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NEUROLOGY 1996;47:425-432
© 1996 American Academy of Neurology

Arthritis and anti-inflammatory agents as possible protective factors for Alzheimer's disease

A review of 17 epidemiologic studies Patrick L. McGeer, PhD, FRCP(C), MD, Michael Schulzer, PhD and Edith G. McGeer, PhD

From the Kinsmen Laboratory of Neurological Research, Department of Psychiatry (Drs McGeer and E.G. McGeer) and the Departments of Medicine and Statistics (Dr. Schulzer), University of British Columbia, Vancouver, BC, Canada.
Supported by grants from the Alzheimer Society of B.C. and the Jack Brown and Family A.D. Research Fund, as well as donations from individual British Columbians.
Received November 3, 1995. Accepted in final form January 19, 1996.
Address correspondence and reprint requests to Dr. Patrick L. McGeer, Kinsmen Laboratory of Neurological Research, University of British Columbia, 2255 Wesbrook Mall, Vancouver, BC, V6T 1Z3, Canada.

Alzheimer's disease (AD) lesions are characterized by the presence of numerous inflammatory proteins.This has led to the hypothesis that brain inflammation is a cause of neuronal injury in AD and that anti-inflammatory drugs may act as protective agents. Seventeen epidemiologic studies from nine different countries have now been published in which arthritis, a major indication for the use of anti-inflammatory drugs, or anti-inflammatory drugs themselves have been considered as risk factors for AD. Both factors appear to be associated with a reduced prevalence of AD. The small size of most studies has limited their individual statistical significance, but similarities in design have made it possible to evaluate combined results. We have used established methods of statistical meta-analysis to estimate the overall chance of individuals exposed to arthritis or anti-inflammatory drugs developing AD as compared with the general population. Seven case-control studies with arthritis as the risk factor yielded an overall odds ratio of 0.556 (p < 0.0001), while four case-control studies with steroids yielded odds ratios of 0.656 (p = 0.049) and three case-control studies with nonsteroidal anti-inflammatory drugs (NSAIDs) yielded an odds ratio of 0.496 (p = 0.0002). When NSAIDs and steroids were combined into a single category of anti-inflammatory drugs, the odds ratio was 0.556 (p < 0.0001). Population-based studies were less similar in design than case-control studies, complicating the process of applying statistical meta-analytical techniques. Nevertheless, population-based studies with rheumatoid arthritis and NSAID use as risk factors strongly supported the results of case-control studies. These data suggest anti-inflammatory drugs may have a protective effect against AD. Controlled clinical trials will be necessary to test this possibility.

NEUROLOGY 1996;47: 425-432




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R. C. Petersen, R. Doody, A. Kurz, R. C. Mohs, J. C. Morris, P. V. Rabins, K. Ritchie, M. Rossor, L. Thal, and B. Winblad
Current Concepts in Mild Cognitive Impairment
Arch Neurol, December 1, 2001; 58(12): 1985 - 1992.
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J. C.S. Breitner and P. P. Zandi
Do Nonsteroidal Antiinflammatory Drugs Reduce the Risk of Alzheimer's Disease?
N. Engl. J. Med., November 22, 2001; 345(21): 1567 - 1568.
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H. YAZAWA, Z.-X. YU, TAKEDA, Y. LE, W. GONG, V. J. FERRANS, J. J. OPPENHEIM, C. C. H. LI, and J. M. WANG
{beta} Amyloid peptide (A{beta}42) is internalized via the G-protein-coupled receptor FPRL1 and forms fibrillar aggregates in macrophages
FASEB J, November 1, 2001; 15(13): 2454 - 2462.
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K. I. Andreasson, A. Savonenko, S. Vidensky, J. J. Goellner, Y. Zhang, A. Shaffer, W. E. Kaufmann, P. F. Worley, P. Isakson, and A. L. Markowska
Age-Dependent Cognitive Deficits and Neuronal Apoptosis in Cyclooxygenase-2 Transgenic Mice
J. Neurosci., October 15, 2001; 21(20): 8198 - 8209.
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A. Bal-Price and G. C. Brown
Inflammatory Neurodegeneration Mediated by Nitric Oxide from Activated Glia-Inhibiting Neuronal Respiration, Causing Glutamate Release and Excitotoxicity
J. Neurosci., September 1, 2001; 21(17): 6480 - 6491.
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 Int J EpidemiolHome page
S. L Tyas, J. Manfreda, L. A Strain, and P. R Montgomery
Risk factors for Alzheimer's disease: a population-based, longitudinal study in Manitoba, Canada
Int. J. Epidemiol., June 1, 2001; 30(3): 590 - 597.
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 NeurologyHome page
R. S. Doody, J.C. Stevens, C. Beck, R.M. Dubinsky, J.A. Kaye, L. Gwyther, R.C. Mohs, L.J. Thal, P.J. Whitehouse, S.T. DeKosky, et al.
Practice parameter: Management of dementia (an evidence-based review): Report of the Quality Standards Subcommittee of the American Academy of Neurology
Neurology, May 8, 2001; 56(9): 1154 - 1166.
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E. G. McGeer and P. L. McGeer
Innate Immunity in Alzheimer's Disease: A Model for Local Inflammatory Reactions
Mol. Interv., April 1, 2001; 1(1): 22 - 29.
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F. Landi, G. Onder, C. Cattel, G. Gambassi, F. Lattanzio, M. Cesari, A. Russo, and R. Bernabei
Functional Status and Clinical Correlates in Cognitively Impaired Community-Living Older People
J Geriatr Psychiatry Neurol, March 1, 2001; 14(1): 21 - 27.
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 Arch NeurolHome page
L. Ho, D. Purohit, V. Haroutunian, J. D. Luterman, F. Willis, J. Naslund, J. D. Buxbaum, R. C. Mohs, P. S. Aisen, and G. M. Pasinetti
Neuronal Cyclooxygenase 2 Expression in the Hippocampal Formation as a Function of the Clinical Progression of Alzheimer Disease
Arch Neurol, March 1, 2001; 58(3): 487 - 492.
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C. K. Combs, J. C. Karlo, S.-C. Kao, and G. E. Landreth
{beta}-Amyloid Stimulation of Microglia and Monocytes Results in TNF{alpha}-Dependent Expression of Inducible Nitric Oxide Synthase and Neuronal Apoptosis
J. Neurosci., February 15, 2001; 21(4): 1179 - 1188.
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K. D. Bornemann, K.-H. Wiederhold, C. Pauli, F. Ermini, M. Stalder, L. Schnell, B. Sommer, M. Jucker, and M. Staufenbiel
A{beta}-Induced Inflammatory Processes in Microglia Cells of APP23 Transgenic Mice
Am. J. Pathol., January 1, 2001; 158(1): 63 - 73.
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 Arch NeurolHome page
G. A. Broe, D. A. Grayson, H. M. Creasey, L. M. Waite, B. J. Casey, H. P. Bennett, W. S. Brooks, and G. M. Halliday
Anti-inflammatory Drugs Protect Against Alzheimer Disease at Low Doses
Arch Neurol, November 1, 2000; 57(11): 1586 - 1591.
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M. T. Heneka, T. Klockgether, and D. L. Feinstein
Peroxisome Proliferator-Activated Receptor-gamma Ligands Reduce Neuronal Inducible Nitric Oxide Synthase Expression and Cell Death In Vivo
J. Neurosci., September 15, 2000; 20(18): 6862 - 6867.
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K. ISHII, F. MUELHAUSER, U. LIEBL, M. PICARD, S. KÜHL, B. PENKE, T. BAYER, M. WIESSLER, M. HENNERICI, K. BEYREUTHER, et al.
Subacute NO generation induced by Alzheimer's {beta}-amyloid in the living brain: reversal by inhibition of the inducible NO synthase
FASEB J, August 1, 2000; 14(11): 1485 - 1489.
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 NeurologyHome page
I. R. A. Mackenzie
Activated microglia in dementia with Lewy bodies
Neurology, July 12, 2000; 55(1): 132 - 134.
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J. C. Anthony, J. C. S. Breitner, P. P. Zandi, M. R. Meyer, I. Jurasova, M. C. Norton, and S. V. Stone
Reduced prevalence of AD in users of NSAIDs and H2 receptor antagonists: The Cache County Study
Neurology, June 13, 2000; 54(11): 2066 - 2071.
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 Arch NeurolHome page
C. E. Shepherd, E. Thiel, H. McCann, A. J. Harding, and G. M. Halliday
Cortical Inflammation in Alzheimer Disease but Not Dementia With Lewy Bodies
Arch Neurol, June 1, 2000; 57(6): 817 - 822.
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 Arch NeurolHome page
G. M. Halliday, C. E. Shepherd, H. McCann, W. G. J. Reid, D. A. Grayson, G. A. Broe, and J. J. Kril
Effect of Anti-inflammatory Medications on Neuropathological Findings in Alzheimer Disease
Arch Neurol, June 1, 2000; 57(6): 831 - 836.
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C. Petersen, S. Petersen, L. Milas, F. F. Lang, and P. J. Tofilon
Enhancement of Intrinsic Tumor Cell Radiosensitivity Induced by a Selective Cyclooxygenase-2 Inhibitor
Clin. Cancer Res., June 1, 2000; 6(6): 2513 - 2520.
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C. Holmes and D. Wilkinson
Molecular biology of Alzheimer's disease
Adv. Psychiatr. Treat., May 1, 2000; 6(3): 193 - 200.
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S. Honda, F. Itoh, M. Yoshimoto, S. Ohno, Y. Hinoda, and K. Imai
Association Between Complement Regulatory Protein Factor H and AM34 Antigen, Detected in Senile Plaques
J Gerontol A Biol Sci Med Sci, May 1, 2000; 55(5): M265 - M269.
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 Arch Intern MedHome page
P. E. Lipsky, P. Brooks, L. J. Crofford, R. DuBois, D. Graham, L. S. Simon, L. B. A. van de Putte, and S. B. Abramson
Unresolved Issues in the Role of Cyclooxygenase-2 in Normal Physiologic Processes and Disease
Arch Intern Med, April 10, 2000; 160(7): 913 - 920.
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A. Castrillo, M. J. M. Diaz-Guerra, S. Hortelano, P. Martin-Sanz, and L. Bosca
Inhibition of Ikappa B Kinase and Ikappa B Phosphorylation by 15-Deoxy-Delta 12,14-Prostaglandin J2 in Activated Murine Macrophages
Mol. Cell. Biol., March 1, 2000; 20(5): 1692 - 1698.
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 NeurologyHome page
P. S. Aisen, K. L. Davis, J. D. Berg, K. Schafer, K. Campbell, R. G. Thomas, M. F. Weiner, M. R. Farlow, M. Sano, M. Grundman, et al.
A randomized controlled trial of prednisone in Alzheimer's disease
Neurology, February 8, 2000; 54(3): 588 - 588.
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 NeurologyHome page
I. R. A. Mackenzie
Anti-inflammatory drugs and Alzheimer-type pathology in aging
Neurology, February 8, 2000; 54(3): 732 - 732.
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C. K. Combs, D. E. Johnson, J. C. Karlo, S. B. Cannady, and G. E. Landreth
Inflammatory Mechanisms in Alzheimer's Disease: Inhibition of beta -Amyloid-Stimulated Proinflammatory Responses and Neurotoxicity by PPARgamma Agonists
J. Neurosci., January 15, 2000; 20(2): 558 - 567.
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D. G. Munoz and H. Feldman
Causes of Alzheimer's disease
Can. Med. Assoc. J., January 1, 2000; 162(1): 65 - 72.
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W. R. Markesbery
The Role of Oxidative Stress in Alzheimer Disease
Arch Neurol, December 1, 1999; 56(12): 1449 - 1452.
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T. J. Montine, K. R. Sidell, B. C. Crews, W. R. Markesbery, L. J. Marnett, L. J. Roberts II, and J. D. Morrow
Elevated CSF prostaglandin E2 levels in patients with probable AD
Neurology, October 22, 1999; 53(7): 1495 - 1495.
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A. J. Lerner
Alzheimer's Disease in Males: Endocrine Issues and Prospects
J. Clin. Endocrinol. Metab., October 1, 1999; 84(10): 3416 - 3419.
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T. V. Petrova, K. T. Akama, and L. J. Van Eldik
Selective Modulation of BV-2 Microglial Activation by Prostaglandin E2. DIFFERENTIAL EFFECTS ON ENDOTOXIN-STIMULATED CYTOKINE INDUCTION
J. Biol. Chem., October 1, 1999; 274(40): 28823 - 28827.
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J. L. Cummings and D. V. Jeste
Alzheimer's Disease and Its Management in the Year 2010
Psychiatr Serv, September 1, 1999; 50(9): 1173 - 1177.
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