilonen J, Ruohtula T, Pesola J, Virtanen SM, Harkonen T, et al. Removal of bovine insulin from cow's milk formula and early initiation of beta‐cell autoimmunity in the FINDIA pilot study. Archives of Pediatrics & Adolescent Medicine 2012;166(7):608‐14. [DOI: 10.1001/archpediatrics.2011.1559; PUBMED: 22393174] - DOI - PubMed
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    1. Hauser B, Blecker U, Keymolen K, Suys B, Gerlo E, Vandenplas Y. Plasma amino acid concentrations in term‐born infants fed a whey predominant or a whey hydrolysate formula. JPEN. Journal of Parenteral and Enteral Nutrition 1997;21(1):27‐30. [DOI: 10.1177/014860719702100127; PUBMED: 9002081] - DOI - PubMed
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    1. Xinias I, Analitis A, Vandenplas Y. A synbiotic partial whey hydrolysate with reduced lactose decreases infantile colic and improves quality of life; A randomized open pilot study. Journal of Pediatric Gastroenterology and Nutrition 2017;64:143.
Yu 2014 {published data only}
    1. Yu MX, Zhuang SQ, Wang DH, Zhou XY, Liu XH, Shi LP, et al. Effects of extensively hydrolyzed protein formula on feeding and growth in preterm infants: a multicenter controlled clinical study. Zhongguo Dang Dai Er Ke za Zhi [Chinese Journal of Contemporary Pediatrics] 2014;16(7):684‐90. [PUBMED: 25008873] - PubMed
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References to ongoing studies

NCT01036243 {published data only}
    1. NCT01036243. Digestive tolerance of slightly hydrolyzed starter infant formula with probiotics [Tolerance of a slightly hydrolyzed starter formula containing probiotics]. clinicaltrials.gov/show/NCT01036243 (first received 21 December 2009).
NCT01156493 {published data only}
    1. NCT01156493. Hydrolized protein formula for premature infants [Randomized trial of hydrolyzed protein premature formula]. clinicaltrials.gov/show/ NCT01156493 (first received 02 July 2010).
NCT01210391 {unpublished data only}
    1. NCT01210391. Growth of infants fed an extensively hydrolyzed infant formula [Assessment of growth of infants fed a 100% whey extensively hydrolyzed formula]. clinicaltrials.gov/show/NCT01210391 (first received 28 September 2010).
NCT01700205 {published data only}
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NCT01735123 {unpublished data only}
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References to other published versions of this review

Osborn 2003
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