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Published in: European Journal of Nutrition 1/2017

Open Access 01-02-2017 | Original Contribution

Daily intake of fermented milk with Lactobacillus casei strain Shirota reduces the incidence and duration of upper respiratory tract infections in healthy middle-aged office workers

Authors: Kan Shida, Tadashi Sato, Ryoko Iizuka, Ryotaro Hoshi, Osamu Watanabe, Tomoki Igarashi, Kouji Miyazaki, Masanobu Nanno, Fumiyasu Ishikawa

Published in: European Journal of Nutrition | Issue 1/2017

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Abstract

Purpose

Although several studies have demonstrated the efficacy of probiotics for preventing upper respiratory tract infections (URTIs) in at-risk populations, including children and the elderly, few studies have investigated the efficacy of probiotics in healthy adults living normal, everyday lives. Thus, we tried to evaluate the effects of Lactobacillus casei strain Shirota-fermented milk (LcS-FM) on the incidence of URTIs in healthy middle-aged office workers.

Methods

In a randomized controlled trial, 96 eligible male workers aged 30–49 years consumed LcS-FM containing 1.0 × 1011 viable LcS cells or control milk (CM) once daily for 12 weeks during the winter season. URTI episodes were evaluated by a physician via a questionnaire of URTI symptoms.

Results

The incidence of URTIs during the intervention period was significantly lower in the LcS-FM group than in the CM group (22.4 vs. 53.2 %, P = 0.002). The time-to-event analysis showed that the LcS-FM group had a significantly higher URTI-free rate than the CM group over the test period (log-rank test: χ 2 11.25, P = 0.0008). The cumulative number of URTI episodes and cumulative days with URTI symptoms per person was lower in the LcS-FM group, and the duration per episode was shorter. Inhibition of both reductions in NK cell activity in peripheral blood mononuclear cells and increases in salivary cortisol levels was observed in the LcS-FM group.

Conclusion

The results suggest that the daily intake of fermented milk with LcS may reduce the risk of URTIs in healthy middle-aged office workers, probably through modulation of the immune system.
Literature
1.
go back to reference Neish AS (2009) Microbes in gastrointestinal health and disease. Gastroenterology 136:65–80CrossRef Neish AS (2009) Microbes in gastrointestinal health and disease. Gastroenterology 136:65–80CrossRef
2.
go back to reference Fuller R (1989) Probiotics in man and animals. J Appl Bacteriol 66:365–378CrossRef Fuller R (1989) Probiotics in man and animals. J Appl Bacteriol 66:365–378CrossRef
3.
go back to reference Shida K, Nanno M (2008) Probiotics and immunology: separating the wheat from the chaff. Trends Immunol 29:565–573CrossRef Shida K, Nanno M (2008) Probiotics and immunology: separating the wheat from the chaff. Trends Immunol 29:565–573CrossRef
4.
go back to reference Mitsuoka T (2014) Development of functional food. Biosci Microbiota Food Health 33:117–128CrossRef Mitsuoka T (2014) Development of functional food. Biosci Microbiota Food Health 33:117–128CrossRef
5.
go back to reference Nomoto K (2005) Prevention of infections by probiotics. J Biosci Bioeng 100:583–592CrossRef Nomoto K (2005) Prevention of infections by probiotics. J Biosci Bioeng 100:583–592CrossRef
6.
go back to reference Alvarez-Olmos MI, Oberhelman RA (2001) Probiotic agents and infectious diseases: a modern perspective on a traditional therapy. Clin Infect Dis 32:1567–1576CrossRef Alvarez-Olmos MI, Oberhelman RA (2001) Probiotic agents and infectious diseases: a modern perspective on a traditional therapy. Clin Infect Dis 32:1567–1576CrossRef
7.
go back to reference King S, Glanville J, Sanders ME, Fitzgerald A, Varley D (2014) Effectiveness of probiotics on the duration of illness in healthy children and adults who develop common acute respiratory infectious conditions: a systematic review and meta-analysis. Br J Nutr 112:41–54CrossRef King S, Glanville J, Sanders ME, Fitzgerald A, Varley D (2014) Effectiveness of probiotics on the duration of illness in healthy children and adults who develop common acute respiratory infectious conditions: a systematic review and meta-analysis. Br J Nutr 112:41–54CrossRef
9.
go back to reference Taipale T, Pienihakkinen K, Isolauri E, Larsen C, Brockmann E, Alanen P, Jokela J, Soderling E (2011) Bifidobacterium animalis subsp. lactis BB-12 in reducing the risk of infections in infancy. Br J Nutr 105:409–416CrossRef Taipale T, Pienihakkinen K, Isolauri E, Larsen C, Brockmann E, Alanen P, Jokela J, Soderling E (2011) Bifidobacterium animalis subsp. lactis BB-12 in reducing the risk of infections in infancy. Br J Nutr 105:409–416CrossRef
10.
go back to reference Merenstein D, Murphy M, Fokar A, Hernandez RK, Park H, Nsouli H, Sanders ME, Davis BA, Niborski V, Tondu F, Shara NM (2010) Use of a fermented dairy probiotic drink containing Lactobacillus casei (DN-114 001) to decrease the rate of illness in kids: the DRINK study. A patient-oriented, double-blind, cluster-randomized, placebo-controlled, clinical trial. Eur J Clin Nutr 64:669–677CrossRef Merenstein D, Murphy M, Fokar A, Hernandez RK, Park H, Nsouli H, Sanders ME, Davis BA, Niborski V, Tondu F, Shara NM (2010) Use of a fermented dairy probiotic drink containing Lactobacillus casei (DN-114 001) to decrease the rate of illness in kids: the DRINK study. A patient-oriented, double-blind, cluster-randomized, placebo-controlled, clinical trial. Eur J Clin Nutr 64:669–677CrossRef
11.
go back to reference Waki N, Matsumoto M, Fukui Y, Suganuma H (2014) Effects of probiotic Lactobacillus brevis KB290 on incidence of influenza infection among schoolchildren: an open-label pilot study. Lett Appl Microbiol 59:565–571CrossRef Waki N, Matsumoto M, Fukui Y, Suganuma H (2014) Effects of probiotic Lactobacillus brevis KB290 on incidence of influenza infection among schoolchildren: an open-label pilot study. Lett Appl Microbiol 59:565–571CrossRef
12.
go back to reference Makino S, Ikegami S, Kume A, Horiuchi H, Sasaki H, Orii N (2010) Reducing the risk of infection in the elderly by dietary intake of yoghurt fermented with Lactobacillus delbrueckii ssp. bulgaricus OLL1073R-1. Br J Nutr 104:998–1006CrossRef Makino S, Ikegami S, Kume A, Horiuchi H, Sasaki H, Orii N (2010) Reducing the risk of infection in the elderly by dietary intake of yoghurt fermented with Lactobacillus delbrueckii ssp. bulgaricus OLL1073R-1. Br J Nutr 104:998–1006CrossRef
13.
go back to reference Tubelius P, Stan V, Zachrisson A (2005) Increasing work-place healthiness with the probiotic Lactobacillus reuteri: a randomised, double-blind placebo-controlled study. Environ Health 4:25CrossRef Tubelius P, Stan V, Zachrisson A (2005) Increasing work-place healthiness with the probiotic Lactobacillus reuteri: a randomised, double-blind placebo-controlled study. Environ Health 4:25CrossRef
14.
go back to reference Guillemard E, Tanguy J, Flavigny A, de la Motte S, Schrezenmeir J (2010) Effects of consumption of a fermented dairy product containing the probiotic Lactobacillus casei DN-114 001 on common respiratory and gastrointestinal infections in shift workers in a randomized controlled trial. J Am Coll Nutr 29:455–468CrossRef Guillemard E, Tanguy J, Flavigny A, de la Motte S, Schrezenmeir J (2010) Effects of consumption of a fermented dairy product containing the probiotic Lactobacillus casei DN-114 001 on common respiratory and gastrointestinal infections in shift workers in a randomized controlled trial. J Am Coll Nutr 29:455–468CrossRef
15.
go back to reference Biron CA, Nguyen KB, Pien GC, Cousens LP, Salazar-Mather TP (1999) Natural killer cells in antiviral defense: function and regulation by innate cytokines. Annu Rev Immunol 17:189–220CrossRef Biron CA, Nguyen KB, Pien GC, Cousens LP, Salazar-Mather TP (1999) Natural killer cells in antiviral defense: function and regulation by innate cytokines. Annu Rev Immunol 17:189–220CrossRef
16.
go back to reference Neville V, Gleeson M, Folland JP (2008) Salivary IgA as a risk factor for upper respiratory infections in elite professional athletes. Med Sci Sports Exerc 40:1228–1236CrossRef Neville V, Gleeson M, Folland JP (2008) Salivary IgA as a risk factor for upper respiratory infections in elite professional athletes. Med Sci Sports Exerc 40:1228–1236CrossRef
17.
go back to reference Morimoto K, Takeshita T, Inoue-Sakurai C, Maruyama S (2001) Lifestyles and mental health status are associated with natural killer cell and lymphokine-activated killer cell activities. Sci Total Environ 270:3–11CrossRef Morimoto K, Takeshita T, Inoue-Sakurai C, Maruyama S (2001) Lifestyles and mental health status are associated with natural killer cell and lymphokine-activated killer cell activities. Sci Total Environ 270:3–11CrossRef
18.
go back to reference Nanno M, Kato I, Kobayashi T, Shida K (2011) Biological effects of probiotics: what impact does Lactobacillus casei Shirota have on us? Int J Immunopathol Pharmacol 24:45S–50S Nanno M, Kato I, Kobayashi T, Shida K (2011) Biological effects of probiotics: what impact does Lactobacillus casei Shirota have on us? Int J Immunopathol Pharmacol 24:45S–50S
19.
go back to reference Kotani Y, Shinkai S, Okamatsu H, Toba M, Ogawa K, Yoshida H, Fukaya T, Fujiwara Y, Chaves PH, Kakumoto K, Kohda N (2010) Oral intake of Lactobacillus pentosus strain b240 accelerates salivary immunoglobulin A secretion in the elderly: a randomized, placebo-controlled, double-blind trial. Immun Ageing 7:11CrossRef Kotani Y, Shinkai S, Okamatsu H, Toba M, Ogawa K, Yoshida H, Fukaya T, Fujiwara Y, Chaves PH, Kakumoto K, Kohda N (2010) Oral intake of Lactobacillus pentosus strain b240 accelerates salivary immunoglobulin A secretion in the elderly: a randomized, placebo-controlled, double-blind trial. Immun Ageing 7:11CrossRef
20.
go back to reference Gleeson M, Bishop NC, Oliveira M, Tauler P (2011) Daily probiotic’s (Lactobacillus casei Shirota) reduction of infection incidence in athletes. Int J Sport Nutr Exerc Metab 21:55–64CrossRef Gleeson M, Bishop NC, Oliveira M, Tauler P (2011) Daily probiotic’s (Lactobacillus casei Shirota) reduction of infection incidence in athletes. Int J Sport Nutr Exerc Metab 21:55–64CrossRef
21.
go back to reference Matsumoto K, Takada T, Shimizu K, Moriyama K, Kawakami K, Hirano K, Kajimoto O, Nomoto K (2010) Effects of a probiotic fermented milk beverage containing Lactobacillus casei strain Shirota on defecation frequency, intestinal microbiota, and the intestinal environment of healthy individuals with soft stools. J Biosci Bioeng 110:547–552CrossRef Matsumoto K, Takada T, Shimizu K, Moriyama K, Kawakami K, Hirano K, Kajimoto O, Nomoto K (2010) Effects of a probiotic fermented milk beverage containing Lactobacillus casei strain Shirota on defecation frequency, intestinal microbiota, and the intestinal environment of healthy individuals with soft stools. J Biosci Bioeng 110:547–552CrossRef
22.
go back to reference Nanno M, Matsumoto S, Shida S (2012) Lactobacillus casei strain Shirota: benefits based on a long history of usage. In: Nair GB, Takeda Y (eds) Health impact of probiotics. Elsevier, New Delhi, pp 85–98 Nanno M, Matsumoto S, Shida S (2012) Lactobacillus casei strain Shirota: benefits based on a long history of usage. In: Nair GB, Takeda Y (eds) Health impact of probiotics. Elsevier, New Delhi, pp 85–98
23.
go back to reference Shida K, Nomoto K (2013) Probiotics as efficient immunopotentiators: translational role in cancer prevention. Indian J Med Res 138:808–814 Shida K, Nomoto K (2013) Probiotics as efficient immunopotentiators: translational role in cancer prevention. Indian J Med Res 138:808–814
24.
go back to reference Fujita R, Iimuro S, Shinozaki T, Sakamaki K, Uemura Y, Takeuchi A, Matsuyama Y, Ohashi Y (2013) Decreased duration of acute upper respiratory tract infections with daily intake of fermented milk: a multicenter, double-blinded, randomized comparative study in users of day care facilities for the elderly population. Am J Infect Control 41:1231–1235CrossRef Fujita R, Iimuro S, Shinozaki T, Sakamaki K, Uemura Y, Takeuchi A, Matsuyama Y, Ohashi Y (2013) Decreased duration of acute upper respiratory tract infections with daily intake of fermented milk: a multicenter, double-blinded, randomized comparative study in users of day care facilities for the elderly population. Am J Infect Control 41:1231–1235CrossRef
25.
go back to reference Van Puyenbroeck K, Hens N, Coenen S, Michiels B, Beunckens C, Molenberghs G, Van Royen P, Verhoeven V (2012) Efficacy of daily intake of Lactobacillus casei Shirota on respiratory symptoms and influenza vaccination immune response: a randomized, double-blind, placebo-controlled trial in healthy elderly nursing home residents. Am J Clin Nutr 95:1165–1171CrossRef Van Puyenbroeck K, Hens N, Coenen S, Michiels B, Beunckens C, Molenberghs G, Van Royen P, Verhoeven V (2012) Efficacy of daily intake of Lactobacillus casei Shirota on respiratory symptoms and influenza vaccination immune response: a randomized, double-blind, placebo-controlled trial in healthy elderly nursing home residents. Am J Clin Nutr 95:1165–1171CrossRef
26.
go back to reference Berggren A, Lazou Ahren I, Larsson N, Onning G (2011) Randomised, double-blind and placebo-controlled study using new probiotic lactobacilli for strengthening the body immune defence against viral infections. Eur J Nutr 50:203–210CrossRef Berggren A, Lazou Ahren I, Larsson N, Onning G (2011) Randomised, double-blind and placebo-controlled study using new probiotic lactobacilli for strengthening the body immune defence against viral infections. Eur J Nutr 50:203–210CrossRef
27.
go back to reference West NP, Horn PL, Pyne DB, Gebski VJ, Lahtinen SJ, Fricker PA, Cripps AW (2013) Probiotic supplementation for respiratory and gastrointestinal illness symptoms in healthy physically active individuals. Clin Nutr 33:581–587CrossRef West NP, Horn PL, Pyne DB, Gebski VJ, Lahtinen SJ, Fricker PA, Cripps AW (2013) Probiotic supplementation for respiratory and gastrointestinal illness symptoms in healthy physically active individuals. Clin Nutr 33:581–587CrossRef
28.
go back to reference de Vrese M, Winkler P, Rautenberg P, Harder T, Noah C, Laue C, Ott S, Hampe J, Schreiber S, Heller K, Schrezenmeir J (2006) Probiotic bacteria reduced duration and severity but not the incidence of common cold episodes in a double blind, randomized, controlled trial. Vaccine 24:6670–6674CrossRef de Vrese M, Winkler P, Rautenberg P, Harder T, Noah C, Laue C, Ott S, Hampe J, Schreiber S, Heller K, Schrezenmeir J (2006) Probiotic bacteria reduced duration and severity but not the incidence of common cold episodes in a double blind, randomized, controlled trial. Vaccine 24:6670–6674CrossRef
29.
go back to reference Winkler P, de Vrese M, Laue C, Schrezenmeir J (2005) Effect of a dietary supplement containing probiotic bacteria plus vitamins and minerals on common cold infections and cellular immune parameters. Int J Clin Pharmacol Ther 43:318–326CrossRef Winkler P, de Vrese M, Laue C, Schrezenmeir J (2005) Effect of a dietary supplement containing probiotic bacteria plus vitamins and minerals on common cold infections and cellular immune parameters. Int J Clin Pharmacol Ther 43:318–326CrossRef
30.
go back to reference Haywood BA, Black KE, Baker D, McGarvey J, Healey P, Brown RC (2014) Probiotic supplementation reduces the duration and incidence of infections but not severity in elite rugby union players. J Sci Med Sport 17:356–360CrossRef Haywood BA, Black KE, Baker D, McGarvey J, Healey P, Brown RC (2014) Probiotic supplementation reduces the duration and incidence of infections but not severity in elite rugby union players. J Sci Med Sport 17:356–360CrossRef
31.
go back to reference Spanhaak S, Havenaar R, Schaafsma G (1998) The effect of consumption of milk fermented by Lactobacillus casei strain Shirota on the intestinal microflora and immune parameters in humans. Eur J Clin Nutr 52:899–907CrossRef Spanhaak S, Havenaar R, Schaafsma G (1998) The effect of consumption of milk fermented by Lactobacillus casei strain Shirota on the intestinal microflora and immune parameters in humans. Eur J Clin Nutr 52:899–907CrossRef
32.
go back to reference Shida K, Suzuki T, Kiyoshima-Shibata J, Shimada S, Nanno M (2006) Essential roles of monocytes in stimulating human peripheral blood mononuclear cells with Lactobacillus casei to produce cytokines and augment natural killer cell activity. Clin Vaccine Immunol 13:997–1003CrossRef Shida K, Suzuki T, Kiyoshima-Shibata J, Shimada S, Nanno M (2006) Essential roles of monocytes in stimulating human peripheral blood mononuclear cells with Lactobacillus casei to produce cytokines and augment natural killer cell activity. Clin Vaccine Immunol 13:997–1003CrossRef
33.
go back to reference Takeda K, Suzuki T, Shimada SI, Shida K, Nanno M, Okumura K (2006) Interleukin-12 is involved in the enhancement of human natural killer cell activity by Lactobacillus casei Shirota. Clin Exp Immunol 146:109–115CrossRef Takeda K, Suzuki T, Shimada SI, Shida K, Nanno M, Okumura K (2006) Interleukin-12 is involved in the enhancement of human natural killer cell activity by Lactobacillus casei Shirota. Clin Exp Immunol 146:109–115CrossRef
34.
go back to reference Mavoungou E, Bouyou-Akotet MK, Kremsner PG (2005) Effects of prolactin and cortisol on natural killer (NK) cell surface expression and function of human natural cytotoxicity receptors (NKp46, NKp44 and NKp30). Clin Exp Immunol 139:287–296CrossRef Mavoungou E, Bouyou-Akotet MK, Kremsner PG (2005) Effects of prolactin and cortisol on natural killer (NK) cell surface expression and function of human natural cytotoxicity receptors (NKp46, NKp44 and NKp30). Clin Exp Immunol 139:287–296CrossRef
35.
go back to reference Langkamp-Henken B, Rowe CC, Ford AL, Christman MC, Nieves C Jr, Khouri L, Specht GJ, Girard SA, Spaiser SJ, Dahl WJ (2015) Bifidobacterium bifidum R0071 results in a greater proportion of healthy days and a lower percentage of academically stressed students reporting a day of cold/flu: a randomised, double-blind, placebo-controlled study. Br J Nutr 113:426–434CrossRef Langkamp-Henken B, Rowe CC, Ford AL, Christman MC, Nieves C Jr, Khouri L, Specht GJ, Girard SA, Spaiser SJ, Dahl WJ (2015) Bifidobacterium bifidum R0071 results in a greater proportion of healthy days and a lower percentage of academically stressed students reporting a day of cold/flu: a randomised, double-blind, placebo-controlled study. Br J Nutr 113:426–434CrossRef
36.
go back to reference Hughes C, Davoodi-Semiromi Y, Colee JC, Culpepper T, Dahl WJ, Mai V, Christman MC, Langkamp-Henken B (2011) Galactooligosaccharide supplementation reduces stress-induced gastrointestinal dysfunction and days of cold or flu: a randomized, double-blind, controlled trial in healthy university students. Am J Clin Nutr 93:1305–1311CrossRef Hughes C, Davoodi-Semiromi Y, Colee JC, Culpepper T, Dahl WJ, Mai V, Christman MC, Langkamp-Henken B (2011) Galactooligosaccharide supplementation reduces stress-induced gastrointestinal dysfunction and days of cold or flu: a randomized, double-blind, controlled trial in healthy university students. Am J Clin Nutr 93:1305–1311CrossRef
37.
go back to reference Wang Y, Kasper LH (2014) The role of microbiome in central nervous system disorders. Brain Behav Immun 38:1–12CrossRef Wang Y, Kasper LH (2014) The role of microbiome in central nervous system disorders. Brain Behav Immun 38:1–12CrossRef
38.
go back to reference Tanida M, Nagai K (2011) Electrophysiological analysis of the mechanism of autonomic action by lactobacilli. Biosci Microflora 30:99–109CrossRef Tanida M, Nagai K (2011) Electrophysiological analysis of the mechanism of autonomic action by lactobacilli. Biosci Microflora 30:99–109CrossRef
39.
go back to reference Tanida M, Imanishi K, Akashi H, Kurata Y, Chonan O, Naito E, Kunihiro S, Kawai M, Kato-Kataoka A, Shibamoto T (2014) Injection of Lactobacillus casei strain Shirota affects autonomic nerve activities in a tissue-specific manner, and regulates glucose and lipid metabolism in rats. J Diabetes Investig 5:153–161CrossRef Tanida M, Imanishi K, Akashi H, Kurata Y, Chonan O, Naito E, Kunihiro S, Kawai M, Kato-Kataoka A, Shibamoto T (2014) Injection of Lactobacillus casei strain Shirota affects autonomic nerve activities in a tissue-specific manner, and regulates glucose and lipid metabolism in rats. J Diabetes Investig 5:153–161CrossRef
40.
go back to reference Segerstrom SC, Miller GE (2004) Psychological stress and the human immune system: a meta-analytic study of 30 years of inquiry. Psychol Bull 130:601–630CrossRef Segerstrom SC, Miller GE (2004) Psychological stress and the human immune system: a meta-analytic study of 30 years of inquiry. Psychol Bull 130:601–630CrossRef
Metadata
Title
Daily intake of fermented milk with Lactobacillus casei strain Shirota reduces the incidence and duration of upper respiratory tract infections in healthy middle-aged office workers
Authors
Kan Shida
Tadashi Sato
Ryoko Iizuka
Ryotaro Hoshi
Osamu Watanabe
Tomoki Igarashi
Kouji Miyazaki
Masanobu Nanno
Fumiyasu Ishikawa
Publication date
01-02-2017
Publisher
Springer Berlin Heidelberg
Published in
European Journal of Nutrition / Issue 1/2017
Print ISSN: 1436-6207
Electronic ISSN: 1436-6215
DOI
https://doi.org/10.1007/s00394-015-1056-1

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