Orally ingested probiotics, prebiotics, and synbiotics as countermeasures for respiratory tract infections in nonelderly adults: a systematic review and meta-analysis
Open accessAbstract
The impact of gut microbiota-targeted interventions on the incidence, duration, and severity of respiratory tract infections (RTIs) in nonelderly adults, and factors moderating any such effects, are unclear. This systematic review and meta-analysis aimed to determine the effects of orally ingested probiotics, prebiotics, and synbiotics compared with placebo on RTI incidence, duration, and severity in nonelderly adults, and to identify potential sources of heterogeneity. Studies were identified by searching CENTRAL, PubMed, Scopus, and Web of Science up to December 2021. English-language, peer-reviewed publications of randomized, placebo-controlled studies that tested an orally ingested probiotic, prebiotic, or synbiotic intervention of any dose for ≥1 wk in adults aged 18-65 y were included. Results were synthesized using intention-to-treat and per-protocol random-effects meta-analysis. Heterogeneity was explored by subgroup meta-analysis and meta-regression. Risk of bias was assessed using the Cochrane risk-of-bias assessment tool for randomized trials version 2 (RoB2). Forty-two manuscripts reporting effects of probiotics (n = 38), prebiotics (n = 2), synbiotics (n = 1) or multiple -biotic types (n = 1) were identified (n = 9179 subjects). Probiotics reduced the risk of experiencing ≥1 RTI (relative risk = 0.91; 95% CI: 0.84, 0.98; P = 0.01), and total days (rate ratio = 0.77; 95% CI: 0.71, 0.83; P < 0.001), duration (Hedges' g = -0.23; 95% CI: -0.39, -0.08; P = 0.004), and severity (Hedges' g = -0.16; 95% CI: -0.29, -0.03; P = 0.02) of RTIs. Effects were relatively consistent across different strain combinations, doses, and durations, although reductions in RTI duration were larger with fermented dairy as the delivery matrix, and beneficial effects of probiotics were not observed in physically active populations. Overall risk of bias was rated as "some concerns" for most studies. In conclusion, orally ingested probiotics, relative to placebo, modestly reduce the incidence, duration, and severity of RTIs in nonelderly adults. Physical activity and delivery matrix may moderate some of these effects. Whether prebiotic and synbiotic interventions confer similar protection remains unclear due to few relevant studies. This trial was registered at https://www.crd.york.ac.uk/prospero/ as CRD42020220213.
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Many systematic reviews and meta-analyses of RCTs suggest beneficial effects of flavonoids and probiotics, while the effects of vitamins A, C, D, E, and zinc remain controversial.
“In recent years, many systematic reviews and meta-analyses of randomized controlled trials (RCTs) have explored the effectiveness of oral nutrient supplements in preventing RTIs,4,8, 9, 10, 11, 12, 13, 14, 15, 16 suggesting beneficial effects of flavonoids and probiotics, while the effects of vitamins A, C, D, E, and zinc remain controversial.”
Fewer systematic reviews have focused on the adult population.
“However, fewer systematic reviews have focused on the adult population.”
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Cites
Bias in meta-analysis detected by a simple, graphical test
Egger, M., Smith, G. D., Schneider, M., & Minder, C. (1997) · BMJ · doi:10.1136/bmj.315.7109.629 · Cited by 56,722 · see citing works
RoB 2: a revised tool for assessing risk of bias in randomised trials
Sterne, J. A. C., Savović, J., Page, M. J., Elbers, R. G., Blencowe, N. S., Boutron, I., Cates, C. J., Cheng, H.-Y., Corbett, M. S., Eldridge, S. M., et al. (2019) · BMJ · doi:10.1136/bmj.l4898 · Cited by 33,583 · see citing works
Cochrane Handbook for Systematic Reviews of Interventions: Cochrane Book Series
(2008) · doi:10.1002/9780470712184 · Cited by 25,048 · see citing works
Hill (2014) · doi:10.1038/nrgastro.2014.66 · Cited by 9,592 · see citing works
Gibson, G. R., Hutkins, R., Sanders, M. E., Prescott, S. L., Reimer, R. A., Salminen, S. J., Scott, K., Stanton, C., Swanson, K. S., Cani, P. D., et al. (2017) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/nrgastro.2017.75 · Cited by 5,634 · see citing works
Naghavi, M., Abajobir, A. A., Abbafati, C., Abbas, K. M., Abd-Allah, F., Abera, S. F., Aboyans, V., Adetokunboh, O., Afshin, A., Agrawal, A., et al. (2017) · The Lancet · doi:10.1016/s0140-6736(17)32152-9 · Cited by 4,821 · see citing works
Introduction to the human gut microbiota
Thursby, E., & Juge, N. (2017) · Biochemical Journal · doi:10.1042/bcj20160510 · Cited by 3,600 · see citing works
Swanson, K. S., Gibson, G. R., Hutkins, R., Reimer, R. A., Reid, G., Verbeke, K., Scott, K. P., Holscher, H. D., Azad, M. B., Delzenne, N. M., et al. (2020) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/s41575-020-0344-2 · Cited by 2,196 · see citing works
Probiotics and prebiotics in intestinal health and disease: from biology to the clinic
Sanders, M. E., Merenstein, D. J., Reid, G., Gibson, G. R., & Rastall, R. A. (2019) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/s41575-019-0173-3 · Cited by 2,059 · see citing works
Health benefits of fermented foods: Microbiota and beyond
Marco, M. L., Heeney, D., Binda, S., Cifelli, C. J., Cotter, P. D., Foligné, B., Gänzle, M., Kort, R., Pasin, G., Pihlanto, A., et al. (2017) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2016.11.010 · Cited by 1,674 · see citing works
How to select, calculate, and interpret effect sizes.
Durlak, J. (2009) · Journal of Pediatric Psychology · doi:10.1093/jpepsy/jsp004 · Cited by 1,487 · see citing works
Marco, M. L., Sanders, M. E., Gänzle, M., Arrieta, M. C., Cotter, P. D., De Vuyst, L., Hill, C., Holzapfel, W., Lebeer, S., Merenstein, D., et al. (2021) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/s41575-020-00390-5 · Cited by 937 · see citing works
The Economic Burden of Non–Influenza-Related Viral Respiratory Tract Infection in the United States
Fendrick, A. M., Monto, A. S., Nightengale, B. S., & Sarnes, M. W. (2003) · Archives of Internal Medicine · doi:10.1001/archinte.163.4.487 · Cited by 854 · see citing works
COVID-19: Current understanding of its Pathophysiology, Clinical presentation and Treatment
Parasher, A. (2020) · Postgraduate Medical Journal · doi:10.1136/postgradmedj-2020-138577 · Cited by 780 · see citing works
National Ambulatory Medical Care Survey: 2001 summary.
Cherry, D. K., Burt, C. W., & Woodwell, D. A. (2003) · PubMed · Cited by 686 · see citing works
Probiotics for preventing acute upper respiratory tract infections
Hao, Q., Dong, B. R., & Wu, T. (2015) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd006895.pub3 · Cited by 569 · see citing works
Systematic review automation technologies
Tsafnat, G., Glasziou, P., Choong, M. K., Dunn, A., Galgani, F., & Coiera, E. (2014) · Systematic Reviews · doi:10.1186/2046-4053-3-74 · Cited by 472 · see citing works
Can exercise affect immune function to increase susceptibility to infection?
Simpson, R. J., Simpson, R. J., Gleeson, M., Gleeson, M., Kruger, K., Pyne, D. B., Pyne, D. B., & Walsh, N. P. (2026) · PubMed · doi:10.22029/eir.2020.1730 · Cited by 365 · see citing works
New perspectives in fermented dairy products and their health relevance
García‐Burgos, M., Moreno‐Fernández, J., Alférez, M. J. M., Díaz‐Castro, J., & López‐Aliaga, I. (2020) · Journal of Functional Foods · doi:10.1016/j.jff.2020.104059 · Cited by 338 · see citing works
Global burden of upper respiratory infections in 204 countries and territories, from 1990 to 2019
Jin, X., Ren, J., Li, R., Gao, Y., Zhang, H., Li, J., Zhang, J., Wang, X., & Wang, G. (2021) · eClinicalMedicine · doi:10.1016/j.eclinm.2021.100986 · Cited by 323 · see citing works
National Ambulatory Medical Care Survey: 2002 summary.
Woodwell, D. A., & Cherry, D. K. (2004) · PubMed · Cited by 314 · see citing works
King, S., Glanville, J., Sanders, M. E., Fitzgerald, A., & Varley, D. (2014) · British Journal Of Nutrition · doi:10.1017/s0007114514000075 · Cited by 283 · see citing works
International Society of Sports Nutrition Position Stand: Probiotics
Jäger, R., Mohr, A. E., Carpenter, K. C., Kerksick, C. M., Purpura, M., Moussa, A., Townsend, J. R., Lamprecht, M., West, N. P., Black, K., et al. (2019) · Journal of the International Society of Sports Nutrition · doi:10.1186/s12970-019-0329-0 · Cited by 277 · see citing works
Exercise and Respiratory Tract Viral Infections
Martin, S. A., Pence, B. D., & Woods, J. A. (2009) · Exercise and Sport Sciences Reviews · doi:10.1097/jes.0b013e3181b7b57b · Cited by 264 · see citing works
de Vrese, M., Winkler, P., Rautenberg, P., Harder, T., Noah, C., Laue, C., Ott, S. J., Hampe, J., Schreiber, S., Heller, K. J., et al. (2005) · Clinical Nutrition · doi:10.1016/j.clnu.2005.02.006 · Cited by 252 · see citing works
Daily Probiotic’s (Lactobacillus casei Shirota) Reduction of Infection Incidence in Athletes
Gleeson, M., Bishop, N. C., Oliveira, M., & Tauler, P. (2011) · International Journal of Sport Nutrition and Exercise Metabolism · doi:10.1123/ijsnem.21.1.55 · Cited by 239 · see citing works
Cox, A. J., Pyne, D. B., Saunders, P. U., & Fricker, P. A. (2010) · British Journal of Sports Medicine · doi:10.1136/bjsm.2007.044628 · Cited by 234 · see citing works
Rizzardini, G., Eskesen, D., Calder, P. C., Capetti, A., Jespersen, L., & Clerici, M. (2012) · British Journal Of Nutrition · doi:10.1017/s000711451100420x · Cited by 217 · see citing works
Probiotics for prevention and treatment of respiratory tract infections in children
Wang, Y., Li, X., Ge, T., Xiao, Y., Liao, Y., Cui, Y., Zhang, Y., Ho, W., Yu, G., & Zhang, T. (2016) · Medicine · doi:10.1097/md.0000000000004509 · Cited by 209 · see citing works
de Vrese, M., Winkler, P., Rautenberg, P., Harder, T., Noah, C., Laue, C., Ott, S., Hampe, J., Schreiber, S., Heller, K., et al. (2006) · Vaccine · doi:10.1016/j.vaccine.2006.05.048 · Cited by 201 · see citing works
Flannery, B. L., Kondor, R. J. G., Chung, J. R., Gaglani, M., Reis, M. D., Zimmerman, R. K., Nowalk, M. P., Jackson, M. L., Jackson, L. A., Monto, A. S., et al. (2019) · The Journal of Infectious Diseases · doi:10.1093/infdis/jiz543 · Cited by 193 · see citing works
West, N. P., Pyne, D. B., Cripps, A. W., Hopkins, W. G., Eskesen, D. C., Jairath, A., Christophersen, C. T., Conlon, M. A., & Fricker, P. A. (2011) · Nutrition Journal · doi:10.1186/1475-2891-10-30 · Cited by 180 · see citing works
Kekkonen, R. A., Vasankari, T. J., Vuorimaa, T., Haahtela, T., Julkunen, I., & Korpela, R. (2007) · International Journal of Sport Nutrition and Exercise Metabolism · doi:10.1123/ijsnem.17.4.352 · Cited by 170 · see citing works
Childs, C. E., Röytiö, H., Alhoniemi, E. J., Fekete, A. A., Forssten, S. D., Hudjec, N., Lim, Y. N., Steger, C. J., Yaqoob, P., Tuohy, K. M., et al. (2014) · British Journal Of Nutrition · doi:10.1017/s0007114513004261 · Cited by 169 · see citing works
West, N. P., Horn, P. L., Pyne, D. B., Gebski, V. J., Lahtinen, S. J., Fricker, P. A., & Cripps, A. W. (2014) · Clinical Nutrition · doi:10.1016/j.clnu.2013.10.002 · Cited by 159 · see citing works
Walsh, N. P., & Oliver, S. J. (2015) · Immunology and Cell Biology · doi:10.1038/icb.2015.99 · Cited by 146 · see citing works
Shida, K., Sato, T., Iizuka, R., Hoshi, R., Watanabe, O., Igarashi, T., Miyazaki, K., Nanno, M., & Ishikawa, F. (2015) · Zeitschrift für Ernährungswissenschaft · doi:10.1007/s00394-015-1056-1 · Cited by 144 · see citing works
Strasser, B., Geiger, D., Schauer, M., Gostner, J., Gatterer, H., Burtscher, M., & Fuchs, D. (2016) · Nutrients · doi:10.3390/nu8110752 · Cited by 142 · see citing works
Zhang, H., Yeh, C., Zong-lian, J., Ding, L., Liu, B. Y., Zhang, L., & Dannelly, H. K. (2018) · Synthetic and Systems Biotechnology · doi:10.1016/j.synbio.2018.03.001 · Cited by 139 · see citing works
Berggren, A., Ahrén, I. L., Larsson, N., & Önning, G. (2010) · European Journal of Nutrition · doi:10.1007/s00394-010-0127-6 · Cited by 132 · see citing works
Chong, H.-X., Yusoff, N. A. A., Hor, Y.-Y., Lew, L.-C., Jaafar, M. H., Choi, S. B., Yusoff, M. S. B., Wahid, N. A., Abdullah, M. F. I. L. B., Zakaria, N., et al. (2019) · Journal of Dairy Science · doi:10.3168/jds.2018-16103 · Cited by 121 · see citing works
Michael, D. R., Jack, A. A., Masetti, G., Davies, T. S., Loxley, K. E., Kerry-Smith, J., Plummer, J. F., Marchesi, J. R., Mullish, B. H., McDonald, J. A. K., et al. (2020) · Scientific Reports · doi:10.1038/s41598-020-60991-7 · Cited by 106 · see citing works
Jespersen, L., Tarnow, I., Eskesen, D. C., Melsæther, C., Michelsen, B., Bügel, S., Dragsted, L. O., Rijkers, G. T., & Calder, P. C. (2015) · American Journal of Clinical Nutrition · doi:10.3945/ajcn.114.103531 · Cited by 103 · see citing works
Gleeson, M., Bishop, N. C., Oliveira, M., McCauley, T., Tauler, P., & Lawrence, C. (2012) · International Journal of Sport Nutrition and Exercise Metabolism · doi:10.1123/ijsnem.22.4.235 · Cited by 100 · see citing works
Turner, R. B., Woodfolk, J. A., Borish, L., Steinke, J. W., Patrie, J. T., Muehling, L. M., Lahtinen, S. J., & Lehtinen, M. J. (2017) · Beneficial Microbes · doi:10.3920/bm2016.0160 · Cited by 97 · see citing works
Tiollier, E., Chennaoui, M., Gomez-Merino, D., Drogou, C., Filaire, E., & Guezennec, C. Y. (2007) · Military Medicine · doi:10.7205/milmed.172.9.1006 · Cited by 95 · see citing works
Guillemard, E., Tanguy, J., Demessant‐Flavigny, A., de la Motte, S., & Schrezenmeir, J. (2010) · Journal of the American College of Nutrition · doi:10.1080/07315724.2010.10719882 · Cited by 92 · see citing works
Sugimura, T., Takahashi, H., Jounai, K., Ohshio, K., Kanayama, M., Tazumi, K., Tanihata, Y., Miura, Y., Fujiwara, D., & Yamamoto, N. (2015) · British Journal Of Nutrition · doi:10.1017/s0007114515002408 · Cited by 91 · see citing works
A New Chance of Preventing Winter Diseases by the Administration of Synbiotic Formulations
Pregliasco, F. E., Anselmi, G., Fonte, L., Giussani, F., Schieppati, S., & Soletti, L. (2008) · Journal of Clinical Gastroenterology · doi:10.1097/mcg.0b013e31817e1c91 · Cited by 89 · see citing works
Chan, C. K. Y., Tao, J., Chan, O. S., Li, H.-B., & Pang, H. (2020) · Advances in Nutrition · doi:10.1093/advances/nmaa003 · Cited by 89 · see citing works
Smith, T. J., Radler, D. R., Denmark, R., Haley, T. F., & Touger-Decker, R. E. (2012) · British Journal Of Nutrition · doi:10.1017/s0007114512004138 · Cited by 86 · see citing works
Haywood, B. A., Black, K. E., Baker, D., McGarvey, J., Healey, P., & Brown, R. C. (2014) · Journal of Science and Medicine in Sport · doi:10.1016/j.jsams.2013.08.004 · Cited by 85 · see citing works
Hor, Y.-Y., Lew, L.-C., Lau, A. S.-Y., Ong, J.-S., Chuah, L., Lee, Y. Y., Choi, S. B., Rashid, F., Wahid, N. A., Sun, Z., et al. (2018) · Journal of Functional Foods · doi:10.1016/j.jff.2018.03.017 · Cited by 76 · see citing works
Michalickova, D., Minic, R., Dikic, N., Andjelkovic, M., Kostic-Vucicevic, M., Stojmenovic, T., Nikolic, I., & Djordjevic, B. (2016) · Applied Physiology, Nutrition, and Metabolism · doi:10.1139/apnm-2015-0541 · Cited by 74 · see citing works
β-Glucan, Immune Function, and Upper Respiratory Tract Infections in Athletes
Nieman, D. C., Henson, D. A., McMahon, M. E., Wrieden, J., Davis, J. M., Murphy, E. A., Gross, S. J., McAnulty, L. S., & Dumke, C. L. (2008) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0b013e31817057c2 · Cited by 74 · see citing works
Hughes, C., Davoodi‐Semiromi, Y., Colee, J., Culpepper, T., Dahl, W. J., Mai, V., Christman, M. C., & Langkamp‐Henken, B. (2011) · American Journal of Clinical Nutrition · doi:10.3945/ajcn.111.014126 · Cited by 70 · see citing works
The influence of 15-week exercise training on dietary patterns among young adults
Joo, J., Williamson, S. A., Vazquez, A. I., Fernández, J. R., & Bray, M. S. (2019) · International Journal of Obesity · doi:10.1038/s41366-018-0299-3 · Cited by 70 · see citing works
Gleeson, M., BISHOP, N. C., & Struszczak, L. (2016) · European Journal of Applied Physiology · doi:10.1007/s00421-016-3415-x · Cited by 66 · see citing works
Vaisberg, M., Paixão, V., Almeida, E., Santos, J. M. B., Foster, R., Rossi, M. N., Pithon-Curi, T., Gorjão, R., Momesso, C. M., Andrade, M., et al. (2019) · Nutrients · doi:10.3390/nu11071678 · Cited by 57 · see citing works
Langkamp-Henken, B., Rowe, C. C., Ford, A. L., Christman, M. C., Nieves, C., Khouri, L., Specht, G. J., Girard, S.-A., Spaiser, S. J., & Dahl, W. J. (2015) · British Journal of Nutrition · doi:10.1017/s0007114514003997 · Cited by 54 · see citing works
Habermann, W., Zimmermann, K., Skarabis, H., Kunze, R., & Rusch, V. (2011) · Arzneimittelforschung · doi:10.1055/s-0031-1299941 · Cited by 49 · see citing works
Kumpu, M., Kekkonen, R. A., Korpela, R., Tynkkynen, S., Järvenpää, S. K., Kautiainen, H., Allen, E. K., Hendley, J. O., Pitkäranta, A., & Winther, B. (2015) · Beneficial Microbes · doi:10.3920/bm2014.0164 · Cited by 47 · see citing works
Meng, H., Lee, Y., Ba, Z., Peng, J., Lin, J., Boyer, A. S., Fleming, J. A., Furumoto, E. J., Roberts, R., Kris‐Etherton, P. M., et al. (2016) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.201500665 · Cited by 45 · see citing works
Li, L., Hong, K., Sun, Q., Xiao, H., Lai, L., Ming, M., & Li, C. (2020) · Evidence-based Complementary and Alternative Medicine · doi:10.1155/2020/8734140 · Cited by 34 · see citing works
Williams, L. M., Stoodley, I. L., Berthon, B. S., & Wood, L. G. (2021) · Advances in Nutrition · doi:10.1093/advances/nmab114 · Cited by 34 · see citing works
Tapiovaara, L. K., Kumpu, M., Mäkivuokko, H., Waris, M. E., Korpela, R., Pitkäranta, A., & Winther, B. (2016) · International Forum of Allergy & Rhinology · doi:10.1002/alr.21748 · Cited by 32 · see citing works
Pumpa, K. L., McKune, A. J., & Harnett, J. (2019) · Journal of science and medicine in sport · doi:10.1016/j.jsams.2019.03.013 · Cited by 28 · see citing works
Möller, G. B., Goulart, M. J. V. D. C., Nicoletto, B. B., Alves, F. D., & Schneider, C. D. (2019) · International Journal of Sport Nutrition and Exercise Metabolism · doi:10.1123/ijsnem.2018-0227 · Cited by 27 · see citing works
Ahrén, I. L., Hillman, M., Nordström, E. A., Larsson, N., & Niskanen, T. M. (2020) · Journal of Nutrition · doi:10.1093/jn/nxaa353 · Cited by 26 · see citing works
Evaluation of Probiotics for Warfighter Health and Performance
Agans, R., Giles, G. E., Goodson, M. S., Karl, J. P., Leyh, S. M., Mumy, K. L., Racicot, K., & Soares, J. W. (2020) · Frontiers in Nutrition · doi:10.3389/fnut.2020.00070 · Cited by 26 · see citing works
Self-citationHabermann, W., Zimmermann, K., Skarabis, H., Kunze, R., & Rusch, V. (2011) · Arzneimittelforschung · doi:10.1055/s-0031-1300140 · Cited by 25 · see citing works
Łagowska, K., & Bajerska, J. (2021) · Journal of Athletic Training · doi:10.4085/592-20 · Cited by 24 · see citing works
Karl, J. P. (2020) · Military Medicine · doi:10.1093/milmed/usaa261 · Cited by 23 · see citing works
Self-citationNishihira, J., Moriya, T., Sakai, F., Kabuki, T., Kawasaki, Y., & Nishimura, M. (2016) · Functional Foods in Health and Disease · doi:10.31989/ffhd.v6i9.284 · Cited by 23 · see citing works
Kalima, K., Lehtoranta, L., He, L., Pitkäniemi, J. M., Lundell, R. V., Julkunen, I., Roivainen, M., Närkiö, M., Mäkelä, M. J., Siitonen, S., et al. (2016) · Beneficial Microbes · doi:10.3920/bm2015.0172 · Cited by 16 · see citing works
Emre, İ. E., Eroğlu, Y., Kara, A., Dinleyici, E. Ç., & Özen, M. (2020) · Beneficial Microbes · doi:10.3920/bm2019.0119 · Cited by 15 · see citing works
Altadill, T., Espadaler, J., & Liong, M. (2021) · Microorganisms · doi:10.3390/microorganisms9030528 · Cited by 13 · see citing works
Lyu, S., Zhang, C. S., Guo, X., Zhang, A. L., Sun, J., Lu, C., Xue, C. C., & Luo, X. (2020) · Evidence-based Complementary and Alternative Medicine · doi:10.1155/2020/5181587 · Cited by 10 · see citing works
Schröder, C., Schmidt, S., Garbe, E., Röhmel, J., & Giersiepen, K. (2015) · BMC Nutrition · doi:10.1186/2055-0928-1-3 · Cited by 7 · see citing works
Flagged first, then by citations
2 of the 81 references couldn’t be matched to a known paper.
Research works printed but not linked: 4
- 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.
- Habermann W, Zimmermann K, Skarabis H, Kunze R, Rusch V. [The effect of a bacterial immunostimulant (human Enterococcus faecalis bacteria) on the occurrence of relapse in patients with chronic recurrent bronchitis]. Arzneimittelforschung 2001;51(11):931-7.
- Habermann W, Zimmermann K, Skarabis H, Kunze R, Rusch V. [Reduction of acute recurrence in patients with chronic recurrent hypertrophic sinusitis by treatment with a bacterial immunostimulant (Enterococcus faecalis bacteriae of human origin)]. Arzneimittelforschung 2002;52(8):622-7.
- Michalickova D, Minic R, Dikic N, Andjelkovic M, Kostic-Vucicevic M, Stojmenovic T, et al. Appl Physiol Nutr Metab 2016;41(7):782-9.
Cited by
Sorted by citations
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Merenstein, D. J., Tancredi, D. J., Karl, J. P., Krist, A. H., Lenoir‐Wijnkoop, I., Reid, G., Roos, S., Szajewska, H., & Sanders, M. E. (2024) · Advances in Nutrition · doi:10.1016/j.advnut.2024.100265 · Cited by 51 · see citing works
Self-citationProbiotic cultivated meat: bacterial-based scaffolds and products to improve cultivated meat
Kolodkin‐Gal, I., Dash, O., & Rak, R. (2023) · Trends in biotechnology · doi:10.1016/j.tibtech.2023.09.002 · Cited by 29 · see citing works
Gizachew, S., Van Beeck, W., Spacova, I., Dekeukeleire, M., Alemu, A., Woldemedhin, W. M., Mariam, S. H., Lebeer, S., & Engidawork, E. (2023) · Fermentation · doi:10.3390/fermentation9030258 · Cited by 26 · see citing works
Yang, K., Chen, Y., Wang, M., Zhang, Y., Yuan, Y. J., Hou, H., & Mao, Y.-H. (2024) · Nutrients · doi:10.3390/nu16111602 · Cited by 13 · see citing works
Comerford, K. B., Lawson, Y., Young, M. A., Knight, M. G., McKinney, K. H., Mpasi, P., & Mitchell, E. P. (2024) · Journal of the National Medical Association · doi:10.1016/j.jnma.2024.01.020 · Cited by 13 · see citing works
Lungaro, L., Malfa, P., Manza, F., Negrelli, M., Costanzini, A., Squarzanti, D. F., Re, M. L., Cariani, A., Ghisellini, S., Caputo, F., et al. (2025) · Nutrients · doi:10.3390/nu17091490 · Cited by 5 · see citing works
Zhang, H., Feng, Y., Yang, H., Li, Y., Ma, Z., Li, L., Chen, L., Zhao, Y., Shan, L., & Xia, Y. (2025) · Ecotoxicology and Environmental Safety · doi:10.1016/j.ecoenv.2025.117848 · Cited by 5 · see citing works
Zhu, Z., Zhu, X., Chu, Y., Zhang, B., & Chen, Y. (2025) · EClinicalMedicine · doi:10.1016/j.eclinm.2025.103479 · Cited by 4 · see citing works
“12,22 Synbiotics were defined as combinations of probiotics (single or multiple strains) and prebiotics (nondigestible carbohydrates fermented by gut microbiota).”
InfluentialThe effect of probiotic Bifidobacterium lactis Bl-04 on innate antiviral responses in vitro
Latvala, S., Lehtinen, M. J., Mäkelä, S. M., Nedveck, D. A., Zabel, B., Ahonen, I., Lehtoranta, L., Turner, R. B., & Liljavirta, J. (2024) · Heliyon · doi:10.1016/j.heliyon.2024.e29588 · Cited by 6 · see citing works
A review of dairy food intake for improving health among black geriatrics in the US
Mitchell, E. P., Comerford, K. B., Knight, M. G., McKinney, K. H., & Lawson, Y. (2024) · Journal of the National Medical Association · doi:10.1016/j.jnma.2024.01.017 · Cited by 3 · see citing works
Colston, S. M., Barbato, R. A., Goodson, M. S., Karl, J. P., Kokoska, R. J., Leary, D. D., Racicot, K., Varaljay, V. A., & Soares, J. W. (2023) · BMJ Military Health · doi:10.1136/military-2022-002307 · Cited by 3 · see citing works
Self-citationMeeting report of the sixth annual tri-service microbiome consortium symposium
Pantoja-Feliciano, I. G., Agans, R., Barbato, R. A., Colston, S. M., Goodson, M. S., Hammamieh, R., Hentchel, K. L., Jones, R. M., Karl, J. P., Kokoska, R. J., et al. (2023) · Environmental Microbiome · doi:10.1186/s40793-023-00523-8 · Cited by 3 · see citing works
Self-citationLiu, S., Lin, G., Peng, X., Wu, X., Wang, W., Lin, J., Lin, Y., & Yang, L. (2026) · Frontiers in Nutrition · doi:10.3389/fnut.2026.1623146 · Cited by 1 · see citing works
Zhu, Z., Zhu, X., Chu, Y., Zhang, B., & Chen, Y. (2025) · SSRN Electronic Journal · doi:10.2139/ssrn.5239044
Additional file 1 of Meeting report of the sixth annual tri-service microbiome consortium symposium
Pantoja-Feliciano De Goodfellow, I. G., Agans, R., Barbato, R. A., Colston, S. M., Goodson, M. S., Hammamieh, R., Hentchel, K. L., Jones, R., Karl, J. P., Kokoska, R. J., et al. (2023) · Figshare · doi:10.6084/m9.figshare.23826895
Self-citationJudijanto, L., & Nurhayati, S. (2026) · Multidisciplinary Reviews · doi:10.31893/multirev.2026453
Taverniti, V., Martínez, I., Tavazzani, B., Baeza-Martínez, C., López-García, F., Carazo-Díaz, C., Agüera-Santos, J., Villena, J., Salva, S., Taranto, M. P., et al. (2026) · Microorganisms · doi:10.3390/microorganisms14061270
Na, F., Wang, Y., Zhou, L., Wang, B., Lian, J., & Xu, X. (2026) · Frontiers in Nutrition · doi:10.3389/fnut.2026.1902533
Andreeva, I. V., Andreev, V. A., Dovgan, E. V., Karpova, E. P., Ovchinnikov, A. Y., Selimzyanova, L. R., & Stetsiouk, О. U. (2026) · Clinical Microbiology and Antimicrobial Chemotherapy · doi:10.36488/cmac.2026.2.171-186
- Authors
- Coleman, J. L., Hatch-McChesney, A., Small, S. D., Allen, J. T., Sullo, E., Agans, R. T., Fagnant, H. S., Bukhari, A. S., & Karl, J. P.
- Affiliations
- U.S. Army Research Institute of Environmental Medicine (US)
- George Washington University (US)
- Naval Medical Research Unit DAYTON (US)
- Corresponding author
- Karl, J Philip
- Venue
- Advances in Nutrition
- Publisher
- Elsevier BV
- Published
- 2022-11
- Volume
- 13
- Issue
- 6
- Pages
- 2277-2295
- ISSN
- 2156-5376 (ISSN-L)
- 2161-8313
- PMC
- PMC9776651
- OpenAlex
- W4290973973
- Cited by
- 19
- References
- 81
- Citations by year
- 2026: 5 · 2025: 4 · 2024: 5 · 2023: 5
- FWCI
- 0.32
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Advances in Nutrition (publishedVersion, cc-by-nc-nd)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- OSTI OAI (U.S. Department of Energy Office of Scientific and Technical Information) (submittedVersion)
- Funders
- U.S. Army Research Institute of Environmental Medicine
- Second Decade Society
- U.S. Department of Energy
- Oak Ridge Institute for Science and Education
- U.S. Army Medical Research and Development Command
- Topics
- Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
- Health Sciences › Nursing › Nutrition and Dietetics › Microbial Metabolites in Food Biotechnology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Keywords
- probiotics, prebiotics, synbiotics, respiratory infections, gut microbiota, non-elderly adults, infection incidence, infection duration, infection severity, fermented dairy, physical activity, risk of bias, subgroup heterogeneity, placebo effect
- MeSH terms
- Adult, Humans, Respiratory Tract Infections, Probiotics, PubMed, Prebiotics, Synbiotics
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