Choosing an appropriate probiotic product for your patient: An evidence-based practical guide

PLoS ONE

Volumn 13, Issue 12, 2018, Pages

  Sniffen, Jason C ^a   McFarland, Lynne V ^b   Evans, Charlesnika T ^c,d   Goldstein, Ellie J C ^e  

^a FLORIDA HOSPITAL   (United States)

^b UNIVERSITY OF WASHINGTON MEDICAL CENTER   (United States)

^c NORTHWESTERN UNIVERSITY   (United States)

^d VETERANS AFFAIRS MEDICAL CENTER   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROBIOTIC AGENT;

EVIDENCE BASED MEDICINE; HUMAN; RANDOMIZED CONTROLLED TRIAL (TOPIC);

EVIDENCE-BASED MEDICINE; HUMANS; PROBIOTICS; RANDOMIZED CONTROLLED TRIALS AS TOPIC;

EID: 85059208063     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0209205     Document Type: Article

References (76)

1. Schultz M, Baranchi A, Thurston L, Yu YC, Wang L, Chen J, et al. Consumer demographics and expectations of probiotic therapy in New Zealand: results of a large telephone survey. N Z Med J. 2011; 124: 36–43.
2. Clarke TC, Black LI, Stussman BJ, Barnes PM, Nahin RL. Trends in the use of complementary health approaches among adults: United States, 2002–2012. National health statistics reports; no 79. Hyatts-ville, MD: National Center for Health Statistics. 2015. Available at: https://nccih.nih.gov/research/statistics/NHIS/2012/natural-products/biotics. Accessed June 1, 2017.
3. Draper K, Ley C, Parsonnet J. A survey of probiotic use practices among patients at a tertiary medical centre. Benef Microbes. 2017; 8(3):345–351. https://doi.org/10.3920/BM2016.0148 PMID: 28403649
4. Yi SH, Jernigan JA, McDonald LC. Prevalence of probiotic use among inpatients: A descriptive study of 145 U.S. hospitals. Am J Infect Control 2016; 44(5):548–53. https://doi.org/10.1016/j.ajic.2015.12.001PMID: 26822808
5. Grand View Research. Nutraceuticals and Functional Foods. Global Industry Report. September 2016. Available at: http://www.grandviewresearch.com/industry-analysis/probiotics-market. Accessed June 1, 2017.
6. Draper K, Ley C, Parsonnet J. Probiotic guidelines and physician practice: a cross-sectional survey and overview of the literature. Benef Microbes. 2017; 8(4):507–519. https://doi.org/10.3920/BM2016.0146PMID: 28618862
7. McFarland LV. From Yaks to Yogurt: The history, development and current use of probiotics. Clin Infect Dis. 2015; 60(S2):S85–S90. https://doi.org/10.1093/cid/civ054 PMID: 25922406
8. Higashikawa F, Noda M, Awaya T, Danshiitsoodol N, Matoba Y, Kumagai T, et al. Antiobesity effect of Pediococcus pentosaceus LP28 on overweight subjects: a randomized, double-blind, placebo-controlled clinical trial. Euro J Clin Nutr. 2016; 70(5):582–587. https://doi.org/10.1038/ejcn.2016.17 PMID: 26956126
9. Mercer MB, Brinich MA, Geller G, Harrison K, Highland J, James K, et al. How Patients View Probiotics: Findings from a Multicenter Study of Patients with Inflammatory Bowel Disease and Irritable Bowel Syndrome. J Clin Gastroenterol. 2012; 46(2):138–144. https://doi.org/10.1097/MCG.0b013e318225f545PMID: 21716123
10. Brinich MA, Mercer MB, Sharp RR. An analysis of online messages about probiotics. BMC Gastroenterol. 2013; 13:5. https://doi.org/10.1186/1471-230X-13-5 PMID: 23311418
11. Kolaček S, Hojsak I, Berni Canani R, Guarino A, Indrio F, Orel R, et al. ESPGHAN Working Group for Probiotics and Prebiotics.Commercial Probiotic Products: A Call for Improved Quality Control. A Position Paper by the ESPGHAN Working Group for Probiotics and Prebiotics. Pediatr Gastroenterol Nutr. 2017 Jul; 65(1):117–124. https://doi.org/10.1097/MPG.0000000000001603
12. Floch MH, Walker WA, Sanders ME, Nieuwdorp M, Kim AS, Brenner DA, et al. Recommendations for Probiotic Use—2015 Update: Proceedings and Consensus Opinion. J Clin Gastroenterol. 2015; 49 (Suppl 1):S69–73. https://doi.org/10.1097/MCG.0000000000000420 PMID: 26447969
13. Cruchet S, Furnes R, Maruy A, Hebel E, Palacios J, Medina F, et al. The Use of Probiotics in Pediatric Gastroenterology: A Review of the Literature and Recommendations by Latin-American Experts. Paediatr Drugs. 2015; 17(3):199–216. https://doi.org/10.1007/s40272-015-0124-6 PMID: 25799959
14. Guarino A, Guandalini S, Lo Vecchio A. Probiotics for Prevention and Treatment of diarrhea. J Clin Gastroenterol. 2015; 49(Supp 1):S37–S45. https://doi.org/10.1097/MCG.0000000000000349 PMID: 26447963
15. Szajewska H, Canani RB, Guarino A, Hojsak I, Indrio F, Kolacek S, et al. ESPGHAN Working Group for ProbioticsPrebiotics. Probiotics for the Prevention of Antibiotic-Associated Diarrhea in Children.J Pediatr Gastroenterol Nutr. 2016; 62(3):495–506. https://doi.org/10.1097/MPG.0000000000001081PMID: 26756877
16. 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. 2015; 4:1. https://doi.org/10.1186/2046-4053-4-1 PMID: 25554246
17. McFarland LV, Goh S. Preventing Pediatric Antibiotic-Associated Diarrhea and Clostridium difficile Infections with Probiotics: a meta-analysis. World J Meta-analysis. 2013; 1(3): 102–120. https://doi.org/10.13105/wjma.v1.i3.02
18. McFarland LV, Malfertheiner P, Huang Y, Wang L. Meta-analysis of single strain probiotics for the eradication of Helicobacter pylori and prevention of adverse events. World Journal of Meta-analysis. 2015; 3 (2):97–117. https://doi.org/10.13105/wjma.v3.i2.97
19. McFarland LV, Huang Y, Wang L, Malfertheiner P. Systematic review and meta-analysis: Multi-strain probiotics as adjunct therapy for Helicobacter pylori eradication and prevention of adverse events. United Euro J Gastroenterol. 2016; 4(4):546–61. https://doi.org/10.1177/205064061561735
20. McFarland LV, Evans CT, Goldstein EJC. Strain-specificity and disease-specificity of probiotic efficacy: a systematic review and meta-analysis. Frontiers in Medicine 2018: 5:124. https://doi.org/10.3389/fmed.2018.00124 PMID: 29868585
21. Higgins JPT, Green S. Cochrane handbook for systematic reviews of interventions. Version 5.1.0. The Cochrane Collaboration, 2011. Available at www.cochrane-handbook.org. Accessed June 1, 2017.
22. Hojsak I, Szajewska H, Canani RB, Guarino A, Indrio F, Kolacek S, et al. Probiotics for the Prevention of Nosocomial Diarrhea in Children. J Pediatr Gastroenterol Nutr. 2018; 66(1):3–9. https://doi.org/10.1097/MPG.0000000000001637 PMID: 28574970
23. 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. https://doi.org/10.1038/nrgastro.2014.66 PMID: 24912386
24. Miquel S, Beaumont M, Martín R, Langella P, Braesco V, Thomas M. A proposed framework for an appropriate evaluation scheme for microorganisms as novel foods with a health claim in Europe. Microb Cell Fact. 2015; 14:48. https://doi.org/10.1186/s12934-015-0229-1 PMID: 25889559
25. Smug LN, Salminen S, Sanders ME, Ebner S. Yoghurt and probiotic bacteria in dietary guidelines of the member states of the European Union. Benef Microbes. 2014; 5(1):61–6. https://doi.org/10.3920/BM2013.0050 PMID: 24463208
26. McFarland LV, Elmer GW, McFarland M. Meta-analysis of Probiotics for the Prevention and Treatment of Acute Pediatric Diarrhea. Internatl J Probiot Prebiot. 2006; 1(1):63–76.
27. Szajewska H, Mrukowicz JZ. Probiotics in the treatment and prevention of acute infectious diarrhea in infants and children: a systematic review of published randomized, double-blind, placebo-controlled trials. J Pediatr Gastroenterol Nutr. 2001; 33(Suppl 2):S17–25.
28. McFarland LV. Systematic review and meta-analysis of Saccharomyces boulardii in adult patients. World J Gastroenterol. 2010; 16(18):2202–22. https://doi.org/10.3748/wjg.v16.i18.2202 PMID: 20458757
29. Campana R, van Hemert S, Baffone W. Strain-specific probiotic properties of lactic acid bacteria and their interference with human intestinal pathogens invasion. Gut Pathol. 2017; 9(12):1–12. https://doi.org/10.1186/s13099-017-0162-4 PMID: 28286570
30. Donelli G, Vuotto C, Mastromarino P. Phenotyping and genotyping are both essential to identify and classify a probiotic microorganism. Micro Ecol Health Dis. 2013; 24:20105. https://doi.org/10.3402/mehd.v24i0.20105 PMID: 24009545
31. Hill C, Scott K, Klaenhammer TR, Quigley E, Sanders ME. Probiotic nomenclature matters. Gut Microbes. 2016; 7(1):1–2. https://doi.org/10.1080/19490976.2015.1127484 PMID: 26939847
32. Goldstein EJ, Tyrrell KL, Citron DM. Lactobacillus species: taxonomic complexity and controversial susceptibilities. Clin Infect Dis. 2015; 60(Suppl 2):S98–107. https://doi.org/10.1093/cid/civ072 PMID: 25922408
33. McFarland LV, Ozen M, Dinleyici EC, Goh S. Comparison of pediatric and adult antibiotic-associated diarrhea and Clostridium difficile infections. World J Gastroenterol. 2016; 22(11):3078–3104. https://doi.org/10.3748/wjg.v22.i11.3078 PMID: 27003987
34. Magill SS, Edwards JR, Bamberg W, Beldavs ZG, Dumyati G, Kainer MA, et al. Multistate point-prevalence survey of healthcare–associated infections. N Engl J Med. 2014; 370:1198–1208. https://doi.org/10.1056/NEJMoa1306801 PMID: 24670166
35. Evans CT, Safdar N. Current Trends in the Epidemiology and Outcomes of Clostridium difficile Infection. Clin Infect Dis. 2015; 60(Suppl 2):S66–71. https://doi.org/10.1093/cid/civ140 PMID: 25922403
36. Goldstein EJ, Johnson SJ, Maziade PJ, Evans CT, Sniffen JC, Millette M, et al. Probiotics and prevention of Clostridium difficile infection. Anaerobe. 2017; 45:114–119. https://doi.org/10.1016/j.anaerobe.2016.12.007 PMID: 27988389
37. McFarland LV. Primary prevention of Clostridium difficile infections-how difficult can it be? Expert Rev Gastroenterol Hepatol. 2017; 11(6):507–521. https://doi.org/10.1080/17474124.2017.1312343 PMID: 28347160
38. Johnson S, Maziade PJ, McFarland LV, Trick W, Donskey C, Currie B, et al. Is primary prevention of Clostridium difficile infection possible with specific probiotics? Int J Infect Dis. 2012; 16(11):e786–92. https://doi.org/10.1016/j.ijid.2012.06.005 PMID: 22863358
39. McFarland LV. An observation on inappropriate probiotic sub-group classifications in the meta-analysis by Lau and Chamberlain. Inter J Gen Med. 2016; 9:333–336. https://doi.org/10.2147/IJGM.S119970PMID: 27757047
40. Gao XW, Mubasher M, Fang CY, Reifer C, Miller LE. Dose-Response Efficacy of a Proprietary Probiotic Formula of Lactobacillus acidophilus CL1285 and Lactobacillus casei LBC80R for Antibiotic-Associated Diarrhea and Clostridium difficile-Associated Diarrhea Prophylaxis in Adult Patients. Am J Gastroenterol. 2010; 105(7):1636–41. https://doi.org/10.1038/ajg.2010.11 PMID: 20145608
41. Maziade PJ, Pereira P, Goldstein EJC. A decade of experience in primary prevention of C. difficile infection at a community hospital using the probiotic combination L. acidophilus CL1285, L. casei LBC80R and L. rhamnosus CLR2 (BioK+). Clin Infect Dis. 2015; 60(Suppl 2): S144–147. https://doi.org/10.1093/cid/civ178 PMID: 25922400
42. McFarland LV, Ship N, Auclair J, Millette M. Primary prevention of Clostridium difficile infections with a specific probiotic combining Lactobacillus acidophilus, L. casei, and L. rhamnosus strains: assessing the evidence. J Hosp Infect. 2018; 99(4):443–452. https://doi.org/10.1016/j.jhin.2018.04.017 PMID: 29702133
43. Trick WE, Sokalski SJ, Johnson S, Bunnell KL, Levato J, Ray MJ, et al. Effectiveness of Probiotic for Primary Prevention of Clostridium difficile Infection: A Single-Center Before-and-After Quality Improvement Intervention at a Tertiary-Care Medical Center. Infect Control Hosp Epidemiol. 2018; 39(7):765–770. https://doi.org/10.1017/ice.2018.76 PMID: 29695310
44. Wang J, Kortsalioudaki C, Heath PT, Buttery J, Clarke P, Gkentzi D, et al. Epidemiology and healthcare factors associated with neonatal enterococcal infections. Arch Dis Child Fetal Neonatal Ed. 2018 Nov 13. pii: fetalneonatal-2018-315387. https://doi.org/10.1136/archdischild-2018-315387 PMID: 30425112
45. Deshpande G, Jape G, Rao S, Patole S. Benefits of probiotics in preterm neonates in low-income and medium-income countries: a systematic review of randomised controlled trials. BMJ Open. 2017 Dec 7; 7(12):e017638. https://doi.org/10.1136/bmjopen-2017-017638 PMID: 29222137
46. Dermyshi E, Wang Y, Yan C, Hong W, Qiu G, Gong X, et al. The "golden age" of probiotics: A systematic review and meta-analysis of randomized and observational studies in preterm infants. Neonatology. 2017; 112: 9–23. https://doi.org/10.1159/000454668 PMID: 28196365
47. McFarland LV. Meta-analysis of probiotics for the prevention of traveler’s diarrhea. Travel Medicine and Infectious Diseases. 2007; 5(2):97–105. https://doi.org/10.1016/j.tmaid.2005.10.003 PMID: 17298915
48. Grandy G, Medina M, Soria R, Terán CG, Araya M. Probiotics in the treatment of acute rotavirus diarrhoea. A randomized, double-blind, controlled trial using two different probiotic preparations in Bolivian children. BMC Infect Dis. 2010; 10:253. https://doi.org/10.1186/1471-2334-10-253 PMID: 20735858
49. Feizizadeh S, Salehi-Abargouei A, Akbari V. Efficacy and safety of Saccharomyces boulardii for acute diarrhea. Pediatrics. 2014; 134:e176–e191. https://doi.org/10.1542/peds.2013-3950 PMID: 24958586
50. Szajewska H, Ruszczyński M, Kolaček S. Meta-analysis shows limited evidence for using Lactobacillus acidophilus LB to treat acute gastroenteritis in children. Acta Paediatr. 2014; 103(3):249–55. https://doi.org/10.1111/apa.12487 PMID: 24175943
51. Urbancsek H, Kazar T, Mezes I, Neumann K. Results of a double-blind, randomized study to evaluate the efficacy and safety of Antibiophilus in patients with radiation-induced diarrhoea. Eur J Gastroenterol Hepatol. 2001; 13: 391–6. PMID: 11338068
52. McFarland LV, Surawicz CM, Greenberg RN, Fekety R, Elmer GW, Moyer KA, et al. A randomized placebo-controlled trial of Saccharomyces boulardii in combination with standard antibiotics for Clostridium difficile disease. J Amer Med Asso. 1994; 271(24): 1913–1918.
53. Surawicz CM, McFarland LV, Greenberg RN, Rubin M, Fekety R, Mulligan ME, et al. The search for a better treatment for recurrent Clostridium difficile disease: the use of high dose vancomycin combined with Saccharomyces boulardii. Clin Infect Dis. 2000; 31:1012–1017. https://doi.org/10.1086/318130PMID: 11049785
54. Pochapin M. The effect of probiotics on Clostridium difficile diarrhea. Am J Gastroenterol. 2000; 95 (S1): S11–13.
55. Lawrence SJ, Korzenik JR, Mundy LM. Probiotics for recurrent Clostridium difficile disease. J Med Microbiol. 2005; 54:905–6. https://doi.org/10.1099/jmm.0.46096-0 PMID: 16091446
56. Millette M, Nguyen A, Amine KM, Lacroix M. Gastrointestinal survival of bacteria in commercial probiotic products. Intern J Prob Preb. 2013; 8(4):149–156.
57. Goldenberg JZ, Lytvyn L, Steurich J, Parkin P, Mahant S, Johnston BC. Probiotics for the prevention of pediatric antibiotic-associated diarrhea. Cochrane Database of Systematic Reviews. 2015; (12): CD004827. https://doi.org/10.1002/14651858.CD004827.pub4 PMID: 26695080
58. Ouwehand AC. A review of dose-responses of probiotics in human studies. Benef Microbes. 2017; 8 (2):143–151. https://doi.org/10.3920/BM2016.0140 PMID: 28008787
59. Patrone V, Molinari P, Morelli L. Microbiological and molecular characterization of commercially available probiotics containing Bacillus clausii from India and Pakistan. Int J Food Microbiol. 2016; 237: 92–97. https://doi.org/10.1016/j.ijfoodmicro.2016.08.012 PMID: 27543819
60. Chen T, Wu Q, Li S, Xiong S, Jiang S, Tan Q, et al. Microbiological quality and characteristics of probiotic products in China. J Sci Food Agric. 2014; 94(1):131–8. https://doi.org/10.1002/jsfa.6221 PMID: 23653326
61. Toscano M, de Vecchi E, Rodighiero V, Drago L. Microbiological and genetic identification of some probiotics proposed for medical use in 2011. J Chemother. 2013; 25(3):156–61. https://doi.org/10.1179/1973947812Y.0000000068 PMID: 23783140
62. Goldstein EJC, Citron DM, Claros MC, Tyrrell KL. Bacterial counts from five over-the-counter probiotics: are you getting what you paid for? Anaerobe. 2014; 25:1–254. https://doi.org/10.1016/j.anaerobe.2013.10.005 PMID: 24184290
63. Sanders ME, Klaenhammer TR, Ouwehand AC, Pot B, Johansen E, Heimbach JT, et al. Effects of genetic, processing, or product formulation changes on efficacy and safety of probiotics. Ann N Y Acad Sci. 2014; 1309:1–18. https://doi.org/10.1111/nyas.12363 PMID: 24571253
64. Grzeskowiac L, Isolauri I, Salminen S, Gueimonde M. Manufacturing process influences properties of probiotic bacteria. Brit J Nutr. 2011; 105:887–894. https://doi.org/10.1017/S0007114510004496 PMID: 21059281
65. Vanhee LM, Goemé F, Nelis HJ, Coenye T. Quality control of fifteen probiotic products containing Saccharomyces boulardii. J Appl Microbiol. 2010; 109(5):1745–52. https://doi.org/10.1111/j.1365-2672.2010.04805.x PMID: 20636342
66. Auclair J, Frappier M, Millette M. Lactobacillus acidophilus CL1285, L. casei LBC80R and L. rhamnosus CLR2 (Bio-K+): characterization, manufacture, mechanisms of action and quality control of a specific probiotic combination for primary prevention of Clostridium difficile infections. Clin Infect Dis. 2015; 60 (Suppl 2):S135–144. https://doi.org/10.1093/cid/civ179 PMID: 25922399
67. Bafeta A, Koh M, Riveros C, Ravaud P. Harms Reporting in Randomized Controlled Trials of Interventions Aimed at Modifying Microbiota: A Systematic Review. Ann Intern Med. 2018 Aug 21; 169(4):240–247. https://doi.org/10.7326/M18-0343 PMID: 30014150
68. Doron S, Snydman DR. Risk and Safety of probiotics. Clin Infect Dis 2015; 60(Supple 2): S129–S134. https://doi.org/10.1093/cid/civ085 PMID: 25922398
69. Esaiassen E, Cavanagh P, Hjerde E, Simonsen GS, Støen R, Klingenberg C. Bifidobacterium longum Subspecies infantis Bacteremia in 3 Extremely Preterm Infants Receiving Probiotics. Emerg Infect Dis. 2016; 22(9):1664–6. https://doi.org/10.3201/eid2209.160033 PMID: 27532215
70. Shane AL, Mody RK, Crump JA, Tarr PI, Steiner TS, Kotloff K, et al. 2017 Infectious Diseases Society of America Clinical Practice Guidelines for the Diagnosis and Management of Infectious Diarrhea. Clin Infect Dis. 2017; 65(12):1963–1973. https://doi.org/10.1093/cid/cix959 PMID: 29194529
71. Hungin APS, Mulligan C, Pot B, Whorwell P, Agreus L, Fracasso P., et al. Systematic review: probiotics in the management of lower gastrointestinal symptoms in clinical practice- an evidence-based international guide. Aliment Pharmacol Therapeutics 2013; 38:864–886.
72. Glanville J, King S, Guarner F, Hill C, Sanders ME. A review of the systematic review process and its applicability for use in evaluating evidence for health claims on probiotic foods in the European Union. Nutr Jour. 2015; 14:16–24. https://doi.org/10.1186/s12937-015-0004-5 PMID: 25889449
73. Guarner F, Khan AG, Garisch J, Eliakim R, Gangl A, Thomson A, et al. World Gastroenterology Organi-sation Global Guidelines: probiotics and prebiotics October 2011. J Clin Gastroenterol. 2012; 46 (6):468–81. https://doi.org/10.1097/MCG.0b013e3182549092 PMID: 22688142
74. Tappenden K. Probiotics are not a one-species-fits-all proposition. Editorial. J Parenteral Enteral Nutr 2012; 36(5):496. https://doi.org/10.1177/0148607112458407 PMID: 22899485
75. Szajewska H. Pooling data on different probiotics is not appropriate to assess the efficacy of probiotics. Eur J Pediatr. 2014; 173(7):975. https://doi.org/10.1007/s00431-014-2340-4 PMID: 24849615
76. Zhao M, Shen C, Ma L. Treatment efficacy of probiotics on atopic dermatitis, zooming in on infants: a systematic review and meta-analysis. Internatl J Dermatology 2018; 57:635–641.