Abstract
The effect of dietary therapy with a human Lactobacillus strain GG (ATCC 53103), bovine colostrum, or bovine immune colostrum with specific antibodies against anaerobic intestinal bacteria on gut defence mechanisms were studied in juvenile chronic arthritis. Thirty patients with juvenile chronic arthritis were randomly allocated to receive a freeze-dried powder of Lactobacillus GG, or bovine colostrum, or bovine immune colostrum, for a two-week period. Immunologic and non-immunologic gut defence mechanisms were indirectly investigated in blood and faecal samples. In patients receiving Lactobacillus GG, the median (interquartile range) frequency of immunoglobulin-secreting cells, determined by enzyme-linked immunospot assay, increased in the IgA class from 1840 (690–2530) to 3480 (1030–13 170)/106 cells; p=0.02. Likewise the median (interquartile range) frequency of specific antibody-secreting cells against dietary antigens increased during the Lactobacillus GG therapy in the IgM class from 3.8 (1.4–5.0) to 11.2 (5.0–30.0)/106 cells; p=0.02. In addition, Lactobacillus GG therapy decreased the median (interquartile range) activity of faecal urease, which has been associated with mucosal tissue damage, from 40.3 (21.7–54.3) to 28.6 (24.5–49.4) nmol. min−1 (mg protein)−1; p=0.10, while, in patients receiving bovine colostrum, faecal urease activity increased (from 42.2 to 80.6; p=0.04). All findings were transient. We suggest that gut defence mechanisms are disturbed in juvenile chronic arthritis and we further suggest that orally administered Lactobacillus GG has a potential to reinforce the mucosal barrier mechanisms in juvenile chronic arthritis.
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Abbreviations
- ELISPOT:
-
solid-phase enzyme-linked immunospot assay
- GLC:
-
gas-liquid chromatography
- Ig:
-
immunoglobulin
- IQR:
-
interquartile range
- ISC:
-
immunoglobulin-secreting cells
- JCA:
-
juvenile chronic arthritis
- Lactobacillus GG:
-
Lactobacillus strain GG (ATCC 53103)
- NSAID:
-
nonsteroidal anti-inflammatory drug
- sASC:
-
specific antibody-secreting cells
- TNF-α:
-
tumour necrosis factor-α
References
Neumann V, Wright V. Arthritis associated with bowel disease. Clin Gastroenterol. 1983;12:767–95.
Schorr-Lesnick B, Brandt LJ. Selected rheumatologic and dermatologic manifestations of inflammatory bowel disease. Am J Gastroenterol. 1988;83:216–23.
Darlington LG, Ramsey NW, Mansfield JR. Placebo-controlled, blind study of dietary manipulation therapy in rheumatoid arthritis. Lancet. 1986;i:236–8
Panush RS. Food induced (“allergic”) arthritis: clinical and serologic studies. J Rheumatol. 1990;17:291–4.
Kjeldsen-Kragh J, Haughen M, Borchgrevink CF et al. Controlled trial of fasting and one-year vegetarian diet in rheumatoid arthritis. Lancet. 1991;338:899–902.
van de Laar MAFJ, van der Korst JK. Food intolerance in rheumatoid arthritis. I. A. double blind, controlled trial of the clinical effects of elimination of milk allergens and azo dyes. Ann Rheum Dis. 1992;51:298–302.
Shinebaum R, Neumann VC, Cook EM, Wright V. Comparison of faecal florae in patients with rheumatoid arthritis and controls. Br J Rheumatol. 1987;26:329–33.
Eerola E, Möttönen T, Hannonen P et al. Intestinal flora in early rheumatoid arthritis. Br J Rheumatol. 1994;33:1030–8
Marcolongo R, Bayeli PF, Montagnani IM. Gastrointestinal involvement in rheumatoid arthritis: a biopsy study. J Rheumatol. 1979;6:163–73.
Mielants H, Veys EM, Joos R, Cuvelier C, De Vos M, Proot F. Late onset pauciarticular juvenile chronic arthritis: relation to gut inflammation. J Rheumatol. 1987;14:459–65.
Sundqvist T, Lindström F, Magnusson K-E, Sköldstam L, Stjernström I, Tagesson C. Influence of fasting on intestinal permeability and disease activity in patients with rheumatoid arthritis. Scand J Rheumatol. 1982;11:33–8.
Smith MD, Gibson RA, Brooks PM. Abnormal bowel permeability in ankylosing spondylitis and rheumatoid arthritis. J Rheumatol. 1985;12:299–305.
Jenkins RT, Rooney PJ, Jones DB, Bienenstock KJ, Goodcare RL. Increased intestinal permeability in patients with rheumatoid arthritis: a side effect of oral nonsteroidal anti-inflammatory drug therapy? Br J Rheumatol. 1987;26:103–7.
Israel EJ, Walker WA. Host defence development in gut and related disorders. Pediatr Clin N Am. 1988;35:1–15.
Sarker SA, Gyr K. Non-immunological defence mechanisms of the gut. Gut 1992;33:987–93.
Brandtzaeg P, Halstensen TS, Kett K et al. Immunobiology and immunopathology of human gut mucosa: humoral immunity and intraepithelial lymphocytes. Gastroenterology. 1989;97:1562–84.
Gray JDA, Shiner M. Influence of gastric pH on gastric and jejunal flora. Gut. 1967;8:574–81.
Simon GL, Gorbach SL. The human intestinal microflora. Dig Dis Sci. 1986;31(Suppl):147S-62S.
Isolauri E, Juntunen M, Sillanaukee P, Koivula T. A human Lactobacillus strain (Lactobacillus casei sp strain GG) promotes recovery from acute diarrhea in children. Pediatrics. 1991;88:90–7.
Isolauri E, Majamaa H, Arvola T, Rantala I, Virtanen E, Arvilommi H. Lactobacillus casei strain GG reverses increased intestinal permeability induced by cow milk in suckling rats. Gastroenterology. 1993;105:1643–50.
Isolauri E, Kaila M, Mykkänen H, Ling WH, Salminen S. Oral bacteriotherapy for viral gastroenteritis. Dig Dis Sci. 1994;39:2595–600
Kaila M, Isolauri E, Soppi E, Virtanen E, Laine S, Arvilommi H. Enhancement of the circulating antibody secreting cell response in human diarrhea by a human Lactobacillus strain. Pediatr Res. 1992;32:141–4
Malin M, Suomalainen H, Saxelin M, Isolauri E. Promotion of IgA immune response in patients with Crohon's disease by oral bacteriotherapy with Lactobacillus GG. Ann Nutr Metab. 1996;40:137–45.
Fuller R. Probiotics in man and animals. J Appl Bacteriol. 1989;66:365–78
Björk L, Hopman J. Significance of the indigenous antimicrobial agents of milk to the dairy industry. Bull Int Dairy Federation. 1991;246:1–19.
Goldman AS. The immune system of human milk: antimicrobial, antiinflammatory and immunomodulating properties. Pediatr Infect Dis J. 1993;12:664–71.
Mietens C, Keinhorst H. Treatment of infantile E. coli gastroenteritis with specific bovine anti-E. coli milk immunoglobulins. Eur J Pediatr. 1979;132:239–52.
Hilpert H, Brüssow H, Mietens C, Sidoti J, Lerner L, Werchau H. Use of bovine milk concentrate containing antibody to rotavirus to treat rotavirus gastroenteritis in infants. J Infect Dis. 1987;156: 158–66.
Isolauri E, Virtanen E, Jalonen T, Arvilommi H. Local immune response measured in blood lymphocytes reflects the clinical reactivity of children with cow's milk allergy. Pediatr Res. 1990;28:582–6.
Yocum DE, Esparza L, Dubry S, Benjamin JB, Volz R, Scuder P. Characteristics of tumor necrosis factor production in rheumatoid arthritis. Cell Immunol. 1989;122:131–45.
Drasar BS, Hill MJ. Bacterial glycosidases. In: Drasar BS, Hill MJ, eds. Human Intestinal Flora. London: Academic Press: 1974:54–71.
Peltonen R, Eerola E. Derect automatic bacterial analysis of rat stool samples: the effects of diet and medical treatment studied by computerized gas-liquid chromatography of bacterial fatty acids. Microbial Ecol Health Dis. 1992;5:93–103.
Braegger CP, Nicholls S, Murch SH, Stephens S, Macdonald TT. Tumor necrosis factor alpha in stool as a marker of intestinal inflammation. Lancet. 1992;339:89–91.
Thomas DW, Sinatra FR, Merritt RJ. Random fecal alpha-1-antitrypsin concentration in children with gastrointestinal disease. Gastroenterology. 1981;80:776–82.
Wood PHN. Nomenclature and classification of arthritis in children. In: Munthe E, ed. The Care of Rheumatic Children. Basle: EULAR Publishers; 1978:47–50.
Donohue DC, Deighton M, Ahokas JT, Salminen S. Toxicity of lactic acid bacteria. In: Salminen S, von Wright A, eds. Lactic Acid Bacteria. New York: Marcel Dekker Inc.; 1993:307–13.
Freeman HJ. Effects of differing purified cellulose, pectin, and hemi-cellulose fiber diets on fecal enzymes in 1,2-dimethylhydrazine-induced rat colon carcinogenesis. Cancer Res. 1986;46:5529–32.
Lowry OH, Rosenbrough NJ, Farr AL, Randall RJ. Protein measurement with the folin phenol reagent. J Biol Chem. 1951;193:265–75.
Moss CW, Nunez-Montiel OL. Analysis of short-chain acids from bacteria by gas-liquid chromatography with a fused-silica capillary column. J Clin Microbiol. 1982;15:308–11.
Kantele A, Arvilommi H, Jokinen I. Specific immunoglobulin-secreting human blood cells after peroral vaccination against Salmonella typhi. J Infect Dis. 1986;158:1126–31.
Forrest BD. Identification of an intestinal immune response using peripheral blood lymphocytes. Lancet. 1988;i:81–3.
Czerkinsky C, Svennerholm A-M, Quiding M, Jonsson R, Holmgren J. Antibody-producing cells in peripheral blood and salivary glands after cholera vaccination of humans. Infect Immun. 1991;59: 996–1001.
Kantele A. Immune response to prolonged intestinal exposure to antigen. Scand J Immunol. 1991;33:225–9.
Mestecky J, McGhee JR. Immunoglobulin A(IgA): molecular and cellular interactions involved in IgA biosynthesis and immune response. In: Dixon FJ, ed. Advances in Immunology. Florida: Academic Press; 1987:153–245.
Goldin BR, Gorbach SL, Saxelin M, Barakat S, Gualtieri L, Salminen S. Survival of Lactobacillus species (strain GG) in human gastrointestinal tract. Dig Dis Sci. 1992;37:121–8.
Elso S, Saxelin M, Salminen S. Attachment of Lactobacillus casei strain GG to human colon carcinoma cell line Caco-2: comparison with other dairy strains. Lett Appl Microbiol. 1991;13:154–6.
Saxelin M, Elo S, Salminen S, Vapaatalo H. Dose response colonisation of faeces after oral administration of Lactobacillus casei strain GG. Microbial Ecol Health Dis. 1991;4:209–14.
Hill MJ, Drasar BS. The normal colonic bacterial flora. Gut. 1995;16:318–23.
Simon Gl, Gorbach SL. Intestinal flora in health and disease. Gastroenterology. 1984;86:174–93.
Mobley HLT, Hausinger RP. Microbial ureases: significance, regulation, and molecular characterization. Microbiol Rev. 1989;53:85–108.
Malin M, Verronen P, Mykkänen H, Salminen S, Isolauri E. Increased bacterial urease activity in faeces in juvenile chronic arthritis: evidence of altered intestinal microflora? Br J Rheumatol. 1996;35:689–94.
Ling WH, Saxelin M, Hänninen O, Salminen S. Enzyme profile of Lactobacillus strain GG by a rapid API ZYM system: a comparison of intestinal bacterial strains. Microbial Ecol Health Dis. 1994;7:99–104.
Majamaa H, Miettinen A, Laine S, Isolauri E. Intestinal inflammation in children with atopic eczema: faecal eosinophil cationic protein and tumor necrosis factor-α as noninvasive indicators of food allergy. Clin Exp Allergy. 1996;26:181–7.
Stolle RJ, Beck LR. Prevention and treatment of rheumatoid arthritis. United States patent number 1988;4, 732, 757.
Ormrod DJ, Miller TE. A low molecular weight component derived from the milk of hyperimmunized cows suppresses inflammation by inhibiting neutrophil emigration. Agents. Action. 1992;37:70–9.
McClead RE, Gregory SA. Resistance of bovine colostral anti-cholera toxin antibody to in vitro and in vivo proteolysis. Infect Immun. 1984;44:474–8.
Nomoto K, Matsuoka Y, Hayakawa K et al. Antibacterial effect of bovine milk antibody against Eschericia coli in a mouse indigenous infection model. Med Microbiol Immunol. 1992;181:87–98.
Kobayashi T, Ohmori T, Yanai M, Kawanishi G, Yoshikai Y, Nomoto K. Protective effect of orally administering immune milk on endogenous infection in X-irradiated mice. Agric Biol Chem. 1991;55:2265–72.
Ishida A, Yoshikai Y, Murosaki S, Hidaka Y, Nomoto K. Administration of milk from cows immunized with intestinal bacteria protects mice from radiation-induced lethality. Biotherapy. 1992;5:215–25.
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Malin, M., Verronen, P., Korhonen, H. et al. Dietary therapy with Lactobacillus GG, bovine colostrum or bovine immune colostrum in patients with juvenile chronic arthritis: Evaluation of effect on gut defence mechanisms. Inflammopharmacol 5, 219–236 (1997). https://doi.org/10.1007/s10787-997-0001-1
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DOI: https://doi.org/10.1007/s10787-997-0001-1