The status of probiotics supplementation during pregnancy

  • Noroyono Wibowo Department of Obstetric and Gynecology, Faculty of Medicine, Universitas Indonesia, Ciptomangunkusumo Hospital, Jakarta
  • Johanes C. Mose Department of Obstetric and Gynecology, Faculty of Medicine, Padjajaran University, Bandung
  • Made K. Karkata Department of Obstetric and Gynecology, Faculty of Medicine, Udayana University, Bali
  • Bangun T. Purwaka Department of Obstetric and Gynecology, Faculty of Medicine, Airlangga University, Surabaya
  • Herman Kristanto Department of Obstetric and Gynecology, Faculty of Medicine, Diponegoro University, Semarang
  • Maisuri T. Chalid Department of Obstetric and Gynecology, Faculty of Medicine, Hasanuddin University, Makassar
  • Yusrawati Yusrawati Department of Obstetric and Gynecology, Faculty of Medicine, Andalas University, Padang
  • Makmur Sitepu Department of Obstetric and Gynecology, Faculty of Medicine, University of Sumatera Utara, Medan
  • Juneke J. Kaeng Department of Obstetric and Gynecology, Faculty of Medicine, Sam Ratulangi University, Medan
  • Nuswil Bernolian Department of Obstetric and Gynecology, Faculty of Medicine, Sriwijaya University, Palembang
  • Damar Prasmusinto Department of Obstetric and Gynecology, Faculty of Medicine, Universitas Indonesia, Ciptomangunkusumo Hospital, Jakarta
  • Rima Irwinda Department of Obstetric and Gynecology, Faculty of Medicine, Universitas Indonesia, Ciptomangunkusumo Hospital, Jakarta
Keywords: preeclampsia, pregnancy, probiotics, prenatal supplementation, preterm labor
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Abstract

Probiotics have been known for their use in medical field for quite a long time. Strong evidences are now available for the use of probiotics in clinical setting. One of the current issues on this topic is the use of probiotics in pregnancy. Recent studies showed that probiotics may be safe and beneficial for prenatal supplementation. In this review, we highlighted several proven use of probiotics supplementation in pregnant women. A few selected strains of probiotics showed promising outcome to prevent preterm labor and preeclampsia, and to reduce atopic eczema but not asthma and wheezing, in offspring of women who had prenatal probiotics supplementation. The mechanism of action responsible for this effect is closely related to the regulation of T cells, although the exact pathways are not defined yet.

References

  1. Jay JM. Modern food microbiology. 6th ed. Maryland, USA: Aspen Publishers, Inc.; 2000. p. 3-5. http://dx.doi.org/10.1007/978-1-4615-4427-2_1

  2. Johannsen E. Probiotic bacteria: their properties and mode of action. SA Fam Pract. 2003;45(3):36-8.

  3. Kumar S. Textbook of Microbiology. 1st ed. Greater Noida, India: Jp Medical Pub; 2012. p. 784. http://dx.doi.org/10.5005/jp/books/11668

  4. Caplice E, Fitzgerald GF. Food fermentations: role of microorganisms in food production and preservation. Int J Food Microbiol. 1999;50(1-2):131-49. http://dx.doi.org/10.1016/S0168-1605(99)00082-3

  5. World Health Organization. Probiotics in food: Health and nutritional properties and guidelines for evaluation. Rome: World Health Organization/Food and Agriculture Organization of The United Nations; 2001.

  6. Bäckhed F, Ley RE, Sonnenburg JL, Peterson DA, Gordon JI. Host-bacterial mutualism in the human intestine. Science. 2005;307(5717):1915-20. http://dx.doi.org/10.1126/science.1104816

  7. Dethlefsen L, McFall-Ngai M, Relman DA. An ecological and evolutionary perspective on human-microbe mutualism and disease. Nature. 2007;449(7164):811-8. http://dx.doi.org/10.1038/nature06245

  8. Hill C, Guarner F, Reid G, Gibson GR, Merenstein DJ, Pot B, et al. Expert consensus document. The International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat Rev Gastroenterol Hepatol. 2014;11(8):506-14. http://dx.doi.org/10.1038/nrgastro.2014.66

  9. Pham M, Lemberg DA, Day AS. Probiotics: sorting the evidence from the myths. Med J Aust. 2008;188(5):304-8.

  10. Charteris WP, Kelly PM, Morelli L, Collins JK. Selective detection, enumeration and identification of potentially probiotic Lactobacillus and Bifidobacterium species in mixed bacterial populations. Int J Food Microbiol. 1997;35(1):1-27. http://dx.doi.org/10.1016/S0168-1605(96)01222-6

  11. Sazawal S, Hiremath G, Dhingra U, Malik P, Deb S, Black RE. Efficacy of probiotics in prevention of acute diarrhoea: a meta-analysis of masked, randomised, placebo-controlled trials. Lancet Infect Dis. 2006;6(6):374-82. http://dx.doi.org/10.1016/S1473-3099(06)70495-9

  12. Hempel S, Newberry SJ, Maher AR, Wang Z, Miles JN, Shanman R, et al. Probiotics for the prevention and treatment of antibiotic-associated diarrhea: a systematic review and meta-analysis. JAMA. 2012;307(18):1959-69. http://dx.doi.org/10.1001/jama.2012.3507

  13. Hoveyda N, Heneghan C, Mahtani KR, Perera R, Roberts N, Glasziou P. A systematic review and meta-analysis: probiotics in the treatment of irritable bowel syndrome. BMC Gastroenterol. 2009;9:15. http://dx.doi.org/10.1186/1471-230X-9-15

  14. Fioramonti J, Theodorou V, Bueno L. Probiotics: what are they? What are their effects on gut physiology?. Best Pract Res Clin Gastroenterol. 2003;17(15):711-24. doi:10.1016/S1521-6918(03)00075-1

  15. Elazab N, Mendy A, Gasana J, Vieira ER, Quizon A, Forno E. Probiotic administration in early life, atopy, and asthma: a meta-analysis of clinical trials. Pediatrics. 2013;132(3):e666-76. doi: 10.1542/peds.2013-0246d

  16. Luoto R, Laitinen K, Nermes M, Isolauri E. Impact of maternal probiotic-supplemented dietary counselling on pregnancy outcome and prenatal and postnatal growth: a double-blind, placebo-controlled study. Br J Nutr. 2010;103(12):1792-9. http://dx.doi.org/10.1017/S0007114509993898

  17. Brantsæter AL, Myhre R, Haugen M, Myking S, Sengpiel V, Magnus P, et al. Intake of probiotic food and risk of preeclampsia in primiparous women: the Norwegian Mother and Child Cohort Study. Am J Epidemiol. 2011;174(7):807-15. http://dx.doi.org/10.1093/aje/kwr168

  18. Yang Y, Guo Y, Kan Q, Zhou XG, Zhou XY, Li Y. A meta-analysis of probiotics for preventing necrotizing enterocolitis in preterm neonates. Braz J Med Biol Res. 2014;47(9):804-10. http://dx.doi.org/10.1590/1414-431X20143857

  19. Boyle RJ, Robins-Browne RM, Tang ML. Probiotic use in clinical practice: what are the risks?. Am J Clin Nutr. 2006;83(6):1256-64.

  20. Wagner RD, Pierson C, Warner T, Dohnalek M, Farmer J, Roberts L, et al. Biotherapeutic effects of probiotic bacteria on candidiasis in immunodeficient mice. Infect Immun. 1997;65(10):4165-72.

  21. Lilly DM, Stillwell RH. Probiotics: growth-promoting factors produced by microorganisms. Science. 1965;147(3659):747-8. http://dx.doi.org/10.1126/science.147.3659.747

  22. Fuller R. Probiotics in man and animals. J Appl Bacteriol. 1989;66(5):365-78. http://dx.doi.org/10.1111/j.1365-2672.1989.tb05105.x

  23. Gibson GR, Roberfroid MB. Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. J Nutr. 1995;125(6):1401-12.

  24. Ohland CL, Macnaughton WK. Probiotic bacteria and intestinal epithelial barrier function. Am J Physiol Gastrointest Liver Physiol. 2010;298(6):G807-19. http://dx.doi.org/10.1152/ajpgi.00243.2009

  25. World Health Organization/Food and Agriculture Organization of the United Nations. Guidelines for the evaluation of probiotics in food. Canada: FAO/WHO Working Group Report; 2002.

  26. Brown M. Modes of action of probiotics: recent developments. J Anim Vet Adv. 2011;10(14):1895-900. http://dx.doi.org/10.3923/javaa.2011.1895.1900

  27. Senok AC, Ismaeel AY, Botta GA. Probiotics: facts and myths. Clin Microbiol Infect. 2005;11(12):958-66. http://dx.doi.org/10.1111/j.1469-0691.2005.01228.x

  28. Bermudez-Brito M, Plaza-Diaz J, Mu-oz-Quezada S, Gómez-Llorente C, Gil A. Probiotic mechanisms of action. Ann Nutr Metab. 2012;61(2):160-74. http://dx.doi.org/10.1159/000342079

  29. Syndman DR. The safety of probiotics. Clin Infect Dis. 2008;46 Suppl 2:S104-11. http://dx.doi.org/10.1086/523331

  30. Marteau P. Safety aspects of probiotic products. Scand J Nutr. 2001;45:22-4. http://dx.doi.org/10.3402/fnr.v45i0.1785

  31. Elias J, Bozzo P, Einarson A. Are probiotics safe for use during pregnancy and lactation?. Can Fam Physician. 2011;57(3):299-301.

  32. Sanders ME, Akkermans LM, Haller D, Hammerman C, Heimbach J, Hörmannsperger G, et al. Safety assessment of probiotics for human use. Gut microbes. 2010;1(3):164-85. http://dx.doi.org/10.4161/gmic.1.3.12127

  33. Mack DR. D(-)-lactic acid-producing probiotics, D(-)-lactic acidosis and infants. Can J Gastroenterol. 2004;18(11):671-5.

  34. Connolly E, Lönnerdal B. D(-)-Lactic acid-producing bacteria: Safe to use in infant formulas. NUTAfoods. 2004;3(3):37-49.

  35. Htyte N, White L, Sandhu G, Jones J, Meisels I. An extreme and life-threatening case of recurrent D-lactate encephalopathy. Nephrol Dial Transplant. 2011;26(4):1432-5. http://dx.doi.org/10.1093/ndt/gfq829

  36. Ku W, Lau DCY, Huen KF. Probiotics Provoked D-lactic acidosis in short bowel syndrome: case report and literature review. HK J Paediatr (new series). 2006;11:246-54.

  37. Munakata S, Arakawa C, Kohira R, Fujita Y, Fuchigami T, Mugishima H. A case of D-lactic acid encephalopathy associated with use of probiotics. Brain Dev. 2010;32(8):691-4. http://dx.doi.org/10.1016/j.braindev.2009.09.024

  38. Papagaroufalis K, Fotiou A, Egli D, Tran LA, Steenhout P. A randomized double blind controlled safety trial evaluating D-lactic acid production in healthy infants fed a Lactobacillus reuteri-containing formula. Nutr Metab Insights. 2014;7:19-27. doi: 10.4137/NMI.S14113

  39. Rolain JM. Food and human gut as reservoirs of transferable antibiotic resistance encoding genes. Front Microbiol. 2013;4:173. http://dx.doi.org/10.3389/fmicb.2013.00173

  40. Shazali N, Foo HL, Loh TC, Choe DW, Abdul Rahim R. Prevalence of antibiotic resistance in lactic acid bacteria isolated from the faeces of broiler chicken in Malaysia. Gut Pathog. 2014;6(1):1. http://dx.doi.org/10.1186/1757-4749-6-1

  41. Gueimonde M, Sánchez B, G de Los Reyes-Gavilán C, Margolles A. Antibiotic resistance in probiotic bacteria. Front Microbiol. 2013;4:202. http://dx.doi.org/10.3389/fmicb.2013.00202

  42. Devirgiliis C, Zinno P, Perozzi G. Update on antibiotic resistance in foodborne Lactobacillus and Lactococcus species. Front Microbiol. 2013;4:301. http://dx.doi.org/10.3389/fmicb.2013.00301

  43. Dugoua JJ, Machado M, Zhu X, Chen X, Koren G, Einarson TR. Probiotic safety in pregnancy: a systematic review and meta-analysis of randomized controlled trials of Lactobacillus, Bifidobacterium, and Saccharomyces spp. J Obstet Gynaecol Can. 2009;31(6):542-52.

  44. Allen SJ, Jordan S, Storey M, Thornton CA, Gravenor M, Garaiova I, et al. Dietary supplementation with Lactobacilli and Bifidobacteria is well tolerated and not associated with adverse events during late pregnancy and early infancy. J Nutr. 2010;140(3):483-8. http://dx.doi.org/10.3945/jn.109.117093

  45. Sykes L, MacIntyre DA, Yap XJ, Ponnampalam S, Teoh TG, Bennett PR. Changes in the Th1:Th2 cytokine bias in pregnancy and the effects of the anti-inflammatory cyclopentenone prostaglandin 15-deoxy-Δ(12,14)-prostaglandin J2. Mediators Inflamm. 2012;2012:416739. http://dx.doi.org/10.1155/2012/416739

  46. Saito S, Nakashima A, Shima T, Ito M. Th1/Th2/Th17 and regulatory T-cell paradigm in pregnancy. Am J Reprod Immunol. 2010;63(6):601-10. http://dx.doi.org/10.1111/j.1600-0897.2010.00852.x

  47. Delcenserie V, Martel D, Lamoureux M, Amiot J, Boutin Y, Roy D. Immunomodulatory effects of probiotics in the intestinal tract. Curr Issues Mol Biol. 2008;10(1-2):37-54.

  48. Tan M, Zhu JC, Du J, Zhang LM, Yin HH. Effects of probiotics on serum levels of Th1/Th2 cytokine and clinical outcomes in severe traumatic brain-injured patients: a prospective randomized pilot study. Crit Care. 2011;15(6):R290. http://dx.doi.org/10.1186/cc10579

  49. who.int [Internet]. Preterm Birth. [update 2014 Nov; cited 2015 Feb]. Available from: http://www.who.int/mediacentre/factsheets/fs363/en/.

  50. Krauss-Silva L, Moreira MEL, Alves MB, Braga A, Camacho KG, Batista MRR, et al. A randomised controlled trial of probiotics for the prevention of spontaneous preterm delivery associated with bacterial vaginosis: preliminary results. Trials. 2011;12:239. http://dx.doi.org/10.1186/1745-6215-12-239

  51. Vitali B, Cruciani F, Baldassarre ME, Capursi T, Spisni E, Valerii MC, et al. Dietary supplementation with probiotics during late pregnancy: outcome on vaginal microbiota and cytokine secretion. BMC Microbiol. 2012;12:236. http://dx.doi.org/10.1186/1471-2180-12-236

  52. Othman M, Neilson JP, Alfirevic Z. Probiotics for preventing preterm labour. Cochrane Database Syst Rev. 2007(1):Cd005941. http://dx.doi.org/10.1002/14651858.cd005941.pub2

  53. Myhre R, Brantsæter AL, Myking S, Gjessing HK, Sengpiel V, Meltzer HM, et al. Intake of probiotic food and risk of spontaneous preterm delivery. Am J Clin Nutr. 2011;93(1):151-7. http://dx.doi.org/10.3945/ajcn.110.004085

  54. Yang S, Li W, Challis JR, Reid G, Kim SO, Bocking AD. Probiotic Lactobacillus rhamnosus GR-1 supernatant prevents lipopolysaccharide-induced preterm birth and reduces inflammation in pregnant CD-1 mice. Am J Obstet Gynecol. 2014;211(1):44.e1-e12. http://dx.doi.org/10.1016/j.ajog.2014.01.029

  55. Yeganegi M, Watson CS, Martins A, Kim SO, Reid G, Challis JR, et al. Effect of Lactobacillus rhamnosus GR-1 supernatant and fetal sex on lipopolysaccharide-induced cytokine and prostaglandin-regulating enzymes in human placental trophoblast cells: implications for treatment of bacterial vaginosis and prevention of preterm labor. Am J Obstet Gynecol. 2009;200(5):532.e1-8. http://dx.doi.org/10.1016/j.ajog.2008.12.032

  56. Yeganegi M. The effect of Lactobacillus rhamnosus GR-1 supernatant on cytokine production and prostaglandins in gestational tissues [thesis]. Ann Arbor: University of Toronto (Canada); 2010.

  57. Dong JY, Szeto IM, Makinen K, Gao Q, Wang J, Qin LQ, et al. Effect of probiotic fermented milk on blood pressure: a meta-analysis of randomised controlled trials. Br J Nutr. 2013;110(7):1188-94. http://dx.doi.org/10.1017/S0007114513001712

  58. Doege K, Grajecki D, Zyriax BC, Detinkina E, Zu Eulenburg C, Buhling KJ. Impact of maternal supplementation with probiotics during pregnancy on atopic eczema in childhood--a meta-analysis. Br J Nutr. 2012;107(1):1-6. http://dx.doi.org/10.1017/S0007114511003400

  59. Pelucchi C, Chatenoud L, Turati F, Galeone C, Moja L, Bach JF, et al. Probiotics supplementation during pregnancy or infancy for the prevention of atopic dermatitis: a meta-analysis. Epidemiology. 2012;23(3):402-14. http://dx.doi.org/10.1097/EDE.0b013e31824d5da2

  60. Bertelsen RJ, Brantsæter AL, Magnus MC, Haugen M, Myhre R, Jacobsson B, et al. Probiotic milk consumption in pregnancy and infancy and subsequent childhood allergic diseases. J Allergy Clin Immunol. 2014;133(1):165-71. http://dx.doi.org/10.1016/j.jaci.2013.07.032

  61. Ouwehand AC. Antiallergic effects of probiotics. J Nutr. 2007;137(3 Suppl 2):794S-7S.

  62. Kalliomäki M, Antoine JM, Herz U, Rijkers GT, Wells JM, Mercenier A. Guidance for substantiating the evidence for beneficial effects of probiotics: prevention and management of allergic diseases by probiotics. J Nutr. 2010;140(3):713S-21S. http://dx.doi.org/10.3945/jn.109.113761

  63. Pali-Schöll I, Renz H, Jensen-Jarolim E. Update on allergies in pregnancy, lactation, and early childhood. J Allergy Clin Immunol. 2009;123(5):1012-21. http://dx.doi.org/10.1016/j.jaci.2009.01.045

  64. Rautava S, Kainonen E, Salminen S, Isolauri E. Maternal probiotic supplementation during pregnancy and breast-feeding reduces the risk of eczema in the infant. J Allergy Clin Immunol. 2012;130(6):1355-60. http://dx.doi.org/10.1016/j.jaci.2012.09.003

  65. Blümer N, Sel S, Virna S, Patrascan CC, Zimmermann S, Herz U, et al. Perinatal maternal application of Lactobacillus rhamnosus GG suppresses allergic airway inflammation in mouse offspring. Clin Exp Allergy. 2007;37(3):348-57. http://dx.doi.org/10.1111/j.1365-2222.2007.02671.x

  66. Feleszko W, Jaworska J, Rha RD, Steinhausen S, Avagyan A, Jaudszus A, et al. Probiotic-induced suppression of allergic sensitization and airway inflammation is associated with an increase of T regulatory-dependent mechanisms in a murine model of asthma. Clin Exp Allergy. 2007;37(4):498-505. http://dx.doi.org/10.1111/j.1365-2222.2006.02629.x

  67. Kim HJ, Kim YJ, Lee SH, Kang MJ, Yu HS, Jung YH, et al. Effects of Lactobacillus rhamnosus on asthma with an adoptive transfer of dendritic cells in mice. J Appl Microbiol. 2013;115(3):872-9. http://dx.doi.org/10.1111/jam.12268

  68. Yu J, Jang SO, Kim BJ, Song YH, Kwon JW, Kang MJ, et al. The effects of Lactobacillus rhamnosus on the prevention of asthma in a murine model. Allergy Asthma Immunol Res. 2010;2(3):199-205. http://dx.doi.org/10.4168/aair.2010.2.3.199

  69. Azad MB, Coneys JG, Kozyrskyj AL, Field CJ, Ramsey CD, Becker AB, et al. Probiotic supplementation during pregnancy or infancy for the prevention of asthma and wheeze: systematic review and meta-analysis. BMJ. 2013;347:f6471. http://dx.doi.org/10.1136/bmj.f6471

Published
2015-06-28
How to Cite
1.
Wibowo N, Mose JC, Karkata MK, Purwaka BT, Kristanto H, Chalid MT, Yusrawati Y, Sitepu M, Kaeng JJ, Bernolian N, Prasmusinto D, Irwinda R. The status of probiotics supplementation during pregnancy. Med J Indones [Internet]. 2015Jun.28 [cited 2019Nov.18];24(2):120-30. Available from: http://mji.ui.ac.id/journal/index.php/mji/article/view/1223
Section
Review Article