The development of probiotics for women’s health

Canadian Journal of Microbiology

Volumn 63, Issue 4, 2017, Pages 269-277

  Reid, Gregor ^a,b  

^a LAWSON HEALTH RESEARCH INSTITUTE   (Canada)

^b UNIVERSITY OF WESTERN ONTARIO   (Canada)

Author keywords

Fermented food; Lactobacillus; Probiotics; Urinary tract; Vaginal

Indexed keywords

PROBIOTIC AGENT;

ANTIBIOTICS; BACTERIUM; DISEASE TREATMENT; FERMENTATION; INFECTIOUS DISEASE; PROBIOTICS; WOMENS HEALTH;

COMMERCIAL PHENOMENA; HUMAN; LACTOBACILLUS; NONHUMAN; PRIORITY JOURNAL; PROCESS DEVELOPMENT; REVIEW; WOMEN'S HEALTH; FEMALE; MICROBIOLOGY; VAGINA;

LACTOBACILLUS;

FEMALE; HUMANS; LACTOBACILLUS; PROBIOTICS; VAGINA; WOMEN'S HEALTH;

EID: 85016954006     PISSN: 00084166     EISSN: 14803275     Source Type: Journal    
DOI: 10.1139/cjm-2016-0733     Document Type: Review

References (99)

1. Allen, S.J., Wareham, K., Wang, D., Bradley, C., Sewell, B., Hutchings, H., et al. 2013. A high-dose preparation of lactobacilli and bifidobacteria in the prevention of antibioticassociated and Clostridium difficile diarrhoea in older people admitted to hospital: a multicentre, randomised, doubleblind, placebo-controlled, parallel arm trial (PLACIDE). Health Technol. Assess. 17(57): 1-140. doi:10.3310/hta17570. PMID: 24309198.
2. Anukam, K., Osazuwa, E., Ahonkhai, I., Ngwu, M., Osemene, G., Bruce, A.W., and Reid, G. 2006a. Augmentation of antimicrobial metronidazole therapy of bacterial vaginosis with oral probiotic Lactobacillus rhamnosus GR-1 and Lactobacillus reuteri RC-14: randomized, double-blind, placebo controlled trial. Microbes Infect. 8(6): 1450-1454. doi:10.1016/j.micinf.2006.01.003. PMID:16697231.
3. Anukam, K.C., Osazuwa, E.O., Ahonkhai, I., and Reid, G. 2006b. Lactobacillus vaginal microbiota of women attending a reproductive health care service in Benin city, Nigeria. Sex. Transm. Dis. 33(1): 59-62. doi:10.1097/01.olq.0000175367.15559.c4. PMID: 16385223.
4. Anukam, K.C., Osazuwa, E., Osemene, G.I., Ehigiagbe, F., Bruce, A.W., and Reid, G. 2006c. Clinical study comparing probiotic Lactobacillus GR-1 and RC-14 with metronidazole vaginal gel to treat symptomatic bacterial vaginosis. Microbes Infect. 8(12-13): 2772-2776. doi:10.1016/j.micinf.2006.08.008. PMID:17045832.
5. Anukam, K.C., Osazuwa, E.O., Osadolor, H.B., Bruce, A.W., and Reid, G. 2008. Yogurt containing probiotic Lactobacillus rhamnosus GR-1 and L. reuteri RC-14 helps resolve moderate diarrhea and increases CD4 count in HIV/AIDS patients. J. Clin. Gastroenterol. 42(3): 239-243. doi:10.1097/MCG.0b013e31802c7465. PMID: 18223503.
6. Arinaitwe, K., Kiremire, B.T., Muir, D.C., Fellin, P., Li, H., Teixeira, C., and Mubiru, D.N. 2016. Legacy and currently used pesticides in the atmospheric environment of Lake Victoria, East Africa. Sci. Total Environ. 543(Pt A): 18. doi:10.1016/j.scitotenv.2015.10.146.
7. Arroyo, R., Martín, V., Maldonado, A., Jiménez, E., Fernández, L., and Rodríguez, J.M. 2010. Treatment of infectious mastitis during lactation: antibiotics versus oral administration of lactobacilli isolated from breast milk. Clin. Infect. Dis. 50(12): 1551-1558. doi:10.1086/652763. PMID:20455694.
8. Atlas, R.M. 1999. Probiotics - Snake oil for the new millennium? Environ. Microbiol. 1(5): 377-382. doi:10.1046/j.1462-2920.1999.00063.x. PMID:11207756.
9. Banupriya, B., Biswal, N., Srinivasaraghavan, R., Narayanan, P., and Mandal, J. 2015. Probiotic prophylaxis to prevent ventilator associated pneumonia (VAP) in children on mechanical ventilation: an open-label randomized controlled trial. Intensive Care Med. 41(4): 677-685. doi:10.1007/s00134-015-3694-4. PMID:25708419.
10. Barker, D.J. 1990. The fetal and infant origins of adult disease. BMJ, 301: 1111. doi:10.1136/bmj.301.6761.1111. PMID:2252919.
11. Baroja, M., Kirjavainen, P.V., Hekmat, S., and Reid, G. 2007. Anti-inflammatory effects of probiotic yogurt in inflammatory bowel disease patients. Clin. Exp. Immunol. 149(3): 470-479. doi:10.1111/j.1365-2249.2007.03434.x. PMID:17590176.
12. Beerepoot, M.A., ter Riet, G., Nys, S., van der Wal, W.M., de Borgie, C.A., de Reijke, T.M., et al. 2012. Lactobacilli vs antibiotics to prevent urinary tract infections: a randomized, double-blind, noninferiority trial in postmenopausal women. Arch. Intern. Med. 172(9): 704-712. doi:10.1001/archinternmed. 2012.777. PMID:22782199.
13. Bisanz, J.E., Enos, M.K., Mwanga, J.R., Changalucha, J., Burton, J.P., Gloor, G.B., and Reid, G. 2014a. Randomized open-label pilot study of the influence of probiotics and the gut microbiome on toxic metal levels in Tanzanian pregnant women and school children. mBio, 5(5): e01580-14. PMID: 25293764.
14. Bisanz, J.E., Seney, S., McMillan, A., Vongsa, R., Koenig, D., Wong, L., et al. 2014b. A systems biology approach investigating the effect of probiotics on the vaginal microbiome and host responses in a double blind, placebo-controlled clinical trial of post-menopausal women. PLoS One, 9(8): e104511. doi: 10.1371/journal.pone.0104511. PMID:25127240.
15. Blaser, M.J. 2016. Antibiotic use and its consequences for the normal microbiome. Science, 352(6285): 544-545. doi:10.1126/science.aad9358. PMID:27126037.
16. Bruce, A.W., and Reid, G. 1988. Intravaginal instillation of lactobacilli for prevention of recurrent urinary tract infections. Can. J. Microbiol. 34: 339-343. doi:10.1139/m88-062. PMID: 3138016.
17. Bruce, A.W., Chadwick, P., Hassan, A., and VanCott, G.F. 1973. Recurrent urethritis in women. Can. Med. Assoc. J. 108(8): 973-976. PMID:4633489.
18. Burton, J.P., and Reid, G. 2002. Evaluation of the bacterial vaginal flora of 20 postmenopausal women by direct (Nugent score) and molecular (polymerase chain reaction and denaturing gradient gel electrophoresis) techniques. J. Infect. Dis. 186(12): 1770-1780. doi:10.1086/345761. PMID:12447763.
19. Burton, J.P., Cadieux, P.A., and Reid, G. 2003. Improved understanding of the bacterial vaginal microbiota of women before and after probiotic instillation. Appl. Environ. Microbiol. 69: 97-101. doi:10.1128/AEM.69.1.97-101.2003. PMID:12513982.
20. Cadieux, P., Burton, J., Gardiner, G., Braunstein, I., Bruce, A.W., Kang, C.Y., and Reid, G. 2002. Lactobacillus strains and vaginal ecology. J. Am. Med. Assoc. 287: 1940-1941. doi:10.1001/jama.287.15.1940. PMID:11960535.
21. Cadieux, P., Wind, A., Sommer, P., Schaefer, L., Crowley, K., Britton, R.A., and Reid, G. 2008. Evaluation of reuterin production in urogenital probiotic Lactobacillus reuteri RC-14. Appl. Environ. Microbiol. 74(15): 4645-4649. doi:10.1128/AEM.00139-08. PMID:18539802.
22. Cook, R.L., Harris, R.J., and Reid, G. 1988. Effect of culture media and growth phase on the morphology of lactobacilli and on their ability to adhere to epithelial cells. Curr. Microbiol. 17(3): 159-166. doi:10.1007/BF01573472.
23. Dols, J.A.M., Boon, M.E., Monachese, M., Changalucha, J., Butamanya, N., Varriano, S., et al. 2011. The impact of probiotic yogurt on HIV positive women in Tanzania. Int. Dairy J. 21(8): 575-577. doi:10.1016/j.idairyj.2011.03.001.
24. Falagas, M.E., Betsi, G.I., Tokas, T., and Athanasiou, S. 2006. Probiotics for prevention of recurrent urinary tract infections in women: a review of the evidence from microbiological and clinical studies. Drugs, 66(9): 1253-1261. doi:10.2165/00003495-200666090-00007. PMID:16827601.
25. FAO/WHO. 2001. Report of the joint FAO/WHO Expert Consultation on evaluation of health and nutritional properties of probiotics in food including powder milk with live lactic acid bacteria [online]. Available from http://www.fao.org/3/aa0512e.pdf.
26. Gajer, P., Brotman, R.M., Bai, G., Sakamoto, J., Schütte, U.M., Zhong, X., et al. 2012. Temporal dynamics of the human vaginal microbiota. Sci. Transl. Med. 4(132): 132ra52. PMID: 22553250.
27. Gan, X.T., Ettinger, G., Huang, C.X., Burton, J.P., Haist, J.V., Rajapurohitam, V., et al. 2014. Probiotic administration attenuates myocardial hypertrophy and heart failure after myocardial infarction in the rat. Circ.: Heart Failure, 7(3): 491-499. doi:10.1161/CIRCHEARTFAILURE.113.000978. PMID: 24625365.
28. Gonçalves, B., Ferreira, C., Alves, C.T., Henriques, M., Azeredo, J., and Silva, S. 2016. Vulvovaginal candidiasis: epidemiology, microbiology and risk factors. Crit. Rev. Microbiol. 42(6): 905-927. doi:10.3109/1040841X.2015.1091805. PMID:26690853.
29. Guarino, A., Dupont, C., Gorelov, A.V., Gottrand, F., Lee, J.K., Lin, Z., et al. 2012. The management of acute diarrhea in children in developed and developing areas: from evidence base to clinical practice. Expert Opin. Pharmacother. 13(1): 17-26. doi:10.1517/14656566.2011.634800. PMID:22106840.
30. Guarino, A., Guandalini, S., and Lo Vecchio, A. 2015. Probiotics for prevention and treatment of diarrhea. J. Clin. Gastroenterol. 49: S37-S45. doi:10.1097/MCG.0000000000000349. PMID: 26447963.
31. Hagberg, L., Bruce, A.W., Reid, G., Svanborg Eden, C., Lincoln, K., and Lidin-Janson, G. 1989. Colonization of the urinary tract with live bacteria from the normal fecal and urethral flora in patients with recurrent symptomatic urinary tract infections. In Host-parasite interactions in urinary tract infections. Edited by E.H. Kass and C. Svanborg Eden. University of Chicago Press, Chicago, Ill., USA. pp. 194-197.
32. Hemsworth, J.C., Hekmat, S., and Reid, G. 2012. Micronutrient supplemented probiotic yogurt for HIV-infected adults taking HAART in London, Canada. Gut Microbes, 3(5): 414-419. doi:10.4161/gmic.21248. PMID:22825497.
33. Hickson, M., D’Souza, A.L., Muthu, N., Rogers, T.R., Want, S., Rajkumar, C., and Bulpitt, C.J. 2007. Use of probiotic Lactobacillus preparation to prevent diarrhoea associated with antibiotics: randomised double blind placebo controlled trial. BMJ, 335: 80. doi:10.1136/bmj.39231.599815.55. PMID:17604300.
34. Hill, C., Guarner, F., Reid, G., Gibson, G.R., Merenstein, D.J., Pot, B., et al. 2014. 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. 11(8): 506-514. PMID:24912386.
35. Ho, M., Chang, Y.Y., Chang, W.C., Lin, H.C., Wang, M.H., Lin, W.C., and Chiu, T.H. 2016. Oral Lactobacillus rhamnosus GR-1 and Lactobacillus reuteri RC-14 to reduce Group B Streptococcus colonization in pregnant women: a randomized controlled trial. Taiwan J. Obstet. Gynecol. 55(4): 515-518. doi:10.1016/j.tjog.2016.06.003. PMID:27590374.
36. Hummelen, R., Changalucha, J., Butamanya, N.L., Cook, A., Habbema, J.D.F., and Reid, G. 2010. Lactobacillus rhamnosus GR-1 and L. reuteri RC-14 to prevent or cure bacterial vaginosis among women with HIV. Int. J. Gynecol. Obstet. 111(3): 245-248. PMID:20801446.
37. Iemoli, E., Trabattoni, D., Parisotto, S., Borgonovo, L., Toscano, M., Rizzardini, G., et al. 2012. Probiotics reduce gut microbial translocation and improve adult atopic dermatitis. J. Clin. Gastroenterol. 46: S33-S40. doi:10.1097/MCG.0b013e31826a8468.PMID:22955355.
38. Irvine, S.L., Hummelen, R., Hekmat, S., Looman, C.W.N., Habbema, J.D.F., and Reid, G. 2010. Probiotic yogurt consumption is associated with an increase of CD4 count among people living with HIV/AIDS. J. Clin. Gastroenterol. 44(9): e201-e205. doi:10.1097/MCG.0b013e3181d8fba8. PMID:20463586.
39. Kang, M.S., Nkurunziza, P., Muwanika, R., Qian, G., Tang, L., Song, X., et al. 2015. Longitudinal evaluation of aflatoxin exposure in two cohorts in south-western Uganda. Food Addit. Contam., Part A, 32(8): 1322-1330. doi:10.1080/19440049.2015.1048749.
40. Kilonzo, R.M., Imungi, J.K., Muiru, W.M., Lamuka, P.O., and Njage, P.M.K. 2014. Household dietary exposure to aflatoxins from maize and maize products in Kenya. Food Addit. Contam., Part A, 31(12): 2055-2062. doi:10.1080/19440049.2014.976595.
41. Kirjavainen, P.K., Laine, R.M., Carter, D., Hammond, J.-A., and Reid, G. 2008. Expression of anti-microbial defense factors in vaginal mucosa following exposure to Lactobacillus rhamnosus GR-1. Int. J. Probiotics, 3: 99-106.
42. Köhler, G.A., Assefa, S., and Reid, G. 2012. Probiotic interference of Lactobacillus rhamnosus GR-1 and Lactobacillus reuteri RC-14 with the opportunistic fungal pathogen Candida albicans. Infect. Dis. Obstet. Gynecol. 2012: 636474. PMID:22811591.
43. Kort, R., Westerik, N., Mariela Serrano, L., Douillard, F.P., Gottstein, W., Mukisa, I.M., et al. 2015. A novel consortium of Lactobacillus rhamnosus and Streptococcus thermophilus for increased access to functional fermented foods. Microb. Cell Fact. 14: 195. doi:10.1186/s12934-015-0370-x. PMID:26643044.
44. Krauss-Silva, L., Moreira, M.E., Alves, M.B., Braga, A., Camacho, K.G., Batista, M.R., et al. 2011. A randomised controlled trial of probiotics for the prevention of spontaneous preterm delivery associated with bacterial vaginosis: preliminary results. Trials, 12: 239. doi:10.1186/1745-6215-12-239. PMID:22059409.
45. Lam, V., Su, J., Koprowski, S., Hsu, A., Tweddell, J.S., Rafiee, P., et al. 2012. Intestinal microbiota determine severity of myocardial infarction in rats. FASEB J. 26(4): 1727-1735. doi:10.1096/fj.11-197921. PMID:22247331.
46. Macklaim, J.M., Gloor, G.B., Anukam, K.C., Cribby, S., and Reid, G. 2011. At the crossroads of vaginal health and disease, the genome sequence of Lactobacillus iners AB-1. Proc. Nat. Acad. Sci. USA, 108: 4688-4695. doi:10.1073/pnas.1000086107. PMID:21059957.
47. Macklaim, J.M., Fernandes, A.D., Di Bella, J.M., Hammond, J.A., Reid, G., and Gloor, G.B. 2013. Comparative meta-RNA-seq of the vaginal microbiota and differential expression by Lactobacillus iners in health and dysbiosis. Microbiome, 1: 12. doi:10.1186/2049-2618-1-12. PMID:24450540.
48. Macklaim, J.M., Clemente, J.C., Knight, R., Gloor, G.B., and Reid, G. 2015. Changes in vaginal microbiota following antimicrobial and probiotic therapy. Microb. Ecol. Health Dis. 26: 27799. PMID:26282697.
49. Martinez, R.C., Franceschini, S.A., Patta, M.C., Quintana, S.M., Candido, R.C., Ferreira, J.C., et al. 2009a. Improved treatment of vulvovaginal candidiasis with fluconazole plus probiotic Lactobacillus rhamnosus GR-1 and Lactobacillus reuteri RC-14. Lett. Appl. Microbiol. 48(3): 269-274. doi:10.1111/j.1472-765X.2008.02477.x. PMID:19187507.
50. Martinez, R.C., Seney, S.L., Summers, K.L., Nomizo, A., De Martinis, E.C., and Reid, G. 2009b. Effect of Lactobacillus rhamnosus GR-1 and Lactobacillus reuteri RC-14 on the ability of Candida albicans to infect cells and induce inflammation. Microbiol. Immunol. 53(9): 487-495. doi:10.1111/j.1348-0421. 2009.00154.x. PMID:19703242.
51. Matsubara, V.H., Wang, Y., Bandara, H.M., Mayer, M.P., and Samaranayake, L.P. 2016. Probiotic lactobacilli inhibit early stages of Candida albicans biofilm development by reducing their growth, cell adhesion, and filamentation. Appl. Microbiol. Biotechnol. 100(14): 6415-6426. doi:10.1007/s00253-016-7527-3. PMID:27087525.
52. Maziade, P.J., Pereira, P., and Goldstein, E.J. 2015. A decade of experience in primary prevention of Clostridium difficile infection at a community hospital using the probiotic combination Lactobacillus acidophilus CL1285, Lactobacillus casei LBC80R, and Lactobacillus rhamnosus CLR2 (Bio-K+). Clin. Infect. Dis. 60: S144-S147. doi:10.1093/cid/civ178. PMID:25922400.
53. McMillan, A., Dell, M., Zellar, M.P., Cribby, S., Martz, S., Hong, E., et al. 2011. Disruption of urogenital biofilms by lactobacilli. Colloids Surf., B, 86(1): 58-64. doi:10.1016/j.colsurfb.2011.03.016.
54. McMillan, A., Rulisa, S., Sumarah, M., Macklaim, J.M., Renaud, J., Bisanz, J.E., et al. 2015. A multi-platform metabolomics approach identifies highly specific biomarkers of bacterial diversity in the vagina of pregnant and nonpregnant women. Sci. Rep. 5: 14174. doi:10.1038/srep14174. PMID:26387596.
55. Millsap, K., Reid, G., van der Mei, H.C., and Busscher, H.J. 1994. Adhesion and displacement of Enterococcus faecalis from hydrophobic and hydrophilic substrata by Lactobacillus and Streptococcus spp. as studied in a parallel plate flow chamber. Appl. Environ. Microbiol. 60: 1867-1874.
56. Morelli, L., Zonenenschain, D., Del Piano, M., and Cognein, P. 2004. Utilization of the intestinal tract as a delivery system for urogenital probiotics. J. Clin. Gastroenterol. 38: S107-S110. doi:10.1097/01.mcg.0000128938.32835.98. PMID:15220672.
57. Nduti, N., McMillan, A., Seney, S., Sumarah, M., Njeru, P., Mwaniki, M., and Reid, G. 2016. Investigating probiotic yoghurt to reduce an aflatoxin B1 among school children in eastern Kenya: preliminary study. Int. Dairy J. 63: 124-129. doi:10.1016/j.idairyj.2016.07.014.
58. Ochieng, E.Z., Lalah, J.O., and Wandiga, S.O. 2007. Analysis of heavy metals in water and surface sediment in five Rift Valley lakes in Kenya for assessment of recent increase in anthropogenic activities. Bull. Environ. Contam. Toxicol. 79(5): 570-576. doi:10.1007/s00128-007-9286-4. PMID:17943221.
59. Okonya, J.S., and Kroschel, J. 2015. A cross-sectional study of pesticide use and knowledge of smallholder potato farmers in Uganda. BioMed Res. Int. 2015: 759049. PMID:26581164.
60. Pattani, R., Palda, V.A., Hwang, S.W., and Shah, P.S. 2013. Probiotics for the prevention of antibiotic-associated diarrhea and Clostridium difficile infection among hospitalized patients: systematic review and meta-analysis. Open Med. 7(2): e56-e67. PMID:24348885.
61. Petrova, M.I., Lievens, E., Verhoeven, T.L.A., Macklaim, J.M., Gloor, G., Schols, D., et al. 2016a. The lectin-like protein 1 in Lactobacillus rhamnosus GR-1 mediates tissue-specific adherence to vaginal epithelium and inhibits urogenital pathogens. Sci. Rep. 6: 37437. doi:10.1038/srep37437. PMID:27869151.
62. Petrova, M., Reid, G., Vaneechoutte, M., and Lebeer, S. 2016b. Lactobacillus iners-Friend or foe? Trends Microbiol. In press. doi:10.1016/j.tim.2016.11.007.
63. Reid, G. 2006. Extra intestinal effects of prebiotics and probiotics. In Prebiotics: development and applications. Edited by G.R. Gibson and R.A. Rastall. John Wiley and Sons, London, UK. pp. 201-211.
64. Reid, G. 2016. Cervicovaginal microbiomes - threats and possibilities. Trends Endocrinol. Metab. 27(7): 446-454. doi:10.1016/j.tem.2016.04.004. PMID:27129670.
65. Reid, G., and Sobel, J.D. 1987. Bacterial adherence in the pathogenesis of urinary tract infection: a review. Clin. Infect. Dis. 9(3): 470-487. doi:10.1093/clinids/9.3.470. PMID:2885910.
66. Reid, G., and Tieszer, C. 1993. Preferential adhesion of bacteria from a mixed population to a urinary catheter. Cells Mater. 3: 171-176.
67. Reid, G., Chan, R.C.Y., Bruce, A.W., and Costerton, J.W. 1985. Prevention of urinary tract infection in rats with an indigenous Lactobacillus casei strain. Infect. Immun. 49(2): 320-324. PMID:3926645.
68. Reid, G., Cook, R.L., and Bruce, A.W. 1987. Examination of strains of lactobacilli for properties which may influence bacterial interference in the urinary tract. J. Urol. 138: 330-335. PMID:3599250.
69. Reid, G., McGroarty, J.A., Angotti, R., and Cook, R.L. 1988. Lactobacillus inhibitor production against Escherichia coli and coaggregation ability with uropathogens. Can. J. Microbiol. 34(3): 344-351. doi:10.1139/m88-063. PMID:3138017.
70. Reid, G., Cook, R.L., Hagberg, L., and Bruce, A.W. 1989. Lactobacilli as competitive colonizers of the urinary tract. In Host-parasite interactions in urinary tract infections. Edited by E.H. Kass and C. Svanborg Eden. University of Chicago Press, Chicago, Ill., USA. pp. 390-396.
71. Reid, G., Bruce, A.W., Cook, R.L., and Llano, M. 1990. Effect on urogenital flora of antibiotic therapy for urinary tract infection. Scand. J. Infect. Dis. 22: 43-47. doi:10.3109/00365549009023118. PMID: 2181630.
72. Reid, G., Millsap, K., and Bruce, A.W. 1994. Implantation of Lactobacillus casei var. rhamnosus into vagina. Lancet, 344: 1229. doi:10.1016/S0140-6736(94)90543-6. PMID:7934561.
73. Reid, G., Bruce, A.W., and Taylor, M. 1995a. Instillation of Lactobacillus and stimulation of indigenous organisms to prevent recurrence of urinary tract infections. Microecol. Ther. 23: 32-45.
74. Reid, G., Tieszer, C., and Lam, D. 1995b. Influence of lactobacilli on the adhesion of Staphylococcus aureus and Candida albicans to diapers. J. Ind. Microbiol. 15: 248-253. doi:10.1007/BF01569832. PMID:8519484.
75. Reid, G., Beuerman, D., Heinemann, C., and Bruce, A.W. 2001a. Probiotic Lactobacillus dose required to restore and maintain a normal vaginal flora. FEMS Immunol. Med. Microbiol. 32: 37-41. doi:10.1111/j.1574-695X.2001.tb00531.x. PMID:11750220.
76. Reid, G., Bruce, A.W., Fraser, N., Heinemann, C., Owen, J., and Henning, B. 2001b. Oral probiotics can resolve urogenital infections. FEMS Immunol. Med. Microbiol. 30: 49-52. doi:10.1111/j.1574-695X.2001.tb01549.x. PMID:11172991.
77. Reid, G., Charbonneau, D., Erb, J., Poehner, R., Gonzalez, S., Gardiner, G., and Bruce, A.W. 2002. Ability of Lactobacillus GR-1 and RC-14 to stimulate host defences and reduce gut translocation and infectivity of Salmonella typhimurium. Preventative Nutrition and Food Science, 7: 168-173. doi:10.3746/jfn.2002.7.2.168.
78. Reid, G., Charbonneau, D., Erb, J., Kochanowski, B., Beuerman, D., Poehner, R., and Bruce, A.W. 2003a. Oral use of Lactobacillus rhamnosus GR-1 and L. fermentum RC-14 significantly alters vaginal flora: randomized, placebo-controlled trial in 64 healthy women. FEMS Immunol. Med. Microbiol. 35: 131-134. doi:10.1016/S0928-8244(02)00465-0. PMID:12628548.
79. Reid, G., Jass, J., Sebulsky, M.T., and McCormick, J.K. 2003b. Potential uses of probiotics in clinical practice. Clin. Microbiol. Rev. 16(4): 658-672. doi:10.1128/CMR.16.4.658-672.2003. PMID:14557292.
80. Reid, M.K.E., Gough, R., Enos, M., and Reid, G. 2013. Social businesses in Tanzania tackling health issues of the Millenium Development Goals, one community kitchen at a time. J. Soc. Bus. 3(1): 24-38.
81. Sanders, M.E., Merenstein, D.J., Ouwehand, A.C., Reid, G., Salminen, S., Cabana, M.D., et al. 2016. Probiotic use in at-risk populations. J. Am. Pharm. Assoc. 56(6): 680-686. doi:10.1016/j.japh.2016.07.001.
82. Sawh, S.C., Deshpande, S., Jansen, S., Reynaert, C.J., and Jones, P.M. 2016. Prevention of necrotizing enterocolitis with probiotics: a systematic review and meta-analysis. PeerJ, 4: e2429. doi:10.7717/peerj.2429. PMID:27761306.
83. Schwebke, J.R., and Desmond, R.A. 2007. A randomized trial of the duration of therapy with metronidazole plus or minus azithromycin for treatment of symptomatic bacterial vaginosis. Clin. Infect. Dis. 44(2): 213-219. doi:10.1086/509577. PMID: 17173219.
84. Schwebke, J.R., and Desmond, R.A. 2011. Tinidazole vs metronidazole for the treatment of bacterial vaginosis. Am. J. Obstet. Gynecol. 204(3): 211.e1-211.e6. PMID:21167471.
85. Srinivasan, S., Morgan, M.T., Fiedler, T.L., Djukovic, D., Hoffman, N.G., Raftery, D., et al. 2015. Metabolic signatures ofbacterialvaginosis.mBio,6(2):e00204-15. doi:10.1128/mBio.00204-15.
86. Stapleton, A.E., Au-Yeung, M., Hooton, T.M., Fredricks, D.N., Roberts, P.L., Czaja, C.A., et al. 2011. Randomized, placebocontrolled phase 2 trial of a Lactobacillus crispatus probiotic given intravaginally for prevention of recurrent urinary tract infection. Clin. Infect. Dis. 52(10): 1212-1217. doi:10.1093/cid/cir183. PMID:21498386.
87. Swidsinski, A., Mendling, W., Loening-Baucke, V., Swidsinski, S., Dörffel, Y., Scholze, J., et al. 2008. An adherent Gardnerella vaginalis biofilm persists on the vaginal epithelium after standard therapy with oral metronidazole. Am. J. Obstet. Gynecol. 198(1): 97.e1-97.e6. PMID:18005928.
88. Talarico, T.L., Casas, I.A., Chung, T.C., and Dobrogosz, W.J. 1988. Production and isolation of reuterin, a growth inhibitor produced by Lactobacillus reuteri. Antimicrob. Agents Chemother. 32(12): 1854-1858. doi:10.1128/AAC.32.12.1854. PMID:3245697.
89. Tytgat, H.L., and de Vos, W.M. 2016. Sugar coating the envelope: glycoconjugates for microbe-host crosstalk. Trends Microbiol. 24(11): 853-861. doi:10.1016/j.tim.2016.06.004. PMID:27374775.
90. Tytgat, H.L., Douillard, F.P., Reunanen, J., Rasinkangas, P., Hendrickx, A.P., Laine, P.K., et al. 2016. Lactobacillus rhamnosus GG outcompetes Enterococcus faecium via mucus-binding pili: evidence for a novel and heterospecific probiotic mechanism. Appl. Environ. Microbiol. 82(19): 5756-5762. doi:10.1128/AEM.01243-16. PMID:27422834.
91. Urbaniak, C., McMillan, A., Angelini, M., Gloor, G.B., Sumarah, M., Burton, J.P., and Reid, G. 2014. Effect of chemotherapy on the microbiota and metabolome of human milk, a case report. Microbiome, 2: 24. doi:10.1186/2049-2618-2-24. PMID:25061513.
92. Urbaniak, C., Angelini, M., Gloor, G.B., and Reid, G. 2016a. Human milk microbiota profiles in relation to birthing method, gestation and infant gender. Microbiome, 4: 1. doi:10.1186/s40168-015-0145-y. PMID:26739322.
93. Urbaniak, C., Gloor, G.B., Brackstone, M., Scott, L., Tangney, M., and Reid, G. 2016b. The microbiota of breast tissue and its association with breast cancer. Appl. Environ. Microbiol. 82(16): 5039-5048. doi:10.1128/AEM.01235-16. PMID:27342554.
94. van Nood, E., Vrieze, A., Nieuwdorp, M., Fuentes, S., Zoetendal, E.G., de Vos, W.M., et al. 2013. Duodenal infusion of donor feces for recurrent Clostridium difficile. N. Engl. J. Med. 368: 407-415. doi:10.1056/NEJMoa1205037. PMID:23323867.
95. Velraeds, M.M.C., van de Belt-Gritter, B., van der Mei, H.C., Reid, G., and Busscher, H.J. 1998. Interference in initial adhesion of uropathogenic bacteria and yeasts to silicone rubber by a Lactobacillus acidophilus biosurfactant. J. Med. Microbiol. 47: 1081-1085. doi:10.1099/00222615-47-12-1081. PMID:9856644.
96. Vujic, G., Jajac Knez, A., Despot Stefanovic, V., and Kuzmic Vrbanovic, V. 2013. Efficacy of orally applied probiotic capsules for bacterial vaginosis and other vaginal infections: a double-blind, randomized, placebo-controlled study. Eur. J. Obstet. Gynecol. Reprod. Biol. 168(1): 75-79. doi:10.1016/j.ejogrb.2012.12.031. PMID:23395559.
97. Wagner, R.D., and Johnson, S.J. 2012. Probiotic Lactobacillus and estrogen effects on vaginal epithelial gene expression responses to Candida albicans. J. Biomed. Sci. 19: 58. doi:10.1186/1423-0127-19-58. PMID:22715972.
98. Yang, S., Reid, G., Challis, J.R., Kim, S.O., Gloor, G.B., and Bocking, A.D. 2015. Is there a role for probiotics in the prevention of preterm birth? Front. Immunol. 6: 62. PMID:25741339.
99. Zhou, X., Hansmann, M.A., Davis, C.C., Suzuki, H., Brown, C.J., Schütte, U., et al. 2010. The vaginal bacterial communities of Japanese women resemble those of women in other racial groups. FEMS Immunol. Med. Microbiol. 58(2): 169-181. doi: 10.1111/j.1574-695X.2009.00618.x. PMID:19912342.