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. 2014 May 23;9(5):e97347.
doi: 10.1371/journal.pone.0097347. eCollection 2014.

Evoked temporal summation in cats to highlight central sensitization related to osteoarthritis-associated chronic pain: a preliminary study

Martin Guillot  1 , Polly M Taylor  2 , Pascale Rialland  1 , Mary P Klinck  1 , M Maxim Moreau, Johanne Martel-Pelletier  3 , Jean-Pierre Pelletier  3 , Eric Troncy  1
Affiliations

Evoked temporal summation in cats to highlight central sensitization related to osteoarthritis-associated chronic pain: a preliminary study

Martin Guillot et al. PLoS One. .

Erratum in

  • PLoS One. 2014;9(11):e114659. Moreau, M Maxim [added]

Abstract

In cats, osteoarthritis causes significant chronic pain. Chronicity of pain is associated with changes in the central nervous system related to central sensitization, which have to be quantified. Our objectives were 1) to develop a quantitative sensory testing device in cats for applying repetitive mechanical stimuli that would evoke temporal summation; 2) to determine the sensitivity of this test to osteoarthritis-associated pain, and 3) to examine the possible correlation between the quantitative sensory testing and assessment using other pain evaluation methods. We hypothesized that mechanical sub-threshold repetitive stimuli would evoke temporal summation, and that cats with osteoarthritis would show a faster response. A blinded longitudinal study was performed in 4 non-osteoarthritis cats and 10 cats with naturally occurring osteoarthritis. Quantification of chronic osteoarthritis pain-related disability was performed over a two week period using peak vertical force kinetic measurement, motor activity intensity assessment and von Frey anesthesiometer-induced paw withdrawal threshold testing. The cats afflicted with osteoarthritis demonstrated characteristic findings consistent with osteoarthritis-associated chronic pain. After a 14-day acclimation period, repetitive mechanical sub-threshold stimuli were applied using a purpose-developed device. Four stimulation profiles of predetermined intensity, duration and time interval were applied randomly four times during a four-day period. The stimulation profiles were different (P<0.001): the higher the intensity of the stimulus, the sooner it produced a consistent painful response. The cats afflicted with osteoarthritis responded more rapidly than cats osteoarthritis free (P = 0.019). There was a positive correlation between the von Frey anesthesiometer-induced paw withdrawal threshold and the response to stimulation profiles #2 (2N/0.4 Hz) and #4 (2N/0.4 Hz): Rhos = 0.64 (P = 0.01) and 0.63 (P = 0.02) respectively. This study is the first report of mechanical temporal summation in awake cats. Our results suggest that central sensitization develops in cats with naturally occurring osteoarthritis, providing an opportunity to improve translational research in osteoarthritis-associated chronic pain.

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Conflict of interest statement

Competing Interests: The authors have the following interests. This study was partly supported by a Collaborative Research and Development grant (#RDCPJ 418399–11, supporting operations and salaries) in partnership with ArthroLab Inc from the Natural Sciences and Engineering Research Council (NSERC) of Canada. Dr. Pascale Rialland received a doctoral Industrial Innovation Scholarship from a partnership including NSERC of Canada, Fonds de recherche du Québec – Nature et Technologies and ArthroLab, Inc. Polly M. Taylor is a director of Topcat Metrology, Ltd. There are no patents, products in development or marketed products to declare. This does not alter the authors' adherence to all the PLOS ONE policies on sharing data and materials, as detailed online in the guide for authors.

Figures

Figure 1
Figure 1. Photograph of the placement of the von Frey probe.
During evaluation, the cats stood in a meshed cage, the probe tip was placed perpendicular to the plantar surface of the foot, and an increasing force was applied without manipulating the limb.
Figure 2
Figure 2. Photograph of the mechanical repetitive stimuli quantitative sensory testing experimental setting.
Cats were placed in a meshed cage. The mechanical stimulator, which was embedded in a small band, was placed around the distal aspect of the cat's foreleg (left in this photograph) and connected to the stimulator device, while a dummy band was installed on the contralateral leg (right in this photograph).
Figure 3
Figure 3. Characterization of osteoarthritis (OA) using chronic pain evaluation methods: A- Least squares means and 95% confidence interval of the log-transformed most affected limb peak vertical ground reaction force (PVF) after-exercise by OA status.
B- Least squares means and 95% confidence interval of the motor activity (MA) intensity by OA status. C- Least squares means and 95% confidence interval of the log-transformed von Frey anesthesiometer-induced paw withdrawal threshold by OA status.
Figure 4
Figure 4. Number of stimuli reached and 95% confidence interval (inverse link of the least squares means estimates and 95% confidence interval obtained using the Poisson generalized linear modelling) following repetitive mechanical stimuli: A- by stimulation profiles (#1 to 4); B- by stimulation profiles and osteoarthritis (OA) status.
Adj-P =  adjusted p-value.
See this image and copyright information in PMC

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Publication types

Grants and funding

This study was supported in part by a Pilot Study grant from the Quebec Bio-Imaging Network (#5886) of the Fonds de recherche du Québec – Santé (Pr. Eric Troncy), by a Discovery grant (#327158-2008, #441651-2013, supporting salaries) and a Collaborative Research and Development grant (#RDCPJ 418399–11, supporting operations and salaries) in partnership with ArthroLab, Inc. from the Natural Sciences and Engineering Research Council (NSERC) of Canada (Pr. Eric Troncy), as well as an ongoing New Opportunities Fund grant (#9483) and a Leader Opportunity Fund grant (#24601), supporting pain/function equipment from the Canada Foundation for Innovation (Pr. Eric Troncy). The funding sources were not involved in the study design, collection, analysis and interpretation of data, writing of the manuscript, nor in the decision to submit the manuscript for publication. Dr. Martin Guillot was the recipient of an Alexander Graham Bell NSERC Canada Graduate Scholarship for doctorate research, and a Doctoral Scholarship from the Canadian Institutes of Health Research – MENTOR Strategic Training Initiative in Health Research Program. Dr. Pascale Rialland received a doctoral Industrial Innovation Scholarship from a partnership including NSERC of Canada (#406726), Fonds de recherche du Québec – Nature et Technologies (#144812) and ArthroLab, Inc. Dr. Mary Klinck was the recipient of a Zoetis – Morris Animal Foundation (#D10-901) doctoral scholarship. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.