Induction of inflammation as a possible mechanism of probiotic effect in atopic eczema–dermatitis syndrome

doi:10.1016/j.jaci.2005.03.047

Journal of Allergy and Clinical Immunology

Volume 115, Issue 6, June 2005, Pages 1254-1259

https://doi.org/10.1016/j.jaci.2005.03.047 Get rights and content

Background

The immunomodulating mechanisms of Lactobacillus GG (LGG) and other probiotics are poorly understood.

Objective

We studied in vivo the immunologic effects of probiotics in infants with atopic eczema–dermatitis syndrome (AEDS) and cow's milk allergy (CMA).

Methods

Two hundred thirty infants with AEDS and suspected CMA received, concomitant with elimination diet, either LGG, a mixture of 4 probiotic strains (MIX), or placebo for 4 weeks. All available paired pretreatment and posttreatment plasma samples (n = 132) were analyzed for concentrations of IL-2, IL-4, IL-6, IL-10, TNF-α, IFN-γ, soluble intercellular adhesion molecule 1, soluble E-selectin, TGF-β1, TGF-β2, and C-reactive protein.

Results

In infants with IgE-associated AEDS, treatment with LGG induced higher C-reactive protein levels than in the placebo group (geometric mean, 0.83 μg/mL [95% CI, 0.56-0.81] vs 0.42 μg/mL [95% CI, 0.27-0.65]; P = .021). Concomitantly, IL-6 levels increased after treatment with LGG (P = .023) but not with MIX or placebo. Soluble E-selectin levels were higher after probiotic than after placebo treatment in infants with IgE-mediated CMA (LGG geometric mean, 86.7 ng/mL [95% CI, 75.2-100]; MIX geometric mean, 91.6 ng/mL [95% CI, 74.8-111.9]; and placebo geometric mean, 64.9 ng/mL [95% CI, 53-79.3]; analysis of covariance, P = .035; LGG vs placebo, P = .023; MIX vs placebo, P = .020). Use of MIX induced an increase in plasma IL-10 levels (P = .016).

Conclusion

Probiotics induced systemically detectable low-grade inflammation, which might explain the clinical effects of probiotics in AEDS and CMA.

Section snippets

Subjects

A group of 230 infants suspected of having CMA were recruited between November 1999 and March 2002 to study the effects of probiotics on AEDS symptoms at the Skin and Allergy Hospital of Helsinki University Central Hospital.¹³ We acquired paired plasma samples of 132 infants (age, 1.4-11.5 months; mean age, 6.5 months; 65% male subjects) for analysis. At the first visit, cow's milk (CM) elimination was started for infants and their breast-feeding mothers. All infants received extensively

Results

After treatment of infants with IgE-associated AEDS, pretreatment-adjusted serum CRP levels were greater in the LGG group than in the placebo group (Table I and Fig 1). However, after treatment, in the whole study population and in infants with IgE-mediated CMA, pretreatment-adjusted serum CRP levels did not differ significantly after probiotic or placebo treatment (Table I).

Among infants with IgE-mediated CMA, adjusted posttreatment serum sE-selectin was higher in the LGG and MIX groups than

Discussion

The data presented document a significant increase in CRP levels in LGG-treated IgE-associated infants with AEDS compared with those seen in the placebo group. CRP is a marker of inflammation, with low levels of CRP reflecting subclinical inflammation, such as in atherosclerosis.¹⁵ IL-6 induces gene activation of CRP in hepatocytes and stimulates CRP secretion.¹⁶ Here we demonstrated concomitantly increased IL-6 and CRP levels in LGG-treated infants with IgE-associated AEDS. In acute allergic

References (41)

M. Kalliomäki et al.
Distinct patterns of neonatal gut microflora in infants in whom atopy was and was not developing
J Allergy Clin Immunol
(2001)
S. Watanabe et al.
Differences in fecal microflora between patients with atopic dermatitis and healthy control subjects
J Allergy Clin Immunol
(2003)
H. Majamaa et al.
Probiotics: a novel approach in the management of food allergy
J Allergy Clin Immunol
(1997)
M. Kalliomäki et al.
Probiotics in primary prevention of atopic disease: a randomised placebo-controlled trial
Lancet
(2001)
Y. Maeda et al.
The failure of oral tolerance induction is functionally coupled to the absence of T cells in Peyer's patches under germfree conditions
Immunobiology
(2001)
V. Rosenfeldt et al.
Effect of probiotic Lactobacillus strains in children with atopic dermatitis
J Allergy Clin Immunol
(2003)
E. Pohjavuori et al.
Lactobacillus GG effect in increasing IFN-gamma production in infants with cow's milk allergy
J Allergy Clin Immunol
(2004)
M. Cesari et al.
Inflammatory markers and cardiovascular disease (The Health, Aging and Body Composition [Health ABC] Study)
Am J Cardiol
(2003)
R.Y. Lin et al.
Interleukin 6 and C-reactive protein levels in patients with acute allergic reactions: an emergency department-based study
Ann Allergy Asthma Immunol
(2001)
J.E. Volanakis
Human C-reactive protein: expression, structure, and function
Mol Immunol
(2001)

Y.K. Lee et al.

Displacement of bacterial pathogens from mucus and Caco-2 cell surface by lactobacilli

J Med Microbiol

(2003)

T. Pritts et al.

Mucosal and enterocyte IL-6 production during sepsis and endotoxemia–role of transcription factors and regulation by the stress response

Am J Surg

(2002)

X.P. Wang et al.

The interleukin-6 cytokine system regulates epidermal permeability barrier homeostasis

J Invest Dermatol

(2004)

B. Zemann et al.

Oral administration of specific antigens to allergy-prone infant dogs induces IL-10 and TGF-beta expression and prevents allergy in adult life

J Allergy Clin Immunol

(2003)

A.M. Faria et al.

Oral tolerance induced by continuous feeding: enhanced up-regulation of transforming growth factor-beta/interleukin-10 and suppression of experimental autoimmune encephalomyelitis

J Autoimmun

(2003)

B. Björkstén et al.

The intestinal microflora in allergic Estonian and Swedish 2-year-old children

Clin Exp Allergy

(1999)

E. Sepp et al.

Effect of Administration of Lactobacillus casei strain GG on the gastrointestinal microbiata of newborns

Microb Ecol Health Dis

(1993)

M. Alander et al.

Persistence of colonization of human colonic mucosa by a probiotic strain, Lactobacillus rhamnosus GG, after oral consumption

Appl Environ Microbiol

(1999)

N. Sudo et al.

The requirement of intestinal bacterial flora for the development of an IgE production system fully susceptible to oral tolerance induction

J Immunol

(1997)

E. Isolauri et al.

Probiotics in the management of atopic eczema

Clin Exp Allergy

(2000)

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Supported by Valio Limited, Finland; the Foundation for Nutrition Research, Helsinki, Finland; the Foundation for Paediatric Research, Helsinki, Finland; the Research Foundation of Orion Corporation, Espoo, Finland; and the Kordelin Foundation, Helsinki, Finland.

Disclosure of potential conflict of interest—none disclosed.

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Food allergy, dermatologic diseases, and anaphylaxisInduction of inflammation as a possible mechanism of probiotic effect in atopic eczema–dermatitis syndrome

Background

Objective

Methods

Results

Conclusion

Section snippets

Subjects

Results

Discussion

J Allergy Clin Immunol

J Allergy Clin Immunol

J Allergy Clin Immunol

Lancet

Immunobiology

J Allergy Clin Immunol

J Allergy Clin Immunol

Am J Cardiol

Ann Allergy Asthma Immunol

Mol Immunol

J Med Microbiol

Am J Surg

J Invest Dermatol

J Allergy Clin Immunol

J Autoimmun

The intestinal microflora in allergic Estonian and Swedish 2-year-old children

Clin Exp Allergy

Effect of Administration of Lactobacillus casei strain GG on the gastrointestinal microbiata of newborns

Microb Ecol Health Dis

Persistence of colonization of human colonic mucosa by a probiotic strain, Lactobacillus rhamnosus GG, after oral consumption

Appl Environ Microbiol

The requirement of intestinal bacterial flora for the development of an IgE production system fully susceptible to oral tolerance induction

J Immunol

Probiotics in the management of atopic eczema

Clin Exp Allergy

Food allergy, dermatologic diseases, and anaphylaxis
Induction of inflammation as a possible mechanism of probiotic effect in atopic eczema–dermatitis syndrome