ARTHRITIS & RHEUMATISM
Vol. 56, No. 12, December 2007, pp 4015–4023
DOI 10.1002/art.23063
© 2007, American College of Rheumatology
Collagen-Induced Arthritis as a Model of Hyperalgesia
Functional and Cellular Analysis of the Analgesic Actions of
Tumor Necrosis Factor Blockade
Julia J. Inglis,
1
Clare A. Notley,
1
David Essex,
1
Alex W. Wilson,
2
Marc Feldmann,
1
Praveen Anand,
1
and Richard Williams
1
Objective. There is a disparity in the animal
models used to study pain in rheumatoid arthritis (RA),
which tends to be acute in nature, and models used to
assess the pathogenesis of RA. The latter models, like
human RA, are lymphocyte-driven and polyarthritic. We
assessed pain behavior and mechanisms in collagen-
induced arthritis (CIA), the model of preclinical arthri-
tis used most commonly in the field of immunology. We
then validated the model using anti–tumor necrosis
factor (anti-TNF) therapy, which has analgesic effects in
models of inflammation as well as in human RA.
Methods. CIA was induced in DBA/1 mice by
immunization with type II collagen at the base of the
tail. Swelling and mechanical and thermal hyperalgesia
were assessed before and for 28 days after the onset of
arthritis. Spontaneous behavior was assessed using an
automated activity monitor. Glial activity was assessed
by glial fibrillary acidic protein expression, and nerve
damage was evaluated by activating transcription factor
3 expression. The actions of anti-TNF therapy on noci-
ception were then evaluated.
Results. Arthritis resulted in a decrease in the
threshold for thermal and mechanical stimuli, begin-
ning on the day of onset. Decreased spontaneous activity
was also observed. A significant increase in the number
of hyperplasic spinal cord astrocytes was observed be-
ginning 10 days after the onset of arthritis. Anti-TNF
therapy was profoundly analgesic, with an efficacy sim-
ilar to that of cyclooxygenase 2 inhibition, and reduced
astrocyte activity in CIA.
Conclusion. This study shows that the CIA model
is suitable for testing not only antiinflammatory but
also analgesic drugs for potential use in RA, and
highlights the importance of using appropriate disease
models to assess relevant pain pathways.
Several animal models are used for the study of
inflammation and inflammatory pain. The most com-
monly used models for the study of inflammatory pain
involve injecting mediators of inflammation into the
footpad or knee (1). This results in a monarthritis, in
which the contralateral limb can be used as an internal
control. However, the inflammation in these models is
acute and often self limiting in nature, differing from
that in arthritis, and does not involve B lymphocytes or
T lymphocytes, which are known to be key in the
pathogenesis of rheumatoid arthritis (RA). Antigen-
induced arthritis, in which mice are immunized with
methylated bovine serum albumin, has been used to
study pain in arthritis (2). This model is T cell dependent
but, unlike RA, is not major histocompatibility complex
restricted or B cell dependent. Streptococcal cell wall–
induced arthritis has also been used for the study of
arthritic pain. However, this model more closely resem-
bles reactive arthritis than human RA.
In contrast to models used to study pain, the
animal model that is currently most widely used to study
the pathogenesis and treatment of RA is collagen-
induced arthritis (CIA) in male DBA/1 mice (3). CIA is
induced by immunization with type II collagen in
Freund’s complete adjuvant (CFA), which induces an
Supported by GlaxoSmithKline and the Arthritis Research
Campaign.
1
Julia J. Inglis, PhD, Clare A. Notley, PhD, David Essex, MSc,
Marc Feldmann, PhD, Praveen Anand, MD, Richard Williams, PhD:
Imperial College London, London, UK;
2
Alex W. Wilson, PhD:
GlaxoSmithKline Research & Development Limited, Essex, UK.
Address correspondence and reprint requests to Julia J. Ing-
lis, PhD, Kennedy Institute of Rheumatology, Imperial College Lon-
don, London W6 8LH, UK. E-mail: j.inglis@imperial.ac.uk.
Submitted for publication January 31, 2007; accepted in
revised form August 20, 2007.
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