European Journal of Nutrition

, Volume 43, Issue 6, pp 381–389 | Cite as

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

  • Ascensión Marcos
  • Julia Wärnberg
  • Esther Nova
  • Sonia Gómez
  • Alberto Alvarez
  • Rocío Alvarez
  • José A. Mateos
  • José M. Cobo
ORIGINAL CONTRIBUTION

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.

Key words

fermented milk Lactobacillus casei DN114001 examination stress immunomodulation cortisol 

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References

  1. 1.
    Biondi M, Zannino L-G (1997) Psychological stress, neuroimmunomodulation and susceptibility to infectious diseases in animals and man: a review. Psychother Psychosom 66:3–26PubMedGoogle Scholar
  2. 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 840:674–683PubMedGoogle Scholar
  3. 3.
    Yang EV, Glaser R (2002) Stress induced immunomodulation and the implications for health. Int Immunopharmacol 2:315–324CrossRefPubMedGoogle Scholar
  4. 4.
    Dobbin JP, Harth M, McCain GA, Martin RA, Cousin K (1991) Cytokine production and lymphocyte transformation during stress. Brain Behav Immunity 5:339–348CrossRefGoogle Scholar
  5. 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 39:1–9CrossRefPubMedGoogle Scholar
  6. 6.
    Kiecolt-Glaser JK, Garner W, Speicher CE, Penn GM, Holliday JE, Glaser R (1984) Psychosocial modifiers of immunocompetance in medical students. Psychosom Med 46:7–14PubMedGoogle Scholar
  7. 7.
    Guidi L, Tricerri A, Vangeli M, et al. (1999) Neuropeptide Y plasma levels and immunological changes during academic stress. Neuropsychobiology 40:188–195CrossRefPubMedGoogle Scholar
  8. 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 64:149–156CrossRefPubMedGoogle Scholar
  9. 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 21:687–694CrossRefPubMedGoogle Scholar
  10. 10.
    Kusnecov AW, Rabin BS (1994) Stressor-induced alterations of immune function: mechanisms and issues. Int Arch Allergy Immunol 105:107–121PubMedGoogle Scholar
  11. 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–S64CrossRefPubMedGoogle Scholar
  12. 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):153–161Google Scholar
  13. 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 54:568–571PubMedGoogle Scholar
  14. 14.
    Agarwal KN, Bhasin SK (2002) Eur J Clin Nutr 56(Suppl 4):S56–S59CrossRefPubMedGoogle Scholar
  15. 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 131:111–117PubMedGoogle Scholar
  16. 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 5:659–664CrossRefGoogle Scholar
  17. 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 00:1–15Google Scholar
  18. 18.
    Kang D-H, Coe CL, McCarthy DO, Ershler WB (1997) Immune responses to final exams in healthy and asthmatic adolescents. Nursing Res 46:12–19CrossRefGoogle Scholar
  19. 19.
    Esterling BA, Kiecolt-Glaser JK, Glaser R (1996) Psychosocial modulation of cytokine-induced natural killer cell activity in older adults. Psychosom Med 58:264–272PubMedGoogle Scholar
  20. 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–S59CrossRefPubMedGoogle Scholar
  21. 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–S34CrossRefPubMedGoogle Scholar
  22. 22.
    Van de Water J, Keen CL, Gershwin ME (1999) The influence of chronic yogurt consumption on immunity. J Nutr 129:1492S–1495SPubMedGoogle Scholar
  23. 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–S68CrossRefPubMedGoogle Scholar
  24. 24.
    Meydani SN, Ha W-K (2000) Immunologic effects of yoghurt. Am J Clin Nutr 71:861–872PubMedGoogle Scholar
  25. 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 64:2706–2708Google Scholar
  26. 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 9:105–108CrossRefPubMedGoogle Scholar
  27. 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 22:599–605CrossRefPubMedGoogle Scholar
  28. 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 87:367–373CrossRefPubMedGoogle Scholar
  29. 29.
    Solis Pereyra B, Aattouri N, Lemonnier D (1997) Role of food in the stimulation of cytokine production. Am J Clin Nutr 66:521S–525SPubMedGoogle Scholar
  30. 30.
    Gill HS, Rutherford KJ (2001) Immune enhancement conferred by oral delivery of Lactobacillus rhamnosus HN001 in different milk-based substrates. J Dairy Res 68:611–616CrossRefPubMedGoogle Scholar
  31. 31.
    Campbell CG, Chew BP, Luedecke LO, Shultz TD (2000) Yogurt consumption does not enhance immune function in healthy premenopausal women. Nutr Cancer 37:27–35CrossRefPubMedGoogle Scholar
  32. 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 64:392–395Google Scholar
  33. 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 18:2613–2623CrossRefPubMedGoogle Scholar
  34. 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 65:153–160Google Scholar
  35. 35.
    Cross ML, Stevenson LM, Gill HS (2001) Anti-allergy properties of fermented foods: an important immunoregulatory mechanism of lactic acid bacteria? Int Immunopharmacol 1:891–901CrossRefPubMedGoogle Scholar
  36. 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 20:499–508CrossRefPubMedGoogle Scholar
  37. 37.
    Christensen NJ, Jensen EW (1994) Effect of psychosocial stress and age on plasma norepinephrine levels: a review. Psychosomatic Med 56:77–83Google Scholar
  38. 38.
    Strausbaugh HJ, Dallman MF, Levine JD (1999) Repeated but not acute stress suppresses inflammatory plasma extravasation. Proc Natl Acad Sci USA 96:14629–14634CrossRefPubMedGoogle Scholar
  39. 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 133:2523–2530CrossRefPubMedGoogle Scholar
  40. 40.
    Dhabar FS (2000) Acute stress enhances while chronic stress suppresses skin immunity. Ann NY Acad Sci 917:876–893PubMedGoogle Scholar
  41. 41.
    Dhabar FS, McEwan BS (1996) Stress induced enhancement of antigen specific cell mediated immunity. J Immunol 156:2608–2615PubMedGoogle Scholar
  42. 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 3:55–70Google Scholar
  43. 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 42:145–152PubMedGoogle Scholar
  44. 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 2:213–22Google Scholar
  45. 45.
    Bailey MT,Coe CL (1999) Maternal separation disrupts the integrity of the intestinal microflora in infant rhesus monkeys. Developtl Psychobiol 35:146–155Google Scholar
  46. 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 44:433–441Google Scholar

Copyright information

© Steinkopff Verlag 2004

Authors and Affiliations

  • Ascensión Marcos
    • 1
  • Julia Wärnberg
    • 1
  • Esther Nova
    • 1
  • Sonia Gómez
    • 1
  • Alberto Alvarez
    • 2
  • Rocío Alvarez
    • 1
  • José A. Mateos
    • 3
  • José M. Cobo
    • 3
  1. 1.Grupo Inmunonutrición, Depo. de Metabolismo y NutriciónInstituto del Frío, CSICMadridSpain
  2. 2.Unidad de Citometría Centro Nacional de Investigaciones CardiovascularesInstituto de Salud Carlos IIIMadridSpain
  3. 3.Coordinación CientíficaDanone S. A.BarcelonaSpain

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