Abstract
Background:
The achievements in combating the increasing trend of overweight and obesity have thus far been inadequate. The recently discovered instrumental role of the gut microbiota in host metabolism may offer a novel target in the prevention and management of obesity.
Objective:
To evaluate the impact of perinatal probiotic intervention on childhood growth patterns and the development of overweight during a 10-year follow-up.
Patients and methods:
Altogether 159 women were randomized and double-blinded to receive probiotics (1 × 1010 colony-forming units of Lactobacillus rhamnosus GG, ATCC 53103) or placebo 4 weeks before expected delivery; the intervention extending for 6 months postnatally. Anthropometric measurements of the children were taken at the ages of 3, 6, 12 and 24 months and at 4, 7 and 10 years in 113 (72%) children.
Results:
The excessive weight gain was detected to be two-parted; the initial phase of excessive weight gain initiating during fetal period and continuing until 24–48 months of age and a second phase of excessive weight gain starting after the age of 24–48 months. The perinatal probiotic intervention appeared to moderate the initial phase of excessive weight gain, especially among children who later became overweight, but not the second phase of excessive weight gain, the impact being most pronounced at the age of 4 years (P=0.063, analysis of variance for repeated measures). The effect of intervention was also shown as a tendency to reduce the birth-weight-adjusted mean body mass index at the age of 4 years (P=0.080, analysis of covariance).
Conclusions:
Early gut microbiota modulation with probiotics may modify the growth pattern of the child by restraining excessive weight gain during the first years of life. This novel observation calls for further epidemiological and clinical trials, with precise data on early growth patterns and on confounding factors influencing weight development.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 12 print issues and online access
$259.00 per year
only $21.58 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Reilly JJ, Methven E, McDowell ZC, Hacking B, Alexander D, Stewart L et al. Health consequences of obesity. Arch Dis Child 2003; 88: 748–752.
Ebbeling CB, Pawlak DB, Ludwig DS . Childhood obesity: public-health crisis, common sense cure. Lancet 2002; 360: 473–481.
Druet C, Ong KK . Early childhood predictors of adult body composition. Best Pract Res Clin endocrinol Metab 2008; 22: 489–502.
Eriksson J, Forsen T, Osmond C, Barker D . Obesity from cradle to grave. Int J Obes 2003; 27: 722–727.
Hui LL, Schooling M, Leung SS, Mak KH, Ho LM, Lam TH et al. Birth weight, infant growth, and childhood body mass index: Hong Kong's children of 1998 birth cohort. Arch Pediatr Adolesc Med 2008; 162: 212–218.
Ekelund U, Ong K, Linné Y, Neovius M, Brage S, Dunger DB et al. Upward weight percentile crossing in infancy and early childhoos independently predicts fat mass in young adults: the Stockholm Weight Development Study (SWEDES). Am J Clin Nutr 2006; 83: 324–330.
Stettler N, Zemel BS, Kumanyika S, Stalling VA . Infant weight gain and childhood overweight status in a multicenter, cohort study. Pediatrics 2002; 109: 194–199.
Mccarthy A, Hughes R, Tilling K, Davies D, Smith GD, Ben-Shlomo Y . Birth weight; postnatal, infant, and childhood growth; and obesity in young adulthood: evidence from the Barry Caerphilly Growth Study. Am J Clin Nutr 2007; 86: 907–913.
Braddon FE, Rodgers B, Wadsworth ME, Davies JM . Onset of obesity in a 36 year birth cohort study. Br Med J (Clin Res Ed) 1986; 293: 299–303.
Bäckhed F, Ding H, Wang T, Hooper LV, Koh GY, Nagy A et al. The gut microbiota as an environmental factor that regulates fat storage. Proc Natl Acad Sci USA 2004; 101: 15718–15723.
Bäckhed F, Manchester JK, Semenkovich CF, Gordon JI . Mechanisms underlying the resistance to diet-induced obesity in germ-free mice. Proc Natl Acad Sci USA 2007; 104: 979–984.
Cani PD, Amar J, Iglesias MA, Poggi M, Knauf C, Bastelica D et al. Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes 2007; 56: 1761–1772.
Amar J, Burcelin R, Ruidavets JB, Cani PD, Fauvel J, Alessi MC et al. Energy intake is associated with endotoxemia in apparently healthy men. Am J Clin Nutr 2008; 87: 1219–1223.
Collado MC, Isolauri E, Laitinen K, Salminen S . Distinct composition of gut microbiota during pregnancy in overweight and normal-weight women. Am J Clin Nutr 2008; 88: 894–899.
Mackie RI, Sghir A, Gaskins HR . Developmental microbial ecology of the neonatal gastrointestinal tract. Am J Clin Nutr 1999; 69: 1035–1045.
Gueimonde M, Laitinen K, Salminen S, Isolauri E . Breast milk: a source of bifidobacteria for infant gut development and maturation? Neonatology 2007; 92: 64–66.
Wang Z, Xiao G, Yao Y, Guo S, Lu K, Sheng Z . The role of Bifidobacteria in gut barrier function after thermal injury in rats. J Trauma 2006; 61: 650–657.
Cani PD, Neyrinck AM, Fava F, Knauf C, Burcelin RG, Tuohy KM et al. Selective increases of bifidobacteria in gut microflora improve high-fat-diet-induced diabetes in mice through a mechanism associated with endotoxaemia. Diabetologia 2007; 50: 2374–2383.
Kalliomäki M, Collado MC, Salminen S, Isolauri E . Early differences in fecal microbiota composition in children may predict overweight. Am J Clin Nutr 2008; 87: 534–538.
Weiss ST . Obesity: insight into the origins of asthma. Nat Immunol 2005; 6: 537–539.
Thuesen BH, Husemoen LL, Hersoug LG, Pisinger C, Linneberg A . Insulin resistance as a predictor of incident asthma-like symptoms in adults. Clin Exp Allergy 2009; 39: 700–707.
Kalliomäki M, Salminen S, Arvilommi H, Kero P, Koskinen P, Isolauri E . Probiotics in primary prevention of atopic disease: a randomized placebo-controlled trial. Lancet 2001; 357: 1076–1079.
Majamaa H, Isolauri E . Probiotics: a novel approach in the management of food allergy. J Allergy Clin Immunol 1997; 99: 179–185.
Corvalán C, Uauy R, Kain J, Martorell R . Obesity indicators and cardiometabolic status in 4-y-old children. Am J Clin Nutr 2010; 91: 166–174.
Cole TJ, Bellizzi MC, Flegal Km, Dietz WH . Establishing a standard definition for child overweight and obesity worldwide: international survey. BMJ 2000; 320: 1240–1246.
Rolland-Cachera MF, Deheeger M, Bellisle F, Sempe M, Guilloud-Bataille M, Patois E . Adiposity rebound in children: a simple indicator for predicting obesity. Am J Clin Nutr 1984; 39: 129–135.
Dietz WH . Critical periods in childhood for the development of obesity. Am J Clin Nutr 1994; 59: 955–959.
Summerbell CD, Waters E, Edmunds LD, Kelly S, Brown T, Campbell KJ . Interventions for preventing obesity in children. Cochrane Database of Systematic Reviews 2005. Issue 3. Art. no. CD001871.
Pesonen M, Kallio MJ, Siimes MA, Elg P, Björksten F, Ranki A . Cord serum immunoglobulin E as a risk factor for allergic symptoms and sensitization in children and young adults. Pediatr Allergy Immunol 2009; 20: 12–18.
Barker DJ . Maternal nutrition, fetal nutrition, and disease in later life. Nutrition 1997; 13: 807–813.
Barker DJ . The developmental origins of adult disease. J Am Coll Nutr 2004; 23 (6 Suppl): 588S–595S.
von Kries R, Koletzko B, Sauerwald T, von Mutius E, Bameft D, Grunert V et al. Breast feeding and obesity: cross sectional study. BMJ 1999; 319: 147–150.
Kramer MS, Barr RG, Leduc DG, Boisjoly C, Pless IB . Infant determinants of childhood weight and adiposity. J Pediatr 1985; 107: 104–107.
Hotamisligil GS . Inflammation and metabolic disorders. Nature 2006; 444: 860–867.
Uribe A, Alam M, Johansson O, Midtvedt T, Theodorsson E . Microflora modulates endocrine cells in the gastrointestinal mucosa of the rat. Gastroenterology 1994; 107: 1259–1269.
Velagapudi VR, Hezaveh R, Reigstad CS, Gopalacharyulu P, Laxman Y, Islam S et al. The gut microbiota modulates host energy and lipid metabolism in mice. J Lipid Res 2009. e-pub ahead of print 29 December 2009, doi:10.1194/jlr.M002774.
Cani PD, Bibiloni R, Knauf C, Waget A, Neyrinck AM, Delzenne NM et al. Changes in gut microbiota control metabolic endotoxemia-induced inflammation in high-fat diet-induced obesity and diabetes in mice. Diabetes 2008; 57: 1470–1481.
Isolauri E . Probiotics and gut inflammation. Curr Opin Gastroenterol 1999; 15: 534–537.
Cani PD, Possemiers S, Van de Wiele T, Guiot Y, Everard A, Rottier O et al. Changes in gut microbiota control inflammation in obese mice through a mechanism involving GLP-2-driven improvement of gut permeability. Gut 2009; 58: 1091–1103.
Christensen HR, Frokiaer H, Petska JJ . Lactobacilli differentially modulate expression of cytokines and maturation surface markers in murine dendritic cells. J Immunol 2002; 168: 171–178.
Acknowledgements
We would like to thank the families participating in our study, Tuija Poussa, MSc, for statistical consultation, Robert MacGilleon, MA, for language review of the manuscript and Johanna Hvitfelt-Koskelainen for help with the follow-up of participants. The study was supported by grants from the Academy of Finland and European Union (Early Nutrition Programming Project (contracts no. 007036, EARNEST)). Provision of L. rhamnosus GG was by Valio Ltd (Helsinki, Finland).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Competing interests
The authors declare no conflict of interest.
Rights and permissions
About this article
Cite this article
Luoto, R., Kalliomäki, M., Laitinen, K. et al. The impact of perinatal probiotic intervention on the development of overweight and obesity: follow-up study from birth to 10 years. Int J Obes 34, 1531–1537 (2010). https://doi.org/10.1038/ijo.2010.50
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/ijo.2010.50
Keywords
This article is cited by
-
Effects of synbiotic supplementation on anthropometric indices and body composition in overweight or obese children and adolescents: a randomized, double-blind, placebo-controlled clinical trial
World Journal of Pediatrics (2023)
-
Early life Lactobacillus rhamnosus GG colonisation inhibits intestinal tumour formation
British Journal of Cancer (2022)
-
Maternal Intake of Probiotics to Program Offspring Health
Current Nutrition Reports (2022)
-
Reduced gut microbiota diversity in patients with congenital generalized lipodystrophy
Diabetology & Metabolic Syndrome (2022)
-
Effect of prenatal lifestyle intervention on maternal postpartum weight retention and child body mass index z-score at 36 months
International Journal of Obesity (2021)