Lactobacillus GG Bacteria Ameliorate Arthritis in Lewis Rats
Open accessAbstract
Probiotic bacteria have beneficial effects in infectious and inflammatory diseases, principally in bowel disorders. In the case of chronic progressive autoimmune arthritides, a major goal of treatment is to reduce inflammation. We hypothesized that probiotic bacteria would ameliorate inflammation found in arthritis models. To assess this effect, Lewis rats were injected with 50 microg bovine alpha-tropomyosin (TRM) or complete Freund's adjuvant (CFA) to induce tropomyosin arthritis (TA) or adjuvant arthritis (AA), respectively. In both models, the rats were divided into 6 groups and fed 0.5 mL/d of the following suspensions: 1) heat-killed Lactobacillus GG (LGG) bacteria; 2) live LGG, both 10(11) colony-forming units (cfu)/L; 3) sterilized milk; 4) plain yogurt; 5) yogurt containing 10(11) cfu/L LGG; or 6) sterilized water. In the disease-prevention experiments, feeding started 1 wk before or after disease induction. In the therapeutic experiments, feeding was initiated at the onset of clinical arthritis. In all experiments, there were significant interactions between time and treatment (P < 0.001), except for milk, which had no effect in the therapeutic experiment. Histologically, rats fed yogurt containing LGG had a milder inflammation in all experiments (P < 0.05), whereas rats fed plain yogurt exhibited a moderate inflammatory score only in the prevention experiments. Anti-TRM antibody titers were not affected by any of the treatments in any of the experiments. Ingestion of live or heat-killed human LGG had a clinically beneficial effect on experimental arthritis. Our observation of the remarkable preventive and curative effect on arthritis using commercial yogurts containing lactobacilli, especially LGG, suggests the need for investigation of these agents in arthritic patients.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Animal studies suggest that fermented milk might augment probiotic functionality when compared to water or saline carriers.
“This is also supported by animal studies that suggest that fermented milk might augment 4 probiotic functionality when compared to water or saline carriers 47 48 .”
Cites
Probiotics in primary prevention of atopic disease: a randomised placebo-controlled trial
Kalliomäki, M. A., Salminen, S., Arvilommi, H. S., Kero, P. O., Koskinen, P. J., & Isolauri, E. (2001) · The Lancet · doi:10.1016/s0140-6736(00)04259-8 · Cited by 2,434 · see citing works
Probiotics: effects on immunity
Isolauri, E., Sütas, Y., Kankaanpää, P., Arvilommi, H. S., & Salminen, S. (2001) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/73.2.444s · Cited by 1,021 · see citing works
Demonstration of safety of probiotics—A review
Salminen, S. (1998) · International Journal of Food Microbiology · doi:10.1016/s0168-1605(98)00128-7 · Cited by 884 · see citing works
Vitamin D in preventive medicine: are we ignoring the evidence?
Zittermann, A. (2003) · British Journal Of Nutrition · doi:10.1079/bjn2003837 · Cited by 877 · see citing works
Development of Arthritis, Periarthritis and Periostitis in Rats Given Adjuvants.
Pearson, C. M. (1956) · Experimental Biology and Medicine · doi:10.3181/00379727-91-22179 · Cited by 846 · see citing works
Protection from gastrointestinal diseases with the use of probiotics
Marteau, P. R., de Vrese, M., Cellier, C., & Schrezenmeir, J. (2001) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/73.2.430s · Cited by 596 · see citing works
Survival ofLactobacillus species (strain GG) in human gastrointestinal tract
Goldin, B. R., Gorbach, S. L., Saxelin, M., Barakat, S., Gualtieri, L. N., & Salminen, S. (1992) · Digestive Diseases and Sciences · doi:10.1007/bf01308354 · Cited by 554 · see citing works
Alander, M., Satokari, R. M., Korpela, R., Saxelin, M., Vilpponen-Salmela, T., Mattila, T., & von Wright, A. (1999) · Applied and Environmental Microbiology · doi:10.1128/aem.65.1.351-354.1999 · Cited by 531 · see citing works
Interleukin‐10 generation in atopic children following oral Lactobacillus rhamnosus GG
Pessi, T., Sütas, Y., Hurme, M., & Isolauri, E. (2000) · Clinical & Experimental Allergy · doi:10.1046/j.1365-2222.2000.00948.x · Cited by 432 · see citing works
Maassen, C. B. M., van Holten-Neelen, C., Balk, F. R. M., Bak‐Glashouwer, M. ‐. H. D., Leer, R. J., Laman, J. D., Boersma, W. J. A., & Claassen, E. (2000) · Vaccine · doi:10.1016/s0264-410x(99)00378-3 · Cited by 326 · see citing works
Modulating immune responses with probiotic bacteria
Matsuzaki, T., & Chin, J. (2000) · Immunology and Cell Biology · doi:10.1046/j.1440-1711.2000.00887.x · Cited by 292 · see citing works
Viable versus inactivated lactobacillus strain GG in acute rotavirus diarrhoea.
Kaila, M., Isolauri, E., Saxelin, M., Arvilommi, H. S., & Vesikari, T. (1995) · Archives of Disease in Childhood · doi:10.1136/adc.72.1.51 · Cited by 287 · see citing works
OʼSullivan, M. (2000) · Digestive and Liver Disease · doi:10.1016/s1590-8658(00)80021-3 · Cited by 245 · see citing works
Matsuzaki, T., Nagata, Y., KADO, S., UCHIDA, K., Kato, I., Hashimoto, S., & Yokokura, T. (1997) · Apmis · doi:10.1111/j.1699-0463.1997.tb05066.x · Cited by 175 · see citing works
Armuzzi, A., Cremonini, F., Ojetti, V., et al. (2001) · Digestion · doi:10.1159/000051865 · Cited by 165 · see citing works
The Role of Fish Oils in the Treatment of Rheumatoid Arthritis
Cleland, L. G., James, M. J., & Proudman, S. (2003) · Drugs · doi:10.2165/00003495-200363090-00001 · Cited by 163 · see citing works
Uncooked, lactobacilli-rich, vegan food and rheumatoid arthritis
Nenonen, M., Helve, T., Rauma, A.-L., & Hänninen, O. (1998) · Lara D. Veeken · doi:10.1093/rheumatology/37.3.274 · Cited by 137 · see citing works
The Use of Probiotics in Gastrointestinal Disease
Madsen, K. L. (2001) · Canadian Journal of Gastroenterology · doi:10.1155/2001/690741 · Cited by 125 · see citing works
CTLA-4 regulates cell cycle progression during a primary immune response
Greenwald, R. J., Oosterwegel, M. A., van der Woude, D., Kubal, A., Mandelbrot, D. A., Boussiotis, V. A., & Sharpe, A. H. (2002) · European Journal of Immunology · doi:10.1002/1521-4141(200202)32:2 · Cited by 120 · see citing works
Adhesion of inactivated probiotic strains to intestinal mucus
Ouwehand, A. C., Tölkkö, S., Kulmala, J., Salminen, S., & Salminen, E. K. (2000) · Letters in Applied Microbiology · doi:10.1046/j.1472-765x.2000.00773.x · Cited by 116 · see citing works
Elmer, G. W. (2001) · American Journal of Health-System Pharmacy · doi:10.1093/ajhp/58.12.1101 · Cited by 109 · see citing works
Antiproliferative Effects of Homogenates Derived from Five Strains of Candidate Probiotic Bacteria
Pessi, T., Sütas, Y., Saxelin, M., Kallioinen, H., & Isolauri, E. (1999) · Applied and Environmental Microbiology · doi:10.1128/aem.65.11.4725-4728.1999 · Cited by 94 · see citing works
Perinatal characteristics and risk of rheumatoid arthritis
Jacobsson, L., Jacobsson, M. E., Askling, J., & Knowler, W. C. (2003) · BMJ · doi:10.1136/bmj.326.7398.1068 · Cited by 89 · see citing works
Maassen, C. B. M., Holten, J., Balk, F. R. M., et al. (1998) · Veterinary Quarterly · doi:10.1080/01652176.1998.9694976 · Cited by 76 · see citing works
Suppression of T-cell activation by Lactobacillus rhamnosus GG-degraded bovine casein
Pessi, T., Isolauri, E., Sütas, Y., Kankaanranta, H., Moilanen, E., & Hurme, M. (2001) · International Immunopharmacology · doi:10.1016/s1567-5769(00)00018-7 · Cited by 68 · see citing works
Probiotics and non-intestinal infectious conditions
de Vrese, M., & Schrezenmeir, J. (2002) · British Journal Of Nutrition · doi:10.1079/bjn2002630 · Cited by 66 · see citing works
Use of lactobacillus-GG in paediatric Crohn's disease
Guandalini, S. (2002) · Digestive and Liver Disease · doi:10.1016/s1590-8658(02)80167-0 · Cited by 63 · see citing works
Kano, H., Kaneko, T., & Kaminogawa, S. (2002) · Journal of Food Protection · doi:10.4315/0362-028x-65.1.153 · Cited by 62 · see citing works
Kirjavainen, P. V., El-Nezami, H. S., Salminen, S., et al. (1999) · Clinical and Diagnostic Laboratory Immunology · doi:10.1128/cdli.6.6.799-802.1999 · Cited by 61 · see citing works
Goldenberg, D. L., Pl, C., & Pa, R. (1983) · PubMed · Cited by 56 · see citing works
Malin, M., VERRONEN, P., Mykkänen, H. M., Salminen, S., & Isolauri, E. (1996) · Lara D. Veeken · doi:10.1093/rheumatology/35.7.689 · Cited by 54 · see citing works
Probiotics and Crohn's disease
Prantera, C., & Scribano, M. L. (2002) · Digestive and Liver Disease · doi:10.1016/s1590-8658(02)80168-2 · Cited by 35 · see citing works
Rovenský, J., Švík, K., Stančíková, M., et al. (2002) · Folia Microbiologica · doi:10.1007/bf02818800 · Cited by 25 · see citing works
Probiotics: could they turn out to be ineffective in irritable bowel syndrome?
Barbara, G. (2000) · Digestive and Liver Disease · doi:10.1016/s1590-8658(00)80022-5 · Cited by 25 · see citing works
Stanescu, R., Lider, O., van Eden, W., et al. (1987) · Arthritis & Rheumatism · doi:10.1002/art.1780300708 · Cited by 24 · see citing works
Baker, H. B. (1954) · BMJ · doi:10.1136/bmj.1.4874.1322 · Cited by 1 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Murray, E., Sharma, R., Smith, K. B., Mar, K. D., Barve, R., Lukasik, M., Pirwani, A. F., Malette-Guyon, E., Lamba, S., Thomas, B. J., et al. (2019) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2019.06.016 · Cited by 150 · see citing works
Probiotics: Immunomodulation and Evaluation of Safety and Efficacy
Ezendam, J., & Loveren, H. (2006) · Nutrition Reviews · doi:10.1111/j.1753-4887.2006.tb00168.x · Cited by 103 · see citing works
Dimidi, E., Zdanaviciene, A., Christodoulides, S., Taheri, S., Louis, P., Duncan, P. I., Emami, N., Crabbé, R., De Castro, C. A., McLean, P., et al. (2019) · Alimentary Pharmacology & Therapeutics · doi:10.1111/apt.15073 · Cited by 80 · see citing works
Immunological Effects of Probiotics and their Significance to Human Health
Gill, H. S., Grover, S., Batish, V. K., & Gill, P. (2009) · Prebiotics and Probiotics Science and Technology · doi:10.1007/978-0-387-79058-9_23 · Cited by 13 · see citing works
- Authors
- Baharav, E., Weinberger, A., Mor, F., & Halpern, M.
- Affiliations
- Tel Aviv University (IL)
- Weizmann Institute of Science (IL)
- Corresponding author
- Weinberger, Abraham
- Venue
- The Journal of Nutrition
- Publisher
- Elsevier BV
- Published
- 2004-08
- Volume
- 134
- Issue
- 8
- Pages
- 1964-1969
- ISSN
- 0022-3166 (ISSN-L)
- OpenAlex
- W2126876417
- Cited by
- 144
- References
- 36
- Citations by year
- 2026: 1 · 2025: 4 · 2024: 1 · 2023: 3 · 2022: 5 · 2021: 4 · 2020: 5 · 2019: 12 · 2018: 4 · 2017: 5 · 2016: 9 · 2015: 7 · 2014: 6 · 2013: 12 · 2012: 11
- FWCI
- 9.93
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Journal of Nutrition (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
- Health Sciences › Medicine › Rheumatology › Rheumatoid Arthritis Research and Therapies
- Health Sciences › Medicine › Complementary and alternative medicine › Natural Compounds in Disease Treatment
- Keywords
- Lactobacillus rhamnosus GG, probiotics, arthritis, adjuvant-induced arthritis, autoimmune arthritis, inflammation, yogurt, heat-killed bacteria, Lewis rats, dietary intervention
- MeSH terms
- Administration, Oral, Animals, Arthritis, Experimental, Female, Lactobacillus, Rats, Inbred Lew, Severity of Illness Index, Probiotics, Rats
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review