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The effect of milk fermented by yogurt cultures plus Lactobacillus casei DN-114001 on the immune response of subjects under academic examination stress

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Summary

Background

A suppressed immune response has been documented in students under examination stress.

Aims

The current study aimed to evaluate the effect of milk fermented with yogurt cultures plus Lactobacillus casei DN-114001 (Actimel®) on the immune system of subjects under academic examination stress.

Methods

University students were allocated to one of two groups, receiving during 6 weeks (3 weeks prior to, as well as the 3-week duration of the examination period) either: a) a glass of semi-skimmed milk each day (control group, n=63) or b) two 100mL portions per day of fermented milk (treatment group, n=73). Anxiety and immunological measurements were monitored at baseline (Phase 0) and study end (Phase 1).

Results

The results were expressed as the differences between the data obtained from Phase 0 and Phase 1. This was calculated by subtracting Phase 1 results from the Phase 0 and it is denominated “Treatment effect”. Mean (± SE) anxiety increased significantly (P<0.05) over the 6-week study in all students, from 40.74±2.50 to 61.19±2.64 (in percentiles). There was no significant treatment effect since this increase was similar in the control and the treatment groups (21.65±5.09 vs 19.14±3.67, respectively). However, there was a significant treatment effect (P<0.05) on the mean change in absolute number of lymphocytes during the 6-week study, which decreased in the control group (–0.04±0.12 cells x 103/mm3) and increased in the treatment group (0.37±0.11 cells x 103/mm3). There was also a significant treatment effect (P<0.05) on the change in absolute numbers of CD56 cells during the 6-week study. Mean absolute CD56 cells significantly decreased (P<0.05) in the control group (–51.97±21.33 cells/mm3),while remaining similar in the treatment group (17.29±17.27 cells/mm3). During the study, mean serum cortisol increased 4.30±0.98 µg/dL in the control group, and 1.75±1.05 µg/dL in the treatment group and no significant differences were found between both values (P=0.062).

Conclusions

Milk fermented with yogurt cultures plus Lactobacillus casei DN-114001 was able to modulate the number of lymphocytes and CD56 cells in subjects under academic examination stress.

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References

  1. Biondi M, Zannino L-G (1997) Psychological stress, neuroimmunomodulation and susceptibility to infectious diseases in animals and man: a review. Psychother Psychosom 66:3–26

    CAS  PubMed  Google Scholar 

  2. Spiegel D, Sephton SE, Terr AI, Stites DP (1998) Effects of psychosocial treatment in prolonging cancer survival may be mediated by neuroimmune pathways. Ann NY Acad Sci 840:674–683

    CAS  PubMed  Google Scholar 

  3. Yang EV, Glaser R (2002) Stress induced immunomodulation and the implications for health. Int Immunopharmacol 2:315–324

    Article  CAS  PubMed  Google Scholar 

  4. Dobbin JP, Harth M, McCain GA, Martin RA, Cousin K (1991) Cytokine production and lymphocyte transformation during stress. Brain Behav Immunity 5:339–348

    Article  CAS  Google Scholar 

  5. Maes M, Van Bockstaele DR, Van Gastel, A et al. (1999) The effects of psychological stress on leukocyte subset distribution in humans: evidence of immune activation. Neuropsychobiology 39:1–9

    Article  CAS  PubMed  Google Scholar 

  6. Kiecolt-Glaser JK, Garner W, Speicher CE, Penn GM, Holliday JE, Glaser R (1984) Psychosocial modifiers of immunocompetance in medical students. Psychosom Med 46:7–14

    CAS  PubMed  Google Scholar 

  7. Guidi L, Tricerri A, Vangeli M, et al. (1999) Neuropeptide Y plasma levels and immunological changes during academic stress. Neuropsychobiology 40:188–195

    Article  CAS  PubMed  Google Scholar 

  8. Sarid O, Anson O, Yaari A, Margalith M (2001) Epstein-Barr virus specific salivary antibodies as related to stress caused by examinations. J Med Virol 64:149–156

    Article  CAS  PubMed  Google Scholar 

  9. Uchakin PN, Tobin B, Cubbage M, Marshall G, Sams C (2001) Immune responsiveness following academic stress in first-year medical students. J Interferon Cytokine Res 21:687–694

    Article  CAS  PubMed  Google Scholar 

  10. Kusnecov AW, Rabin BS (1994) Stressor-induced alterations of immune function: mechanisms and issues. Int Arch Allergy Immunol 105:107–121

    CAS  PubMed  Google Scholar 

  11. Marcos A (2000) Eating disorders: a situation of malnutrition with peculiar changes in the immune system. Eur J Clin Nutr 54(Suppl 1):S61–S64

    Article  CAS  PubMed  Google Scholar 

  12. Paubert-Braquet M (1995) Enhancement of host resistance against Salmonella typhimurium in mice fed a diet supplemented with yogurt or milk fermented with various Lactobacillus casei strains. Int J Immunotherapy 11(4):153–161

    Google Scholar 

  13. Pedone CA, Arnaud CC, Postaire ER, Bouley CF, Reinert P (2000) Multicentric study of the effect of milk fermented by Lactobacillus casei on the incidence of diarrhoea. Int J Clin Pract 54:568–571

    CAS  PubMed  Google Scholar 

  14. Agarwal KN, Bhasin SK (2002) Eur J Clin Nutr 56(Suppl 4):S56–S59

    Article  PubMed  Google Scholar 

  15. Guerin-Danan C, Meslin JC, Chambard A, et al. (2001) Food supplementation with milk fermented by Lactobacillus casei DN114001 protects suckling rats from rotavirus associated diarrhoea. J Nutr 131:111–117

    CAS  PubMed  Google Scholar 

  16. Borruel N, Carol M, Casellas F, et al. (2002) Increased mucosal TNF alpha production in Crohn’s disease can be downregulated ex vivo by probiotic bacteria. Gut 5:659–664

    Article  Google Scholar 

  17. Pujol P, Huguet J, Drobnic F, Banquels M, Ruiz O, Galilea P, Sagarra N, Aguilera S, Burnat A, Mateos JA, Postaire E (2000) The effect of fermented milk containing Lactobacillus casei on the immune response to exercise. Sports Med Training Rehab 00:1–15

    Google Scholar 

  18. Kang D-H, Coe CL, McCarthy DO, Ershler WB (1997) Immune responses to final exams in healthy and asthmatic adolescents. Nursing Res 46:12–19

    Article  CAS  Google Scholar 

  19. Esterling BA, Kiecolt-Glaser JK, Glaser R (1996) Psychosocial modulation of cytokine-induced natural killer cell activity in older adults. Psychosom Med 58:264–272

    CAS  PubMed  Google Scholar 

  20. Solis B, Samartin S, Gomez S, Nova E, de la Rosa B, Marcos A (2002) Probiotics as a help in children suffering from malnutrition and diarrhoea. Eur J Clin Nutr 56(Suppl 3):S57–S59

    Article  CAS  PubMed  Google Scholar 

  21. Solis B, Nova E, Gomez S, et al. (2002) The effect of fermented milk on interferon production in malnourished children and in anorexia nervosa patients undergoing nutritional care. Eur J Clin Nutr 56(Suppl 4):S27–S34

    Article  CAS  PubMed  Google Scholar 

  22. Van de Water J, Keen CL, Gershwin ME (1999) The influence of chronic yogurt consumption on immunity. J Nutr 129:1492S–1495S

    CAS  PubMed  Google Scholar 

  23. Perdigon G, De Moreno D, LeBlanc A, Valdez J, Rachid M (2002) Role of yogurt in the prevention of colon cancer. Eur J Clin Nutr 56(Suppl 3):S65–S68

    Article  CAS  PubMed  Google Scholar 

  24. Meydani SN, Ha W-K (2000) Immunologic effects of yoghurt. Am J Clin Nutr 71:861–872

    CAS  PubMed  Google Scholar 

  25. Nagao F, Nakayama M, Muto T, Okumura K (2000) Effects of a fermented milk drink containing Lactobacillus casei strain Shirota on the immune system in healthy volunteers. Biosci Biotech Biochem 64:2706–2708

    CAS  Google Scholar 

  26. Hori T, Kiyoshima J, Shida K, Yasui H (2002) Augmentation of cellular immunity and reduction of influenza virus titer in aged mice fed Lactobacillus casei strain Shirota. Clin Diagn Lab Immunol 9:105–108

    Article  PubMed  Google Scholar 

  27. Takagi A, Matsuzaki T, Sato M, Nomoto K, Morotomi M, Yokokura T (2001) Enhancement of natural killer cytotoxicity delayed murine carcinogenesis by a probiotic microorganism. Carcinogenesis 22:599–605

    Article  CAS  PubMed  Google Scholar 

  28. Aattour N, Bouras M, Tome D, Marcos A, Lemonnier D (2002) Oral ingestion of lactic acid bacteria by rats increases lymphocyte proliferation and interferon gamma production. Br J Nutr 87:367–373

    Article  PubMed  Google Scholar 

  29. Solis Pereyra B, Aattouri N, Lemonnier D (1997) Role of food in the stimulation of cytokine production. Am J Clin Nutr 66:521S–525S

    CAS  PubMed  Google Scholar 

  30. Gill HS, Rutherford KJ (2001) Immune enhancement conferred by oral delivery of Lactobacillus rhamnosus HN001 in different milk-based substrates. J Dairy Res 68:611–616

    Article  CAS  PubMed  Google Scholar 

  31. Campbell CG, Chew BP, Luedecke LO, Shultz TD (2000) Yogurt consumption does not enhance immune function in healthy premenopausal women. Nutr Cancer 37:27–35

    Article  CAS  PubMed  Google Scholar 

  32. Pestka JJ, Ha CL, Warner RW, Lee JH, Ustunol Z (2001) Effects of ingestion of yogurts containing Bifidobacterium and Lactobacillus acidophilus on spleen and peyers patch lymphocyte populations in the mouse. J Food Protect 64:392–395

    CAS  Google Scholar 

  33. Maassen CB, van Holten-Neelen C, Balk F, et al. (2000) Strain dependent induction of cytokine profiles in the gut by orally administered Lactobacillus strains. Vaccine 18:2613–2623

    Article  CAS  PubMed  Google Scholar 

  34. Kano H, Kaneko T, Kaminogawa S (2002) Oral intake of Lactobacillus delbruckii subsp. bulgaricus OLL1073R-1 prevents collagen induced arthritis in mice. J Food Protect 65:153–160

    Google Scholar 

  35. Cross ML, Stevenson LM, Gill HS (2001) Anti-allergy properties of fermented foods: an important immunoregulatory mechanism of lactic acid bacteria? Int Immunopharmacol 1:891–901

    Article  CAS  PubMed  Google Scholar 

  36. Malarkey WB, Pearl DK, Demers LM, Kiecolt-Glaser JK, Glaser R (1995) Influence of academic stress and season on 24-hour mean concentrations of ACTH, cortisol and b endorphin. Psychoneuroendocrinology 20:499–508

    Article  CAS  PubMed  Google Scholar 

  37. Christensen NJ, Jensen EW (1994) Effect of psychosocial stress and age on plasma norepinephrine levels: a review. Psychosomatic Med 56:77–83

    CAS  Google Scholar 

  38. Strausbaugh HJ, Dallman MF, Levine JD (1999) Repeated but not acute stress suppresses inflammatory plasma extravasation. Proc Natl Acad Sci USA 96:14629–14634

    Article  CAS  PubMed  Google Scholar 

  39. Zhou D, Kusnecov AW, Shurin MR, De-Paoli M, Rabin DS (1993) Exposure to physical and psychological stressors elevates plasma interleukin 6: relationship to the activation of the hypothalamic-pituitary-adrenal axis. Endocrinology 133:2523–2530

    Article  CAS  PubMed  Google Scholar 

  40. Dhabar FS (2000) Acute stress enhances while chronic stress suppresses skin immunity. Ann NY Acad Sci 917:876–893

    PubMed  Google Scholar 

  41. Dhabar FS, McEwan BS (1996) Stress induced enhancement of antigen specific cell mediated immunity. J Immunol 156:2608–2615

    PubMed  Google Scholar 

  42. Lu ZW, Hayley S, Ravindran AV, Merali Z, Anisman H (1999) Influence of psychosocial, psychogenic and neurogenic stressors on several aspects of immune functioning in mice. Stress 3:55–70

    Google Scholar 

  43. Filaretova L, Maltcev N, Bogdanov A, Levkovich Y (1999) Role of gastric microcirculation in the gastroprotection by glucocorticoids released during water restraint stress in rats. Chin J Physiol 42:145–152

    CAS  PubMed  Google Scholar 

  44. Gitlin N, Ginn P, Kobayashi K, Arakawa A (1988) The relationship between plasma cortisol and gastric mucosa prostaglandin levels in rats with stress ulcers. Alim Pharmacol Ther 2:213–22

    CAS  Google Scholar 

  45. Bailey MT,Coe CL (1999) Maternal separation disrupts the integrity of the intestinal microflora in infant rhesus monkeys. Developtl Psychobiol 35:146–155

    CAS  Google Scholar 

  46. Zomborszky Z, Feher T, Horn E, Poteczin E, Tuboly S, Kovacs-Zomborszky M (1996) Comparison of some blood parameters of captured and farmed red deer (Cervus Elaphus) hinds. Acta Veterin Hungarica 44:433–441

    CAS  Google Scholar 

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Authors and Affiliations

  1. Grupo Inmunonutrición, Depo. de Metabolismo y Nutrición, Instituto del Frío, CSIC, C/Jose Antonio Novais 10, 28040, Madrid, Spain

    Ascensión Marcos PhD, Julia Wärnberg BSc, Esther Nova PhD, Sonia Gómez PhD & Rocío Alvarez BSc

  2. Unidad de Citometría Centro Nacional de Investigaciones Cardiovasculares, Instituto de Salud Carlos III, Madrid, Spain

    Alberto Alvarez PhD

  3. Coordinación Científica, Danone S. A., Barcelona, Spain

    José A. Mateos PhD & José M. Cobo PhD

Authors
  1. Ascensión Marcos PhD
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  2. Julia Wärnberg BSc
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  3. Esther Nova PhD
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  4. Sonia Gómez PhD
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Correspondence to Ascensión Marcos PhD.

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Marcos, A., Wärnberg, J., Nova, E. et al. The effect of milk fermented by yogurt cultures plus Lactobacillus casei DN-114001 on the immune response of subjects under academic examination stress. Eur J Nutr 43, 381–389 (2004). https://doi.org/10.1007/s00394-004-0517-8

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  • DOI: https://doi.org/10.1007/s00394-004-0517-8

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