The Rationale for Probiotics Improving Reproductive Health and Pregnancy Outcome

American Journal of Reproductive Immunology

Volumn 69, Issue 6, 2013, Pages 558-566

  Reid, Jennifer N S ^a,b   Bisanz, Jordan E ^b,c   Monachese, Marc ^b,c   Burton, Jeremy P ^b   Reid, Gregor ^b,c  

^a UNIVERSITY OF GUELPH   (Canada)

^b LAWSON HEALTH RESEARCH INSTITUTE   (Canada)

^c UNIVERSITY OF WESTERN ONTARIO   (Canada)

Author keywords

Bacterial vaginosis; Fetus; Infant; Lactobacilli; Vagina

Indexed keywords

ARSENIC; CADMIUM; CYCLIC AMP; LEAD; MERCURY; MITOGEN ACTIVATED PROTEIN KINASE; PROBIOTIC AGENT;

ARTICLE; BLASTOCYST; BRAIN; CONCEPTION; ENVIRONMENTAL EXPOSURE; GENITAL SYSTEM; HUMAN; IMMUNITY; INFANT MORTALITY; INFECTION RISK; LACTOBACILLUS; LEAD POISONING; MATERNAL MORTALITY; MATERNAL NUTRITION; MICROBIOME; MICROFLORA; MORBIDITY; PEER REVIEW; PERINEUM; PREGNANCY OUTCOME; PRIORITY JOURNAL; RECTUM; REPRODUCTIVE HEALTH; RISK REDUCTION; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; URINARY TRACT INFECTION; VAGINA CANDIDIASIS;

FEMALE; FERTILITY; GENITALIA, FEMALE; HUMANS; LACTOBACILLUS; PREGNANCY; PREGNANCY COMPLICATIONS; PREGNANCY OUTCOME; PROBIOTICS; REPRODUCTION; REPRODUCTIVE HEALTH;

EID: 84877688426     PISSN: 10467408     EISSN: 16000897     Source Type: Journal    
DOI: 10.1111/aji.12086     Document Type: Article

References (90)

1. Burton JP, Reid G: Evaluation of the bacterial vaginal flora of twenty postmenopausal women by direct (Nugent Score) and molecular (polymerase chain reaction and denaturing gradient gel electrophoresis) techniques. J Infect Dis 2003; 186:1777-1780.
2. 2-producing lactobacilli, and bacterial vaginosis in pregnant women. Clin Infect Dis 1993; 16(Suppl 4):S273-S281.
3. Hummelen R, Macklaim J, Fernandes A, Dickson R, Changalucha J, Gloor GB, Reid G: Deep sequencing of the vaginal microbiome in HIV patients. PLoS ONE 2010; 5:e12078.
4. Anukam KC, Reid G: Organisms associated with bacterial vaginosis in Nigerian women as determined by PCR-DGGE and 16S rRNA gene sequence. Afr Health Sci 2007; 7:68-72.
5. Macklaim JM, Cohen CR, Donders G, Gloor GB, Hill JE, Parham GP, Ravel J, Spear G, van deWijgert WJ, Reid G: Exploring a road map to counter misconceptions about the cervicovaginal microbiome and disease. Reprod Sci 2012; 19:1154-1162.
6. Ma B, Forney LJ, Ravel J: Vaginal microbiome: rethinking health and disease. Annu Rev Microbiol 2012; 66:371-389.
7. Dominguez-Bello MG, Costello EK, Contreras M, Magris M, Hidalgo G, Fierer N, Knight R: Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc Natl Acad Sci U S A 2010; 107:11971-11975.
8. Zhou X, Hansmann MA, Davis CC, Suzuki H, Brown CJ, Schütte U, Pierson JD, Forney LJ: The vaginal bacterial communities of Japanese women resemble those of women in other racial groups. FEMS Immunol Med Microbiol 2010; 58:169-181.
9. Gajer P, Brotman RM, Bai G, Sakamoto J, Schütte UM, Zhong X, Koenig SS, Fu L, Ma ZS, Zhou X, Abdo Z, Forney LJ, Ravel J: Temporal dynamics of the human vaginal microbiota. Sci Transl Med 2012; 4:132ra52.
10. Fethers K, Twin J, Fairley CK, Fowkes FJ, Garland SM, Fehler G, Morton AM, Hocking JS, Tabrizi SN, Bradshaw CS: Bacterial vaginosis (BV) candidate bacteria: associations with BV and behavioural practices in sexually-experienced and inexperienced women. PLoS ONE 2012; 7:e30633.
11. Santiago GL, Cools P, Verstraelen H, Trog M, Missine G, El Aila AN, Verhelst R, Tency I, Claeys G, Temmerman M, Vaneechoutte M: Longitudinal study of the dynamics of vaginal microflora during two consecutive menstrual cycles. PLoS ONE 2011; 6:e28180.
12. Pépin J, Deslandes S, Giroux G, Sobéla F, Khonde N, Diakité S, Demeule S, Labbé AC, Carrier N, Frost E: The complex vaginal flora of West African women with bacterial vaginosis. PLoS ONE 2011; 6:e25082.
13. AbouZahr C, Wardlaw T: Maternal Mortality in 2000: Estimates developed by WHO, UNICEF AND UNFPA. Geneva, World Health Organization, 2003. http://www.who.int.proxy1.lib.uwo.ca/reproductivehealth/publications/maternal_mortality_2000/mme.pdf.
14. Black RE, Cousens S, Johnson HL, Lawn JE, Rudan I, Bassani DG, Jha P, Campbell H, Walker CF, Cibulskis R, Eisele T, Liu L, Mathers C, Child Health Epidemiology Reference Group of WHO UNICEF: Global, regional, and national causes of child mortality in 2008: a systematic analysis. Lancet 2010; 375:1969-1987.
15. Devries KM, Kishor S, Johnson H, Stöckl H, Bacchus LJ, Garcia-Moreno C, Watts C: Intimate partner violence during pregnancy: analysis of prevalence data from 19 countries. Reprod Health Matters 2010; 18:158-170.
16. Chilongozi D, Wang L, Brown L, Taha T, Valentine M, Emel L, Sinkala M, Kafulafula G, Noor RA, Read JS, Brown ER, Goldenberg RL, Hoffman IH0ST: Morbidity and mortality among a cohort of human immunodeficiency virus type 1-infected and uninfected pregnant women and their infants from Malawi, Zambia, and Tanzania. Pediatr Infect Dis J 2008; 27:808-814.
17. Liu L, Johnson HL, Cousens S, Perin J, Scott S, Lawn JE, Rudan I, Campbell H, Cibulskis R, Li M, Mathers C, Black RE, Child Health Epidemiology Reference Group of WHO and UNICEF: Global, regional, and national causes of child mortality: an updated systematic analysis for 2010 with time trends since 2000. Lancet 2012;379:2151-61.
18. FAO/WHO: Evaluation of health and nutritional properties of powder milk and live lactic acid bacteria. Food and Agriculture Organization of the United Nations and World Health Organization Expert Consultation Report 2001. Available at: ftp://ftp.fao.org/es/esn/food/reid.pdf. Accessed April 6, 2012.
19. Novakovic B, Saffery R: The ever growing complexity of placental epigenetics - Role in adverse pregnancy outcomes and fetal programming. Placenta 2012; 33:959-970.
20. Dielubanza EJ, Schaeffer AJ: Urinary tract infections in women. Med Clin North Am 2011; 95:27-41.
21. Quan M: Vaginitis: diagnosis and management. Postgrad Med 2010; 122:117-127.
22. Ilkit M, Guzel AB:The epidemiology, pathogenesis, and diagnosis of vulvovaginal candidosis: a mycological perspective. Crit Rev Microbiol 2011;37:250-261.
23. Hay P: Recurrent bacterial vaginosis. Curr Opin Infect Dis 2009; 22:82-86.
24. Witkin SS, Linhares IM, Giraldo P: Bacterial flora of the female genital tract: function and immune regulation. Best Pract Res Clin Obstet Gynaecol 2007; 21:347-354.
25. Mak P, Siwek M, Pohl J, Dubin A: Menstrual hemocidin HbB115-146 is an acidophilic antibacterial peptide potentiating the activity of human defensins, cathelicidin and lysozyme. Am J Reprod Immunol 2007; 57:81-91.
26. Cohen MS, Black JR, Proctor RA, Sparling PF: Host defences and the vaginal mucosa. A re-evaluation. Scand J Urol Nephrol Suppl 1984; 86:13-22.
27. Borovkova N, Korrovits P, Ausmees K, Türk S, Jõers K, Punab M, Mändar R: Influence of sexual intercourse on genital tract microbiota in infertile couples. Anaerobe 2011; 17:414-418.
28. Marrazzo JM, Thomas KK, Agnew K, Ringwood K: Prevalence and risks for bacterial vaginosis in women who have sex with women. Sex Transm Dis 2010; 37:335-339.
29. Turner AN, Morrison CS, Munjoma MW, Moyo P, Chipato T, Van deWijgert JH: Vaginal practices of HIV-negative Zimbabwean women. Infect Dis Obstet Gynecol 2010;2010.
30. Donders GG, Berger J, Heuninckx H, Bellen G, Cornelis A: Vaginal flora changes on Pap smears after insertion of levonorgestrel-releasing intrauterine device. Contraception 2011; 83:352-356.
31. Kim TK, Thomas SM, Ho M, Sharma S, Reich CI, Frank JA, Yeater KM, Biggs DR, Nakamura N, Stumpf R, Leigh SR, Tapping RI, Blanke SR, Slauch JM, Gaskins HR, Weisbaum JS, Olsen GJ, Hoyer LL, Wilson BA: Heterogeneity of vaginal microbial communities within individuals. J Clin Microbiol 2009; 47:1181-1189.
32. Limperopoulos C, Bassan H, Sullivan NR, Soul JS, Robertson Jr RL, Moore M, Ringer SA, Volpe JJ, du Plessis AJ: Positive screening for autism in ex-preterm infants: prevalence and risk factors. Pediatrics 2008; 121:758-765.
33. Careaga M, Ashwood P: Autism spectrum disorders: from immunity to behavior. Methods Mol Biol 2012; 934:219-240.
34. McLean PG, Bergonzelli GE, Collins SM, Bercik P: Targeting the microbiota-gut-brain axis to modulate behavior: which bacterial strain will translate best to humans? Proc Natl Acad Sci U S A 2012; 109:E174.
35. Cryan JF, Dinan TG: Mind-altering microorganisms: the impact of the gut microbiota on brain and behaviour. Nat Rev Neurosci 2012; 13:701-712.
36. Benach JL, Li E, McGovern MM: A microbial association with autism. MBio 2012; 3:e00019-12.
37. Finegold SM, Downes J, Summanen PH: Microbiology of regressive autism. Anaerobe 2012; 18:260-262.
38. Enos M, Burton JP, Dols J, Buhulata S, Changalucha J, Reid G: Probiotics for the first 1000 days of life in the developing world. Benef Microbes 2013; 1-14. [Epub ahead of print]
39. Limwattananon S, Tangcharoensathien V, Sirilak S: Trends and inequities in where women delivered their babies in 25 low-income countries: evidence from Demographic and Health Surveys. Reprod Health Matters 2011; 19:75-85.
40. Ahmad SA, Sayed MH, Barua S, Khan MH, Faruquee MH, Jalil A, Hadi SA, Talukder HK: Arsenic in drinking water and pregnancy outcomes. Environ Health Perspect 2001; 109:629-631.
41. Bloom MS, Fitzgerald EF, Kim K, Neamtiu I, Gurzau ES: Spontaneous pregnancy loss in humans and exposure to arsenic in drinking water. Int J Hyg Environ Health 2010; 213:401-413.
42. Yunus M, Sohel N, Hore SK, Rahman M: Arsenic exposure and adverse health effects: a review of recent findings from arsenic and health studies in Matlab, Bangladesh. Kaohsiung J Med Sci 2011; 27:371-376.
43. Vahter M: Effects of arsenic on maternal and fetal health. Annu Rev Nutr 2009; 29:381-399.
44. Thompson J, Bannigan J: Cadmium: toxic effects on the reproductive system and the embryo. Reprod Toxicol 2008; 25:304-315.
45. Dorea JG, Donangelo CM: Early (in uterus and infant) exposure to mercury and lead. Clin Nutr 2006; 25:369-376.
46. Monachese M, Burton JP, Reid G: Bioremediation and tolerance of humans to heavy metals through microbial processes: a potential role for probiotics? Appl Environ Microbiol 2012; 78:6397-6404.
47. Saldana TM, Basso O, Hoppin JA, Baird DD, Knott C, Blair A, Alavanja MC, Sandler DP: Pesticide exposure and self-reported gestational diabetes mellitus in the Agricultural Health Study. Diabetes Care 2007; 30:529-534.
48. Manson J, Brabec MJ, Buelke-Sam J, Carlson GP, Chapin RE, Favor JB, Fischer LJ, Hattis D, Lees PS, Perreault-Darney S, Rutledge J, Smith TJ, Tice RR, Working P: NTP-CERHR expert panel report on the reproductive and developmental toxicity of acrylamide. Birth Defects Res B Dev Reprod Toxicol 2005; 74:17-113.
49. Rauch SA, Braun JM, Barr DB, Calafat AM, Khoury J, Montesano AM, Yolton K, Lanphear BP: Associations of prenatal exposure to organophosphate pesticide metabolites with gestational age and birth weight. Environ Health Perspect 2012; 120:1055-1060.
50. Sharma E, Mustafa M, Pathak R, Guleria K, Ahmed RS, Vaid NB, Banerjee BD: A case control study of gene environmental interaction in fetal growth restriction with special reference to organochlorine pesticides. Eur J Obstet Gynecol Reprod Biol 2012; 161:163-169.
51. LaPrairie JL, Schechter JC, Robinson BA, Brennan PA: Perinatal risk factors in the development of aggression and violence. Adv Genet 2011; 75:215-253.
52. Tatsuta N, Nakai K, Murata K, Suzuki K, Iwai-Shimada M, Yaginuma-Sakurai K, Kurokawa N, Nakamura T, Hosokawa T, Satoh H: Prenatal exposures to environmental chemicals and birth order as risk factors for child behavior problems. Environ Res 2012; 114:47-52.
53. Esteban-Vasallo MD, Aragonés N, Pollan M, López-Abente G, Perez-Gomez B: Mercury, cadmium, and lead levels in human placenta: a systematic review. Environ Health Perspect 2012; 120:1369-1377.
54. Gerhardsson L, Lundh T: Metal concentrations in blood and hair in pregnant females in southern Sweden. J Environ Health 2010; 72:37-41.
55. Schoeman K, Bend JR, Hill J, Nash K, Koren G: Defining a lowest observable adverse effect hair concentrations of mercury for neurodevelopmental effects of prenatal methylmercury exposure through maternal fish consumption: a systematic review. Ther Drug Monit 2009; 31:670-682.
56. Schoeman K, Tanaka T, Bend JR, Koren G: Hair mercury levels of women of reproductive age in Ontario, Canada: implications to fetal safety and fish consumption. J Pediatr 2010; 157:127-131.
57. Hastie CE, Smith GC, Mackay DF, Pell JP: Maternal risk of ischaemic heart disease following elective and spontaneous pre-term delivery: retrospective cohort study of 750 350 singleton pregnancies. Int J Epidemiol 2011; 40:914-919.
58. Yeganegi M, Watson CS, Martins A, Kim SO, Reid G, Challis JRG, Bocking AD: 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 labour. Amer J Obstet Gynecol 2009; 200:532.
59. Yeganegi M, Leung CG, Martins A, Kim SO, Reid G, Challis JRG, Bocking AD: Lactobacillus rhamnosus GR-1-induced IL-10 production in human placental trophoblast cells involves activation of JAK/STAT and MAPK pathways. Reprod Sci 2010; 17:1043-1051.
60. Yeganegi M, Leung CG, Martins A, Kim SO, Reid G, Challis JRG, Bocking AD: Lactobacillus rhamnosus GR-1 stimulates colony stimulating factor 3 (granulocyte) (CSF3) output in placental trophoblast cells in a fetal sex-dependant manner. Biol Reprod 2011; 84:18-25.
61. Anukam KC, Osazuwa E, Osemene GI, Ehigiagbe F, Bruce AW, Reid G: Clinical study comparing probiotic Lactobacillus GR-1 and RC-14 with metronidazole vaginal gel to treat symptomatic bacterial vaginosis. Microbes Infect 2006; 13:2772-2776.
62. Martinez RC, Franceschini SA, Patta MC, Quintana SM, Candido RC, Ferreira JC, Pereira DME, Reid G: Improved cure of bacterial vaginosis with single dose of tinidazole (2 g) and Lactobacillus rhamnosus GR-1 and Lactobacillus reuteri RC-14: a randomized, double-blind, placebo-controlled trial. Can J Microbiol 2009; 55:133-138.
63. Hummelen R, Changalucha J, Butamanya NL, Cook A, Habbema JDF, Reid G: Lactobacillus rhamnosus GR-1 and L. reuteri RC-14 to prevent or cure bacterial vaginosis among women with HIV. In. J Gynecol Obstet 2010; 111:245-248.
64. Patel RM, Myers LS, Kurundkar AR, Maheshwari A, Nusrat A, Lin PW: Probiotic bacteria induce maturation of intestinal claudin 3 expression and barrier function. Am J Pathol 2012; 180:626-635.
65. Wang Y, Kirpich I, Liu Y, Ma Z, Barve S, McClain CJ, Feng W: Lactobacillus rhamnosus GG treatment potentiates intestinal hypoxia-inducible factor, promotes intestinal integrity and ameliorates alcohol-induced liver injury. Am J Pathol 2011; 179:2866-2875.
66. García-Ródenas CL, Bergonzelli GE, Nutten S, Schumann A, Cherbut C, Turini M, Ornstein K, Rochat F, Corthésy-Theulaz I: Nutritional approach to restore impaired intestinal barrier function and growth after neonatal stress in rats. J Pediatr Gastroenterol Nutr 2006; 43:16-24.
67. Sherman PM, Ossa JC, Johnson-Henry K: Unraveling mechanisms of action of probiotics. Nutr Clin Pract 2009; 24:10-14.
68. Brantsaeter AL, Myhre R, Haugen M, Myking S, Sengpiel V, Magnus P, Jacobsson B, Meltzer HM: Intake of probiotic food and risk of preeclampsia in primiparous women: the Norwegian Mother and Child Cohort Study. Am J Epidemiol 2011; 174:807-815.
69. Sharafetdinov K, Plotnikova OA, Alekseeva RI, Sentsova TB, Kaganov BS: Influence of a low-calorie diet with inclusion of probiotic product containing bacterias Lactobacillus plantarum Tensia DSM 21380 on clinical and metabolic characteristics in patients with obesity and arterial hypertension. Vopr Pitan 2012; 81:80-85.
70. Kumar M, Nagpal R, Kumar R, Hemalatha R, Verma V, Kumar A, Chakraborty C, Singh B, Marotta F, Jain S, Yadav H: Cholesterol-lowering probiotics as potential biotherapeutics for metabolic diseases. Exp Diabetes Res 2012;2012:902917.
71. Lam V, Su J, Koprowski S, Hsu A, Tweddell JS, Rafiee P, Gross GJ, Salzman NH, Baker JE: Intestinal microbiota determine severity of myocardial infarction in rats. FASEB J 2012; 26:1727-1735.
72. Naruszewicz M, Johansson ML, Zapolska-Downar D, Bukowska H: Effect of Lactobacillus plantarum 299v on cardiovascular disease risk factors in smokers. Am J Clin Nutr 2002; 76:1249-1255.
73. Barker DJ: Sir Richard Doll Lecture. Developmental origins of chronic disease. Public Health 2012; 126:185-189.
74. Tamashiro KL, Moran TH: Perinatal environment and its influences on metabolic programming of offspring. Physiol Behav 2010; 100:560-566.
75. Christian P, Murray-Kolb LE, Khatry SK, Katz J, Schaefer BA, Cole PM, Leclerq SC, Tielsch JM: Prenatal micronutrient supplementation and intellectual and motor function in early school-aged children in Nepal. JAMA 2010; 304:2716-2723.
76. Chang CY, Ke DS, Chen JY: Essential fatty acids and human brain. Acta Neurol Taiwan 2009; 18:231-241.
77. Hennessy AA, Ross RP, Devery R, Stanton C: The health promoting properties of the conjugated isomers of α-linolenic acid. Lipids 2011; 46:105-119.
78. Reid G: Neuroactive probiotics. BioEssays 2011; 33:562.
79. Cardenas I, Mor G, Aldo P, Lang SM, Stabach P, Sharp A, Romero R, Mazaki-Tovi S, Gervasi M, Means RE: Placental viral infection sensitizes to endotoxin-induced pre-term labor: a double hit hypothesis. Am J Reprod Immunol 2011; 65:110-117.
80. Nicholson JK, Holmes E, Kinross J, Burcelin R, Gibson G, Jia W, Pettersson S: Host-gut microbiota metabolic interactions. Science 2012; 336:1262-1267.
81. Bercik P, Collins SM, Verdu EF: Microbes and the gut-brain axis. Neurogastroenterol Motil 2012; 24:405-413.
82. 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; 107:1-6.
83. Thomas CM, Hong T, van Pijkeren JP, Hemarajata P, Trinh DV, Hu W, Britton RA, Kalkum M, Versalovic J: Histamine derived from probiotic Lactobacillus reuteri suppresses TNF via modulation of PKA and ERK signaling. PLoS ONE. 2012;7:e31951.
84. Hummel S, Veltman K, Cichon C, Sonnenborn U, Schmidt MA: Differential targeting of the E-Cadherin/β-Catenin complex by gram-positive probiotic lactobacilli improves epithelial barrier function. Appl Environ Microbiol 2012; 78:1140-1147.
85. Lee YK, Mazmanian SK: Has the microbiota played a critical role in the evolution of the adaptive immune system? Science 2010; 6012:1768-1773.
86. Krauss-Silva L, Moreira ME, Alves MB, Braga A, Camacho KG, Batista MR, Almada-Horta A, Rebello MR, Guerra F: A randomised controlled trial of probiotics for the prevention of spontaneous preterm delivery associated with bacterial vaginosis: preliminary results. Trials 2011; 12:239.
87. Gonzales-Marin C, Spratt DA, Allaker RP: Maternal oral origin of Fusobacterium nucleatum in adverse pregnancy outcomes as determined using the 16S-23S rRNA gene intergenic transcribed spacer region. J Med Microbiol 2013; 1:133-134.
88. Vitali B, Cruciani F, Baldassarre ME, Capursi T, Spisni E, Valerii MC, Candela M, Turroni S, Brigidi P: Dietary supplementation with probiotics during late pregnancy: outcome on vaginal microbiota and cytokine secretion. BMC Microbiol 2012; 12:236.
89. Holscher HD, Czerkies LA, Cekola P, Litov R, Benbow M, Santema S, Alexander DD, Perez V, Sun S, Saavedra JM, Tappenden KA: Bifidobacterium lactis Bb12 enhances intestinal antibody response in formula-fed infants: a randomized, double-blind, controlled trial. JPEN J Parenter Enteral Nutr 2012; 1(Suppl):106S-117S.
90. Reid G: The potential role for probiotic yogurt for people living with HIV/AIDS. Gut Microbes 2010; 1:411-414.