A Systematic Review and Meta-Analysis: The Effectiveness of Probiotics for Viral Gastroenteritis

Author(s): Fereshteh Ansari, Fariba Pashazadeh, Elaheh Nourollahi, Sakineh Hajebrahimi, Zachary Munn, Hadi Pourjafar*

Journal Name: Current Pharmaceutical Biotechnology

Volume 21 , Issue 11 , 2020


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Abstract:

Background: Probiotics can be used for the treatment of viral gastroenteritis.

Objective: This systematic review is to evaluate the evidence regarding the effect of probiotics on human cases of viral gastroenteritis.

Methods: The objective of this review is to evaluate the effectiveness of probiotics against placebo or standard treatment for viral gastroenteritis. A comprehensive search of Cochrane Library, EMBASE, MEDLINE via PubMed and Ovid databases, and unpublished studies (till 27 January 2018) was conducted followed by a process of study selection and critical appraisal by two independent reviewers. Randomized controlled trials assessing probiotic administration in human subjects infected with any species of gastroenteritis viruses were considered for inclusion. Only studies with a confirmed viral cause of infection were included. This study was developed using the JBI methodology for systematic reviews, which is in accordance with the PRISMA guideline. Meta-analysis was conducted where feasible. Data were pooled using the inverse variance method with random effects models and expressed as Mean Differences (MDs) with 95% Confidence Intervals (CIs). Heterogeneity was assessed by Cochran Q statistic and quantified by the I2 statistic. We included 17 RCTs, containing 3,082 patients.

Results: Probiotics can improve symptoms of viral gastroenteritis, including the duration of diarrhea (mean difference 0.7 days, 95% CI 0.31 to 1.09 days, n = 740, ten trials) and duration of hospitalization (mean difference 0.76 days, 95% CI 0.61 to 0.92 days, n = 329, four trials).

Conclusion: The results of this review show that the administration of probiotics in patients with viral gastroenteritis should be considered.

Keywords: Viral gastroenteritis, probiotics, prebiotics, diarrhea, gastritis, enteric infections, virus shedding.

[1]
Wiener, C.; Fauci, A.S.; Braunwald, E.; Kasper, D.L.; Hauser, S.L.; Longo, D.L.; Jameson, J.L.; Loscalzo, J. Harrison’s principles of internal medicine, self-assessment and board review; McGraw Hill Professional, 2008.
[2]
Malik, Y.S.; Verma, A.K.; Kumar, N.; Touil, N.; Karthik, K.; Tiwari, R.; Bora, D.P.; Dhama, K.; Ghosh, S.; Hemida, M.G.; Abdel-Moneim, A.S.; Bányai, K.; Vlasova, A.N.; Kobayashi, N.; Singh, R.K. Advances in diagnostic approaches for viral etiologies of diarrhea: From the lab to the field. Front. Microbiol., 2019, 10, 1957.
[http://dx.doi.org/10.3389/fmicb.2019.01957] [PMID: 31608017]
[3]
Mokomane, M.; Kasvosve, I.; de Melo, E.; Pernica, J.M.; Goldfarb, D.M. The global problem of childhood diarrhoeal diseases: Emerging strategies in prevention and management. Ther. Adv. Infect. Dis. 2018, 2, 5(1), 29-43.
[http://dx.doi.org/10.1177/2049936117744429]
[4]
Chow, C.M.; Leung, A.K.; Hon, K.L. Acute gastroenteritis: from guidelines to real life. Clin. Exp. Gastroenterol., 2010, 3, 97-112.
[http://dx.doi.org/10.2147/CEG.S6554] [PMID: 21694853]
[5]
Ansaldi, F. Gastroenteritis Burden in the Adult Community: Prospects for Vaccines. In: Adult Vaccinations; Michel, JP.; Maggi, S., Eds.; Practical Issues in Geriatrics. Springer , 2019.
[6]
Dennehy, P.H. Viral gastroenteritis in children. Pediatr. Infect. Dis. J., 2011, 30(1), 63-64.
[http://dx.doi.org/10.1097/INF.0b013e3182059102] [PMID: 21173676]
[7]
Eckardt, A.J.; Baumgart, D.C. Viral gastroenteritis in adults. Recent Pat. Antiinfect. Drug Discov., 2011, 6(1), 54-63.
[http://dx.doi.org/10.2174/157489111794407877] [PMID: 21210762]
[8]
Vu, D.L.; Bosch, A.; Pintó, R.M.; Guix, S. Epidemiology of classic and novel human astrovirus: gastroenteritis and beyond. Viruses, 2017, 9(2), 33.
[http://dx.doi.org/10.3390/v9020033] [PMID: 28218712]
[9]
Freedman, S.B.; Pasichnyk, D.; Black, K.J.; Fitzpatrick, E.; Gouin, S.; Milne, A.; Hartling, L. Pediatric Emergency Research Canada Gastroenteritis Study Group Group PERCGS. Gastroenteritis therapies in developed countries: Systematic review and meta-analysis. PLoS One, 2015, 10(6), e0128754.
[http://dx.doi.org/10.1371/journal.pone.0128754] [PMID: 26075617]
[10]
Fooks, L.J.; Gibson, G.R. Probiotics as modulators of the gut flora. Br. J. Nutr., 2002, 88(S1 Suppl. 1), S39-S49.
[http://dx.doi.org/10.1079/BJN2002628] [PMID: 12215180]
[11]
Verna, E.C.; Lucak, S. Use of probiotics in gastrointestinal disorders: What to recommend? Therap. Adv. Gastroenterol., 2010, 3(5), 307-319.
[http://dx.doi.org/10.1177/1756283X10373814] [PMID: 21180611]
[12]
Ansari, F.; Pourjafar, H.; Jodat, V.; Sahebi, J.; Ataei, A. Effect of Eudragit S100 nanoparticles and alginate chitosan encapsulation on the viability of Lactobacillus acidophilus and Lactobacillus rhamnosus. AMB Express, 2017, 7(1), 144.
[http://dx.doi.org/10.1186/s13568-017-0442-x] [PMID: 28687035]
[13]
Ghasemnezhad, R.; Razavilar, V.; Pourjafar, H.; Khosravi-Darani, K.; Ala, K. The viability of free and encapsulated Lactobacillus casei and Bifidobacterium animalis in chocolate milk, and evaluation of its pH changes and sensory properties during storage Ann. Res. Rev. Biol 2017, 1-8.
[14]
Pourjafar, H; Noori, N; Gandomi, H; Basti, AA; Ansari, F Stability and efficiency of double-coated beads containing Lactobacillus acidophilus obtained from the calcium alginate-chitosan and Eudragit S100 nanoparticles microencapsulation. Int. J. Probiotics Prebiotics, 2018, 13(2/3), 77-84. Gale Document Number: GALE|A569457753
[15]
Abdolhosseinzadeh, E.; Dehnad, A.R.; Pourjafar, H.; Homayouni, A.; Ansari, F. The production of probiotic Scallion Yogurt: Viability of Lactobacillus acidophilus freely and microencapsulated in the product. Carpath. J. Food Sci. Technol., 2018, 10(3), 72-80.
[16]
Li, D.; Breiman, A.; le Pendu, J.; Uyttendaele, M. Anti-viral Effect of Bifidobacterium adolescentis against Noroviruses. Front. Microbiol., 2016, 7, 864.
[http://dx.doi.org/10.3389/fmicb.2016.00864] [PMID: 27375585]
[17]
Mirzaei, H.; Pourjafar, H.; Homayouni, A. The effect of microencapsulation with calcium alginate and resistant starch on the Lactobacillus acidophilus (La5) survival rate in simulated gastrointestinal juice conditions. J. Vet. Res. (Pulawy), 2011, 66(4), 337-377.
[18]
Pourjafar, H.; Noori, N.; Gandomi, H.; Akhondzadeh Basti, A. Study of protective role of double coated beads of calcium alginate-chitosan-eudragit S100 nanoparticles achieved from microencapsulation of Lactobacillus acidophilus as a predominant flora of human and animals gut. J. Vet. Res. (Pulawy), 2016, 71(3), 311-320.
[19]
Tuohy, K.M.; Probert, H.M.; Smejkal, C.W.; Gibson, G.R. Using probiotics and prebiotics to improve gut health. Drug Discov. Today, 2003, 8(15), 692-700.
[http://dx.doi.org/10.1016/S1359-6446(03)02746-6] [PMID: 12927512]
[20]
Patro-Gołąb, B.; Shamir, R.; Szajewska, H. Yogurt for treating acute gastroenteritis in children: Systematic review and meta-analysis. Clin. Nutr., 2015, 34(5), 818-824.
[http://dx.doi.org/10.1016/j.clnu.2014.09.004] [PMID: 25267702]
[21]
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), 249-255.
[http://dx.doi.org/10.1111/apa.12487] [PMID: 24175943]
[22]
Guarino, A.; Lo Vecchio, A.; Canani, R.B. Probiotics as prevention and treatment for diarrhea. Curr. Opin. Gastroenterol., 2009, 25(1), 18-23.
[http://dx.doi.org/10.1097/MOG.0b013e32831b4455] [PMID: 19114770]
[23]
Szajewska, H.; Skórka, A.; Ruszczyński, M.; Gieruszczak-Białek, D. Meta-analysis: Lactobacillus GG for treating acute diarrhoea in children. Aliment. Pharmacol. Ther., 2007, 25(8), 871-881.
[http://dx.doi.org/10.1111/j.1365-2036.2007.03282.x] [PMID: 17402990]
[24]
Aponte, B.G.; Mancilla, B.C.A.; Carreazo, N.Y.; Galarza, R.R.A. Probiotics for treating persistent diarrhoea in children. Cochrane Database Syst. Rev., 2013, 10(8), CD007401.
[http://dx.doi.org/10.1002/14651858.CD007401.pub3] [PMID: 23963712]
[25]
Ahmadi, E.; Alizadeh-Navaei, R.; Rezai, M.S. Efficacy of probiotic use in acute rotavirus diarrhea in children: A systematic review and meta-analysis. Caspian J. Intern. Med., 2015, 6(4), 187-195.https://www.ncbi.nlm.nih.gov/pubmed/26644891
[PMID: 26644891]
[26]
Sterne, J.A.; Sutton, A.J.; Ioannidis, J.P.; Terrin, N.; Jones, D.R.; Lau, J.; Carpenter, J.; Rücker, G.; Harbord, R.M.; Schmid, C.H. Recommendations for examining and interpreting funnel plot asymmetry in meta-analyses of randomised controlled trials. BMJ,, 2011, 343d4002
[http://dx.doi.org/10.1136/bmj.d4002]
[27]
Hong Chau, T.T.; Minh Chau, N.N.; Hoang Le, N.T. Chung The, H.; Voong Vinh, P.; Nguyen To, N.T.; Ngoc, N.M.; Tuan, H.M.; Chau Ngoc, T.L.; Kolader, M.E.; Farrar, J.J.; Wolbers, M.; Thwaites, G.E.; Baker, S. Oxford-Vietnam probiotics study group. A double-blind, randomized, placebo-controlled trial of Lactobacillus acidophilus for the treatment of acute watery diarrhea in vietnamese children. Pediatr. Infect. Dis. J., 2018, 37(1), 35-42.
[http://dx.doi.org/10.1097/INF.0000000000001712] [PMID: 28787388]
[28]
Basu, S.; Chatterjee, M.; Ganguly, S.; Chandra, P.K. Efficacy of Lactobacillus rhamnosus GG in acute watery diarrhoea of Indian children: A randomised controlled trial. J. Paediatr. Child Health, 2007, 43(12), 837-842.
[http://dx.doi.org/10.1111/j.1440-1754.2007.01201.x] [PMID: 17803667]
[29]
Simakachorn, N.; Pichaipat, V.; Rithipornpaisarn, P.; Kongkaew, C.; Tongpradit, P.; Varavithya, W. Clinical evaluation of the addition of lyophilized, heat-killed Lactobacillus acidophilus LB to oral rehydration therapy in the treatment of acute diarrhea in children. J. Pediatr. Gastroenterol. Nutr. , 2000, 30(1), 68-72.
[http://dx.doi.org/10.1097/00005176-200001000-00020] [PMID: 10630442]
[30]
Gaon, D.; Garcia, H.; Winter, L.; Rodríguez, N.; Quintas, R.; Gonzalez, S.N.; Oliver, G. Effect of Lactobacillus strains and Saccharomyces boulardii on persistent diarrhea in children Medicina (Buenos Aires), 2003, 63(4), 293-298.
[31]
Rosenfeldt, V.; Michaelsen, K.F.; Jakobsen, M.; Larsen, C.N.; Møller, P.L.; Pedersen, P.; Tvede, M.; Weyrehter, H.; Valerius, N.H.; Paerregaard, A. Effect of probiotic Lactobacillus strains in young children hospitalized with acute diarrhea. Pediatr. Infect. Dis. J., 2002, 21(5), 411-416.
[http://dx.doi.org/10.1097/00006454-200205000-00012] [PMID: 12150178]
[32]
Ritchie, B.K.; Brewster, D.R.; Tran, C.D.; Davidson, G.P.; McNeil, Y.; Butler, R.N. Efficacy of Lactobacillus GG in aboriginal children with acute diarrhoeal disease: A randomised clinical trial. J. Pediatr. Gastroenterol. Nutr., 2010, 50(6), 619-624.
[http://dx.doi.org/10.1097/MPG.0b013e3181bbf53d] [PMID: 20400916]
[33]
Teran, C.G.; Teran-Escalera, C.N.; Villarroel, P.; Nitazoxanide, V.S. Nitazoxanide vs. probiotics for the treatment of acute rotavirus diarrhea in children: A randomized, single blind, controlled trial in Bolivian children. Int. J. Infect. Dis., 2009, 13(4), 518-523.
[http://dx.doi.org/10.1016/j.ijid.2008.09.014] [PMID: 19070525]
[34]
Grandy, G.; Medina, M.; Soria, R.; Terán, C.G.; 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(1), 253.
[http://dx.doi.org/10.1186/1471-2334-10-253] [PMID: 20735858]
[35]
Guandalini, S.; Pensabene, L.; Zikri, M.A.; Dias, J.A.; Casali, L.G.; Hoekstra, H.; Kolacek, S.; Massar, K.; Micetic-Turk, D.; Papadopoulou, A.; de Sousa, J.S.; Sandhu, B.; Szajewska, H.; Weizman, Z. Lactobacillus GG administered in oral rehydration solution to children with acute diarrhea: A multicenter European trial. J. Pediatr. Gastroenterol. Nutr., 2000, 30(1), 54-60.
[http://dx.doi.org/10.1097/00005176-200001000-00018] [PMID: 10630440]
[36]
İşlek, A.; Sayar, E.; Yılmaz, A.; Baysan, B.O.; Mutlu, D.; Artan, R. The role of Bifidobacterium lactis B94 plus inulin in the treatment of acute infectious diarrhea in children. Turk. J. Gastroenterol., 2014, 25(6), 628-633.
[http://dx.doi.org/10.5152/tjg.2014.14022] [PMID: 25599772]
[37]
Sindhu, K.N.; Sowmyanarayanan, T.V.; Paul, A.; Babji, S.; Ajjampur, S.S.; Priyadarshini, S.; Sarkar, R.; Balasubramanian, K.A.; Wanke, C.A.; Ward, H.D.; Kang, G. Immune response and intestinal permeability in children with acute gastroenteritis treated with Lactobacillus rhamnosus GG: A randomized, double-blind, placebo-controlled trial. Clin. Infect. Dis., 2014, 58(8), 1107-1115.
[http://dx.doi.org/10.1093/cid/ciu065] [PMID: 24501384]
[38]
Szymański, H.; Pejcz, J.; Jawień, M.; Chmielarczyk, A.; Strus, M.; Heczko, P.B. Treatment of acute infectious diarrhoea in infants and children with a mixture of three Lactobacillus rhamnosus strains--a randomized, double-blind, placebo-controlled trial. Aliment. Pharmacol. Ther., 2006, 23(2), 247-253.
[http://dx.doi.org/10.1111/j.1365-2036.2006.02740.x] [PMID: 16393304]
[39]
Abbaskhanian, A.; Rezai, M.S.; Karami, H.; Hasnpour, A. The effect of fermented yogurt on rotavirus diarrhea in children. Health Med., 2012, 6(5), 1600-1604.
[40]
Dalgic, N.; Sancar, M.; Bayraktar, B.; Pullu, M.; Hasim, O. Probiotic, zinc and lactose-free formula in children with rotavirus diarrhea: Are they effective? Pediatr. Int., 2011, 53(5), 677-682.
[http://dx.doi.org/10.1111/j.1442-200X.2011.03325.x] [PMID: 21261786]
[41]
Das, S.; Gupta, P.K.; Das, R.R. Efficacy and safety of Saccharomyces boulardii in acute rotavirus diarrhea: Double blind randomized controlled trial from a developing country. J. Trop. Pediatr., 2016, 62(6), 464-470.
[PMID: 27283364]
[42]
Lee, D.K.; Park, J.E.; Kim, M.J.; Seo, J.G.; Lee, J.H.; Ha, N.J. Probiotic bacteria, B. longum and L. acidophilus inhibit infection by rotavirus in vitro and decrease the duration of diarrhea in pediatric patients. Clin. Res. Hepatol. Gastroenterol., 2015, 39(2), 237-244.
[http://dx.doi.org/10.1016/j.clinre.2014.09.006] [PMID: 25459995]
[43]
Sarker, S.A.; Sultana, S.; Fuchs, G.J.; Alam, N.H.; Azim, T.; Brüssow, H.; Hammarström, L. Lactobacillus paracasei strain ST11 has no effect on rotavirus but ameliorates the outcome of nonrotavirus diarrhea in children from Bangladesh. Pediatrics, 2005, 116(2), e221-e228.
[http://dx.doi.org/10.1542/peds.2004-2334] [PMID: 15995003]
[44]
Riddle, M.S.; DuPont, H.L.; Connor, B.A. ACG clinical guideline: diagnosis, treatment, and prevention of acute diarrheal infections in adults. Am. J. Gastroenterol., 2016, 111(5), 602-622.
[http://dx.doi.org/10.1038/ajg.2016.126] [PMID: 27068718]
[45]
Allen, S.J.; Martinez, E.G.; Gregorio, G.V.; Dans, L.F. Probiotics for treating acute infectious diarrhoea. Sao Paulo Med. J., 2011, 129(3), 185-185.
[http://dx.doi.org/10.1590/S1516-31802011000300012]
[46]
Dubey, A.P.; Rajeshwari, K.; Chakravarty, A.; Famularo, G. Use of VSL[sharp]3 in the treatment of rotavirus diarrhea in children: preliminary results. J. Clin. Gastroenterol., 2008, 42(Suppl. 3 Pt 1), S126-S129.
[http://dx.doi.org/10.1097/MCG.0b013e31816fc2f6] [PMID: 18806703]
[47]
Huang, Y.; Liu, P.Y.; Hsieh, K.S. Clinical effectiveness of threecombination probiotics therapy in pediatric patients with salmonella and rotavirus gastroenteritis: Randomised clinical trial. Int. J. Infect. Dis. 2012, 16e199
[http://dx.doi.org/10.1016/j.ijid.2012.05.776]
[48]
Majamaa, H.; Isolauri, E.; Saxelin, M.; Vesikari, T. Lactic acid bacteria in the treatment of acute rotavirus gastroenteritis. J. Pediatr. Gastroenterol. Nutr., 1995, 20(3), 333-338.
[http://dx.doi.org/10.1097/00005176-199504000-00012] [PMID: 7608829]
[49]
Erdoğan, O.; Tanyeri, B.; Torun, E.; Gönüllü, E.; Arslan, H.; Erenberk, U.; Öktem, F. The comparition of the efficacy of two different probiotics in rotavirus gastroenteritis in children. J. Trop. Med., 2012., 2012787240
[http://dx.doi.org/10.1155/2012/787240] [PMID: 22778754]
[50]
Isolauri, E.; Kaila, M.; Mykkänen, H.; Ling, W.H.; Salminen, S. Oral bacteriotherapy for viral gastroenteritis. Dig. Dis. Sci., 1994, 39(12), 2595-2600.
[http://dx.doi.org/10.1007/BF02087695] [PMID: 7995184]
[51]
Guarino, A.; Canani, R.B.; Spagnuolo, M.I.; Albano, F.; Di Benedetto, L. Oral bacterial therapy reduces the duration of symptoms and of viral excretion in children with mild diarrhea. J. Pediatr. Gastroenterol. Nutr., 1997, 25(5), 516-519.
[http://dx.doi.org/10.1097/00005176-199711000-00005] [PMID: 9360205]
[52]
Fang, S.B.; Lee, H.C.; Hu, J.J.; Hou, S.Y.; Liu, H.L.; Fang, H.W. Dose-dependent effect of Lactobacillus rhamnosus on quantitative reduction of faecal rotavirus shedding in children. J. Trop. Pediatr., 2009, 55(5), 297-301.
[http://dx.doi.org/10.1093/tropej/fmp001] [PMID: 19203988]
[53]
Kaila, M.; Isolauri, E.; Saxelin, M.; Arvilommi, H.; Vesikari, T. Viable versus inactivated lactobacillus strain GG in acute rotavirus diarrhoea. Arch. Dis. Child., 1995, 72(1), 51-53.
[http://dx.doi.org/10.1136/adc.72.1.51] [PMID: 7717739]
[54]
Kaila, M.; Isolauri, E.; Soppi, E.; Virtanen, E.; Laine, S.; Arvilommi, H. Enhancement of the circulating antibody secreting cell response in human diarrhea by a human Lactobacillus strain. Pediatr. Res., 1992, 32(2), 141-144.
[http://dx.doi.org/10.1203/00006450-199208000-00002] [PMID: 1324462]
[55]
García-Menor, E.; García-Marín, F.; Vecino-López, R.; Horcajo-Martínez, G.; de Ibarrondo Guerrica-Echevarría, M.J.; Gómez-González, P.; Velasco-Ortega, S.; Suárez-Almarza, J.; Nieto-Magro, C. A multicenter, prospective, randomized controlled trial to evaluate the additional benefit of a multistrain synbiotic (Prodefen ®) in the clinical management of acute viral diarrhea in children. Global Pediatr. Health, 2016, 3, 2333794X16679587.
[http://dx.doi.org/10.1177/2333794X16679587]
[56]
Narayanappa, D. Randomized double-blinded controlled trial to evaluate the efficacy and safety of Bifilac in patients with acute viral diarrhea. Indian J. Pediatr., 2008, 75(7), 709-713.
[http://dx.doi.org/10.1007/s12098-008-0134-2] [PMID: 18716740]
[57]
Narayanappa, D. A randomized double blind placebo controlled trial to evaluate the efficacy and safety of Bifilac in children with acute rotaviral diarrhea. Int. J. Probiotics Prebiotics, 2009, 4(2), 87-90.
[58]
Park, M.S.; Kwon, B.; Ku, S.; Ji, G.E. Ji, G. The efficacy of Bifidobacterium longum BORI and Lactobacillus acidophilus AD031 probiotic treatment in infants with rotavirus infection. Nutrients, 2017, 9(8), 887.
[http://dx.doi.org/10.3390/nu9080887] [PMID: 28813007]
[59]
Liberati, A.; Altman, D.G.; Tetzlaff, J.; Mulrow, C.; Gøtzsche, P.C.; Ioannidis, J.P.; Clarke, M.; Devereaux, P.J.; Kleijnen, J.; Moher, D. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: Explanation and elaboration. PLoS Med., 2009, 6(7), e1000100.
[http://dx.doi.org/10.1371/journal.pmed.1000100] [PMID: 19621070]


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VOLUME: 21
ISSUE: 11
Year: 2020
Published on: 20 September, 2020
Page: [1042 - 1051]
Pages: 10
DOI: 10.2174/1389201021666200416123931
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