Are probiotics and prebiotics effective in the prevention of travellers’ diarrhea: A systematic review and meta-analysis

Travel Medicine and Infectious Disease

Volumn 27, Issue , 2019, Pages 11-19

  McFarland, Lynne V ^a   Goh, Shan ^b  

^a UNIVERSITY OF WASHINGTON   (United States)

^b UNIVERSITY OF HERTFORDSHIRE   (United Kingdom)

Author keywords

E coli; Lactobacillus; Prebiotics; Saccharomyces; Travel

Indexed keywords

PREBIOTIC AGENT; PROBIOTIC AGENT; ANTIINFECTIVE AGENT;

ANTIBIOTIC PROPHYLAXIS; ARTICLE; DRUG EFFICACY; DRUG SAFETY; HUMAN; LACTOBACILLUS ACIDOPHILUS; META ANALYSIS; NONHUMAN; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL (TOPIC); SACCHAROMYCES BOULARDII; SYSTEMATIC REVIEW; TRAVEL; TRAVELLER DIARRHEA; DIARRHEA; FACTUAL DATABASE; INCIDENCE; LACTOBACILLUS; MICROBIOLOGY; SOLDIER; TRAVEL RELATED DISEASE;

ANTI-BACTERIAL AGENTS; DATABASES, FACTUAL; DIARRHEA; HUMANS; INCIDENCE; LACTOBACILLUS; MILITARY PERSONNEL; PREBIOTICS; PROBIOTICS; RANDOMIZED CONTROLLED TRIALS AS TOPIC; SACCHAROMYCES BOULARDII; TRAVEL; TRAVEL-RELATED ILLNESS;

EID: 85054136765     PISSN: 14778939     EISSN: 18730442     Source Type: Journal    
DOI: 10.1016/j.tmaid.2018.09.007     Document Type: Article

References (67)

1. Paredes-Paredes, M., Flores-Figueroa, J., Dupont, H.L., Advances in the treatment of travellers’ diarrhea. Curr Gastroenterol Rep 13:5 (2011), 402–407, 10.1007/s11894-011-0208-6.
2. Giddings, S.L., Stevens, A.M., Leung, D.T., Travellers’ diarrhea. Med Clin 100:2 (2016), 317–330, 10.1016/j.mcna.2015.08.017.
3. Siikamaki, H., Kivela, P., Fotopoulos, M., Kantele, A., A closer look at travellers’ infections abroad: Finnish nationwide data with incidences, 2010 to 2012. Trav Med Infect Dis 15 (2017), 29–36.
4. Angelo, K.M., Kozarsky, P.E., Ryan, E.T., Chen, L.H., Sotir, M.J., What proportion of international travellers acquire a travel-related illness? A review of the literature. J Trav Med, 24(5), 2017, 10.1093/jtm/tax046.
5. Kuenzli, E., Jergensen, D., Kling, K., Jaeger, V.K., DeCrom, S., Steffen, R., et al. Previous exposure in a high-risk area for travellers’ diarrhoea within the past year is associated with a significant protective effect for travellers’ diarrhoea: a prospective observational cohort study in travellers to South Asia. Inter Soc Trav Med 24:5 (2017), 1–6, 10.1093/jtm/tax056.
6. Steffen, R., Hill, D.R., DuPont, H.L., Travellers’ diarrhea: a clinical review. J Am Med Assoc 313:1 (2015), 71–80, 10.1001/jama.2014.17006.
7. Chen, L.H., Leder, K., Barbre, K.A., Schlagenhauf, P., Libman, M., Keystone, J., et al. Business travel-associated illness: a GeoSentinel analysis. J Trav Med 25:1 (2018), 1–10, 10.1093/jtm/tax097.
8. Schwille-Kiuntke, J., Mazurak, N., Enck, P., Systematic review with meta-analysis: post-infectious irritable bowel syndrome after travellers’ diarrhoea. Aliment Pharmacol Ther 41:11 (2015), 1029–1037, 10.1111/apt.13199.
9. Zaidi, D., Wine, E., An update on travellers’ diarrhea. Curr Opin Gastroenterol 31:1 (2015), 7–13, 10.1097/MOG.0000000000000133.
10. Pitzurra, R., Steffen, R., Tschopp, A., Mutsch, M., Diarrhoea in a large prospective cohort of European travellers to resource-limited destinations. BMC Infect Dis, 10, 2010, 231, 10.1186/1471-2334-10-231.
11. Lääveri, T., Sterne, J., Rombo, L., Kantele, A., Systematic review of loperamide: No proof of antibiotics being superior to loperamide in treatment of mild/moderate travellers’ diarrhoea. Trav Med Infect Dis 14:4 (2016), 299–312, 10.1016/j.tmaid.2016.06.006.
12. Riddle, M.S., Connor, B.A., Beeching, N.J., DuPont, H.L., Hamer, D.H., Kozarsky, P., et al. Guidelines for the prevention and treatment of travellers’ diarrhea: a graded expert panel report. J Trav Med 24:suppl_1 (2017), S57–S74, 10.1093/jtm/tax026.
13. Steffen, R., Tornieporth, N., Clemens, S.A., Chatterjee, S., Cavalcanti, A.M., Collard, F., et al. Epidemiology of travellers’ diarrhea: details of a global survey. J Trav Med 11:4 (2004), 231–237.
14. Lalani, T., Maguire, J.D., Grant, E.M., Fraser, J., Ganesan, A., Johnson, M.D., et al. Epidemiology and self-treatment of travellers’ diarrhea in a large, prospective cohort of department of defense beneficiaries. J Trav Med 22:3 (2015), 152–160, 10.1111/jtm.12179.
15. Evans, D.P., Non-pharmocotherapeutic interventions in travellers diarrhea (TD). Inter Soc Travel Med 25:S1 (2018), S38–S45.
16. Vilkman, K., Lääveri, T., Pakkanen, S.H., Kantele, A., Stand-by antibiotics encourage unwarranted use of antibiotics for travellers’ diarrhea: a prospective study. Trav Med Infect Dis, 2018, 10.1016/j.tmaid.2018.06.007 in press.
17. McDonald, L.C., Effects of short- and long-course antibiotics on the lower intestinal microbiome as they relate to traveller's diarrhea. J Trav Med 24:suppl_1 (2017), S35–S38, 10.1093/jtm/taw084.
18. DuPont, H.L., Steffen, R., Use of antimicrobial agents for treatment and prevention of travellers’ diarrhoea in the face of enhanced risk of transient fecal carriage of multi-drug resistant enterobacteriaceae: setting the stage for consensus recommendations. J Trav Med 24:suppl_1 (2017), S57–S62, 10.1093/jtm/tax040.
19. Kantele, A., Mero, S., Kirveskari, J., Lääveri, T., Fluoroquinolone antibiotic users select fluoroquinolone-resistant ESBL-producing Enterobacteriaceae (ESBL-PE) - data of a prospective traveller study. Trav Med Infect Dis 16 (2017), 23–30, 10.1016/j.tmaid.2017.01.003.
20. Kantele, A., Lääveri, T., Mero, S., Vilkman, K., Pakkanen, S.H., Ollgren, J., et al. Antimicrobials increase travellers’ risk of colonization by extended-spectrum betalactamase-producing Enterobacteriaceae. Clin Infect Dis 60:6 (2015), 837–846, 10.1093/cid/ciu957.
21. McFarland, L.V., Use of probiotics to correct dysbiosis of normal microbiota following disease or disruptive events: a systematic review. BMJ Open, 4(8), 2014, e005047, 10.1136/bmjopen-2014-005047.
22. Connor, B.A., Rogova, M., Whyte, O., Use of a multiplex DNA extraction PCR in the identification of pathogens in travellers’ diarrhea. J Trav Med 25:1 (2018), 1–6, 10.1093/jtm/tax087.
23. Karl, J.P., Margolis, L.M., Madslien, E.H., Murphy, N.E., Castellani, J.W., Gundersen, Y., et al. Changes in intestinal microbiota composition and metabolism coincide with increased intestinal permeability in young adults under prolonged physiological stress. Am J Physiol Gastrointest Liver Physiol 312:6 (2017), G559–G571, 10.1152/ajpgi.00066.2017.
24. Rasko, D.A., Changes in microbiome during and after travellers’ diarrhea: what we know and what we do not. J Trav Med 24:suppl_1 (2017), S52–S56, 10.1093/jtm/tax017.
25. Riddle, M.S., Connor, B.A., The traveling microbiome. Curr Infect Dis Rep, 18(9), 2016, 29, 10.1007/s11908-016-0536-7.
26. Jakobsson, H.E., Jernberg, C., Andersson, A.F., Sjölund-Karlsson, M., Jansson, J.K., Engstrand, L., Short-term antibiotic treatment has differing long-term impacts on the human throat and gut microbiome. PloS One, 5(3), 2010, e9836, 10.1371/journal.pone.0009836.
27. Pitz, A.M., Park, G.W., Lee, D., Boissy, Y.L., Vinjé J., Antimicrobial activity of bismuth subsalicylate on Clostridium difficile, Escherichia coli O157:H7, norovirus, and other common enteric pathogens. Gut Microb 6:2 (2015), 93–100, 10.1080/19490976.2015.1008336.
28. DuPont, H.L., Ericsson, C.D., Farthing, M.J., Gorbach, S., Pickering, L.K., Rombo, L., et al. Expert review of the evidence base for prevention of travellers’ diarrhea. J Trav Med 16:3 (2009), 149–160, 10.1111/j.1708-8305.2008.00299.x.
29. Linares, D.M., Ross, P., Stanton, C., Beneficial microbes: the pharmacy in the gut. Bioengineered 7:1 (2016), 11–20.
30. McFarland, L.V., From Yaks to Yogurt: the history, development and current use of probiotics. Clin Infect Dis 60:S2 (2015), S85–S90, 10.1093/cid/civ054.
31. Roussel, C., Sivignon, A., de Vallée, A., Garrait, G., Denis, S., Tsilia, V., et al. Anti-infectious properties of the probiotic Saccharomyces cerevisiae CNCM I-3856 on enterotoxigenic E. coli (ETEC) strain H10407. Appl Microbiol Biotechnol 102:14 (2018), 6175–6189, 10.1007/s00253-018-9053-y.
32. Patel, R., DuPont, H.L., New approaches for bacteriotherapy: prebiotics, new-generation probiotics and synbiotics. Clin Infect Dis 60:Suppl 2 (2015), S108–S122.
33. Koo, H.L., DuPont, H.L., Current and future developments in travellers’ diarrhea therapy. Expert Rev Anti Infect Ther 4:3 (2006), 417–427.
34. Takahashi, O., Noguchi, Y., Tokuda, Y., Omata, F., Fukui, T., Prevention of travellers’ diarrhea with probiotics. J Clin Gastroenterol, 43(2), 2009, 198.
35. Ritchie, M.L., Romanuk, T.N., A meta-analysis of probiotic efficacy for gastrointestinal diseases. PloS One, 7(4), 2012, e34938, 10.1371/journal.pone.0034938.
36. McFarland, L.V., Meta-analysis of probiotics for the prevention of travellers’ diarrhea. Trav Med Infect Dis 5:2 (2007), 97–105, 10.1016/j.tmaid.2005.10.003.
37. McFarland, L.V., Evans, C.T., Goldstein, E.J.C., Strain-specificity and disease-specificity of probiotic efficacy: a systematic review and meta-analysis. Front Med 5:article 124 (2018), 1–14, 10.3389/fmed.2018.00124.
38. Guarner, F., Khan, A.G., Garisch, J., Eliakim, R., Gangl, A., Thomson, A., et al. World gastroenterology organisation global guidelines: probiotics and prebiotics october 2011. J Clin Gastroenterol 46:6 (2012), 468–481, 10.1097/MCG.0b013e3182549092.
39. Szajewska, H., Pooling data on different probiotics is not appropriate to assess the efficacy of probiotics. Eur J Pediatr, 173(7), 2014, 975, 10.1007/s00431-014-2340-4.
40. Hill, C., Guarner, F., Reid, G., Gibson, G.R., Merenstein, D.J., 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 11:8 (2014), 506–514, 10.1038/nrgastro.2014.66.
41. McFarland, L.V., Goh, S., Preventing pediatric antibiotic-associated diarrhea and Clostridium difficile infections with probiotics: a meta-analysis. World J Meta-analysis 1:3 (2013), 102–120, 10.13105/wjma.v1.i3. 02.
42. Liberati, A., Altman, D.G., Tetzlaff, J., Mulrow, C., Gotzsche, P.C., Ioannidis, J.P., et al. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate healthcare interventions: explanation and elaboration. Br Med J, 339, 2009, b2700, 10.1016/j.jclinepi.2009.06.006.
43. Der Simonian, R., Laird, N., Meta-analysis in clinical trials. Contr Clin Trials 7:3 (1986), 177–188.
44. Ioannidis, J.P., Interpretation of tests of heterogeneity and bias in meta-analysis. J Eval Clin Pract 14:5 (2008), 951–957.
45. Higgins, J.P.T., Green, S., (eds.) Cochrane handbook for systematic reviews of interventions. Version 5.1.0 [updated March 2011]. The Cochrane Collaboration, 2011 Available from: www.cochrane-handbook.org. (Accessed 1 January 2018)
46. Kollaritsch, H., Kremsner, P., Wiedermann, G., Scheiner, O., Prevention of traveller's diarrhea: comparison of different non-antibiotic preparations. Trav Med Interl 7 (1989), 9–18.
47. Kollaritsch, H., Holst, H., Grobara, P., Wiedermann, G., Prophylaxe der reisediarrhoe mit Saccharomyces boulardii. Prevention of travellers’ diarrhea with Saccharomyces boulardii. Results of a placebo controlled double-blind study. Fortschr Med 111:9 (1993), 152–156.
48. Katelaris, P., Salam, I., Farthing, M.J.G., Lactobacilli to prevent travellers’ diarrhea. N Engl J Med 333 (1995), 1360–1361.
49. Oksanen, P.J., Salminen, S., Saxelin, M., Hamalainen, P., Ihantola-Vormisto, A., Muurasniemi-Isoviita, L., et al. Prevention of travellers’ diarrhoea by Lactobacillus GG. Ann Med 22:1 (1990), 53–56.
50. Hilton, E., Kolakowski, P., Singer, C., Smith, M., Efficacy of Lactobacillus GG as a diarrheal preventive in travellers. J Trav Med 4:1 (1997), 41–43.
51. Briand, V., Buffet, P., Genty, S., Lacombe, K., Godineau, N., Salomon, J., et al. Absence of efficacy of nonviable Lactobacillus acidophilus for the prevention of travellers’ diarrhea: a randomized, double-blind, controlled study. Clin Infect Dis 43:9 (2006), 1170–1175.
52. De-dios-Pozo-Olano, J., Warram, J.H. Jr., G'omez, R.G., Cavazos, M.G., Effect of a lactobacilli preparation on travellers’ diarrhea. A randomized, double blind clinical trial. Gastroenterol 74 (1978), 829–830.
53. Black, F.T., Anderson, P.L., Orskov, J., Gaarslev, K., Laulund, S., Prophylactic efficacy of Lactobacilli on traveller's diarrhea. Travel Med 7 (1989), 333–335.
54. Virk, A., Mandrekar, J., Berbari, E.F., Boyce, T.G., Fischer, P.R., Kasten, M.J., et al. A randomized, double blind, placebo-controlled trial of an oral synbiotic (AKSB) for prevention of travellers’ diarrhea. J Trav Med 20:2 (2013), 88–94, 10.1111/jtm.12008.
55. Cummings, J.H., Christie, S., Cole, T.J., A study of fructo oligosaccharides in the prevention of travellers’ diarrhoea. Aliment Pharmacol Ther 15:8 (2001), 1139–1145.
56. Drakoularakou, A., Tzortzis, G., Rastall, R.A., Gibson, G.R., A double-blind, placebo-controlled, randomized human study assessing the capacity of a novel galacto-oligosaccharide mixture in reducing travellers’ diarrhea. Eur J Clin Nutr 64:2 (2010), 146–152, 10.1038/ejcn.2009.120.
57. Krokowicz, L., Kaczmarek, B.F., Krokowicz, P., Stojcev, Z., Mackiewicz, J., Walkowiak, J., et al. Sodium butyrate and short chain fatty acids in prevention of travellers’ diarrhoea: a randomized prospective study. Trav Med Infect Dis 12:2 (2014), 183–188, 10.1016/j.tmaid.2013.08.008.
58. Schindler, V.A., Jaeger, V.K., Held, L., Hatz, C., Buhler, S., Travel style is a major risk factor for diarrhoea in India: a prospective cohort study. Clin Microbiol Infect, 21, 2015 676.e1-676.e4.
59. Reuland, E.A., Sonder, G.J.B., Stolte, I., Naiemi, N., Koek, A., Linde, G.B., et al. Travel to Asia and traveller's diarrhoea with antibiotic treatment are independent risk factors for acquiring ciprofloxacin-resistant and extended spectrum B-lactamase-producing Enterobacteriaceae-a prospective cohort study. Clin Microbiol Infect, 22, 2016 731.e1-731.e7.
60. McFarland, L.V., Systematic review and meta-analysis of Saccharomyces boulardii in adult patients. World J Gastroenterol 16:18 (2010), 2202–2222, 10.3748/wjg.v16.i18.2202.
61. Moher, D., Shamseer, L., Clarke, M., Ghersi, D., Liberati, A., Petticrew, M., et al. Preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P) 2015 statement. Syst Rev, 4, 2015, 1, 10.1186/2046-4053-4-1.
62. Clements, M.L., Levine, M.M., Black, R.E., Robins-Browne, R.M., Cisneros, L.A., Drusano, G.L., et al. Lactobacillus prophylaxis for diarrhea due to enterotoxigenic Escherichia coli. Antimicrob Agents Chemother 20 (1981), 104–108.
63. Bruns, R., Raedsch, R., Therapy of traveller's diarrhea. Med Welt 46 (1995), 591–596.
64. Kirchhelle, A., Frühwein, N., Tobüren, D., Treatment of persistent diarrhea with S. boulardii in returning travellers. Results of a prospective study. Fortschr Med 114:11 (1996), 136–140.
65. Bruggencate, S.J.M.T., Girard, S.A., Floris-Vollenbroek, E.G.M., Bhardwaj, R., Tompkins, T.A., The effect of a multi-strain probiotic on the resistance toward E. coli challenge in a randomized, placebo-controlled double-blind intervention study. Eur J Clin Nutr 69 (2015), 385–391, 10.1038/ejcn.2014.238.
66. Cottrell, J., Koenig, K., Perfekt, R., Hofmann, R., Loperamide–Simethicone Acute Diarrhoea Study Team, Comparison of two forms of loperamide-simeticone and a probiotic yeast (Saccharomyces boulardii) in the treatment of acute diarrhoea in adults: a randomised non-inferiority clinical trial. Drugs R 15:4 (2015), 363–373, 10.1007/s40268-015-0111-y.
67. McFarland, L.V., Ozen, M., Dinleyici, E.C., Goh, S., Comparison of pediatric and adult antibiotic-associated diarrhea and Clostridium difficile infections. World J Gastroenterol 22:11 (2016), 3078–3104, 10.3748/wjg.v22.i11.3078.