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Background: Placebo controls are essential in evaluating the effectiveness of medical treatments. Top of pageAbstractOsteoarthritis (OA) is an age-related joint disease that is characterized by degeneration of articular cartilage and chronic pain. Top of pageIntroductionOsteoarthritis (OA) is a degenerative disorder of the joints that causes significant pain and functional disability. Full figure and legend (149K)Hind limb weight bearing is a measure of pain and this was measured using an incapacitance tester.
Microscopic analysis of the damaged cartilage in the femoral and tibial articular cartilage of an OA rat model using India ink staining at 4 weeks after MIA injection.
Full figure and legend (182K)We analyzed the MMP13 expression, which is a key catabolic enzyme, to assess the effects of GSPE on the catabolic activity of chondrocytes. The MMP13 expression in synovium and cartilage in the OA model using immunohistochemistry at 4 weeks after MIA injection. Immunohistochemical analysis of the IL-1β and nitrotyrosine expressions after treatment with GSPE in the MIA-induced arthritis models at 4 weeks after MIA injection. Effectiveness and Implications of Alternative Placebo Treatments: A Systematic Review and Network Meta-analysis of Osteoarthritis Trials.
Bannuru reports grants from the Agency for Healthcare Research and Quality during the conduct of the study and grants and personal fees from the American College of Rheumatology and Sanofi outside the submitted work.
Oxidative stress is considered one of the pathophysiological factors in the progression of OA. An experimental model of OA in rats was induced by intraarticular injection of monosodium iodoacetate (MIA) into the knee joint.
Four weeks after the MIA injection, the hind limb weight bearing of the ipsilateral limb was significantly lower in the MIA-treated group than that in the nonarthritis group. Bone and osteophyte formation was evaluated in the hematoxylin and eosin-stained, paraffin-embedded knee joint sections and micro-CT analysis of the MIA injected rats treated with GSPE or vehicle, respectively.
The gross morphological changes of the femoral condyles and tibial plateau were photographed using a digital camera with application of India ink to contrast the cartilage lesions. Positive immunohistochemical reactivity to MMP13 was visualized as brown cytoplasmic and nuclear staining. Immunohistochemistry was performed on representative sections of the joints from the MIA-injected rats treated with GSPE or with vehicle. IL-1β is the main cytokine instigator of cartilage degeneration in arthritis, and it induces MMP in chondrocytes. However, the effects of antioxidants on the symptoms and structural changes of OA are controversial (Henrotin and Kurz, 2007). Increased oxidative stress and its relation with collagen metabolism in knee osteoarthritis. This differential model showed marked differences in the relative efficacies and hierarchy of the active treatments compared with a network model that considered all placebos equivalent. We investigated the effects of grape seed proanthocyanidin extract (GSPE), which is an antioxidant, on monosodium iodoacetate (MIA)-induced arthritis of the knee joint of rat, which is an animal model of human OA. To confirm the cartilage protective activity of GSPE, we immunostained for the IL-1β expression in cartilage and subchondral bone. Henrotin and Kurz suggested that drugs with high antioxidant activity could be used as therapeutic modalities for OA (Henrotin and Kurz, 2007). In the model accounting for differential effects, intra-articular and topical therapies were superior to oral treatments in reducing pain.
Osteophytes are also called bone spurs, and they are smooth outgrowths of bone that build up on the edges of joints due to OA. We used hematoxylin and eosin, Safranin O fast green and toluidine blue staining to examine the structural changes in the joints. The strong expression of cytoplasmic and nuclear MMP13 was observed in the MIA-treated group. We observed an increased IL-1β expression on the cartilage of the MIA-treated group.
GSPE has higher antioxidant activity than other well-known antioxidants such as vitamin C, vitamin E and gallic acid (Ariga, 2004).
The antioxidative function, preventive action on disease and utilization of proanthocyanidins. Taichman, MD, PhD, Executive Deputy Editor, reports that he has no financial relationships or interests to disclose. Pain was measured using the paw withdrawal latency (PWL), the paw withdrawal threshold (PWT) and the hind limb weight bearing ability. There is much evidence indicating that oxidative stress is involved in the pathogenesis of OA. The joint from non-induced rat showed smooth articular cartilage surfaces with the underneath layer of flattened chondrocytes in the tangential zone. Further, the polyphenols in GSPE have already shown beneficial antioxidant effects on other oxidative stress-associated diseases (Cho et al., 2009). Wong reports grants from the Patient-Centered Outcomes Research Institute and National Institutes of Health National Center for Complementary and Alternative Medicine and nonfinancial support from the European League Against Rheumatism outside the submitted work.
Joint damage was assessed using histological and microscopic analysis and microcomputerized tomography.
Increased ROS promote cartilage degradation by inhibiting cartilage matrix synthesis and inducing chondrocyte apoptosis and cartilage matrix breakdown (Henrotin et al., 2005). At 4 weeks after MIA injection along with GSPE treatment, histological analysis revealed osteoclasts on the subchondral bone fragmented trabeculae of the MIA-treated group (arrow), but GPSE decreased osteoclast generation (Figure 2A). The chondrocytes were normally distributed in parallel rows in the transitional and radial zones of the articular cartilage. This result suggests that GSPE can reduce the activity of the catabolic enzyme MMP13 and this enzyme has been implicated in cartilage breakdown.Figure 5.

We performed immunohistochemical staining for nitrotyrosine, which is a marker for oxidant stress, to determine whether antioxidant activity is responsible for the antinociceptive effect of GSPE and its protective effect against structural damage to knee joints. Thus, our present data show that GSPE treatment led to a significant reduction of the pain and structural changes in MIA induced OA rats.
A new class of potent matrix metalloproteinase 13 inhibitors for potential treatment of osteoarthritis: Evidence of histologic and clinical efficacy without musculoskeletal toxicity in rat models. Mulrow, MD, MSc, Senior Deputy Editor, reports that she has no relationships or interests to disclose.
Matrix metalloproteinase-13 (MMP13) and nitrotyrosine were detected using immunohistochemistry. The serum total antioxidant capacity, the thiol level and the catalase activity of OA patients are low (Altindag et al., 2007). We used micro-CT to examine the direct effect of GSPE on the MIA-induced osteophyte formation. The MIA-treated group showed degeneration of the articular cartilage and disappearance of chondrocytes and proteoglycan in the tangential, transitional and radial zones of the cartilage after 2 weeks, and more severe structural changes after 4 weeks (Figures 4A and 4B).
Nitrotyrosine was not detected in the cartilage or synovium of the nonarthritis group, but it was detected in the cartilage and chondrocytes of the MIA-treated group (Figure 6). To the best of our knowledge, this is the first report to demonstrate the effects of GSPE on MIA-induced OA of the knee joint in rats.We showed that GSPE treatment resulted in a significant decrease in chondrocyte damage and proteoglycan loss in MIA-induced OA.
Kent reports grants from the National Institutes of Health during the conduct of the study.
Deborah Cotton, MD, MPH, Deputy Editor, reports that she has no financial relationships or interest to disclose. The cartilage from patients with OA contains less extracellular antioxidants such as superoxide dismutase than does normal cartilage (Regan et al., 2005).
Osteophytes were detected in the MIA-treated group, but not in the GSPE-treated groups (Figure 2B). The nitrotyrosine staining of cartilage and synovium was reduced in the high-dose GSPE group.Figure 6. Transcriptional profiling and pathway analysis of monosodium iodoacetate-induced experimental osteoarthritis in rats: relevance to human disease. GSPE reduced the loss of chondrocytes and proteoglycan, the production of MMP13, nitrotyrosine and IL-1β and the formation of osteophytes, and it reduced the number of subchondral bone fractures in the MIA-treated rats. These results indicate that GSPE is antinociceptive and it is protective against joint damage in the MIA-treated rat model of OA. The modified Mankin scores were significantly lower in the GSPE treated group than in the MIA-treated group (Figure 4C).
As mentioned earlier, the degradation of cartilage results from the imbalance between the mechanical stresses and catabolic activity, and the latter is mainly controlled by ROS and MMPs. Antinociceptive efficacy of lacosamide in the monosodium iodoacetate rat model for osteoarthritis pain.
Proanthocyanidins are potent natural antioxidants, and they are the most abundant phenolic compounds in grape seeds and they are high molecular weight polymers comprised of dimers or trimers of (+)-catechin and (-)-epicatechin (Fine, 2000). We observed extensive areas of loosely arranged spindle cells contained within a fine stroma instead of subchondral bone marrow in the MIA-treated group.
Thus, our results can be explained that the antioxidant defense of GSPE decreased the chondrocyte damage by scavenging ROS and MMPs, by preventing their formation or by repairing the damage.We utilized nitrotyrosine to investigate the role of GSPE and especially to probe the relationship between the antioxidant activity and antinociceptive effect of GSPE. Williams, MD, Deputy Editor, reports that he has no financial relationships or interests to disclose.
There was a reduction in trabecular connectivity in the MIA-treated group (Figure 4D, arrow).
Weight bearing as a measure of disease progression and efficacy of anti-inflammatory compounds in a model of monosodium iodoacetate-induced osteoarthritis.
However, its effects on the chronic pain and structural damage relevant to the pain in OA have not been investigated.
The antioxidant vitamins A, C, E and selenium in the treatment of arthritis: a systematic review of randomized clinical trials. Four days after the injection of MIA, the paw withdrawal latency (PWL) and paw withdrawal threshold (PWT) were lower in the MIA-treated group than in the nonarthritis group, which had received a saline injection instead of MIA. Our present data indicates that treatment with high dose GSPE decreased nitrotyrosine production in the cartilage and synovium, and this suggests that the antioxidant activity of GSPE may contribute to reducing pain in the MIA rat model of OA.We then analyzed the MMP13 expression to assess the effects of GSPE on the catabolic activity of chondrocytes.
MMP13 is one of the most important metalloproteases involved in the osteoarthritic pathological process (Reboul et al., 1996).
Effects of adenovirus-mediated bFGF, IL-1Ra and IGF-1 gene transfer on human osteoarthritic chondrocytes and osteoarthritis in rabbits.
The MMP13 expression was significantly upregulated in the cartilage of MIA-treated rats (Barve et al., 2007). Effects of grape seed proanthocyanidin extracts on peripheral nerves in streptozocin-induced diabetic rats.
Our immunohistochemical staining results demonstrated that the GSPE-treated rats had fewer MMP13-producing cells in their arthritic joints than did the MIA-treated rats. New serum biochemical markers (Coll 2-1 and Coll 2-1 NO2) for studying oxidative-related type II collagen network degradation in patients with osteoarthritis and rheumatoid arthritis. These results support the fact that GSPE has a chondroprotective effect by balancing the production of ROS and MMP.Although articular cartilage is primarily affected in OA, it does not have nerve fibers.
Endogenous production of reactive oxygen species is required for stimulation of human articular chondrocyte matrix metalloproteinase production by fibronectin fragments. Therefore, it is possible that GSPE relieves pain by inhibiting vascularization after MIA treatment.Pain fibers are present in the synovium, ligaments, bone, muscle and meniscus of the knee. In the MIA rat model of OA, synovial inflammation occurs during the first week after MIA treatment and it resolves 1 week later (Beyreuther et al., 2007). Peripheral sensitization is caused by inflammatory mediators such as substance P, calcitonin gene-related peptide, vasoactive intestinal peptide (VIP), eicosanoids, ion channel ligands and cytokines (McDougall, 2006).

Site specific changes in gene expression and cartilage metabolism during early experimental osteoarthritis.
Ingestion of IH636 grape seed proanthocyanidin extract to prevent selenite-induced oxidative stress in experimental cataract.
Oligomeric proanthocyanidin complexes: history, structure, and phytopharmaceutical applications. Mono-iodoacetate-induced histologic changes in subchondral bone and articular cartilage of rat femorotibial joints: an animal model of osteoarthritis. Further, the GSPE-treated rats have fewer osteoclasts and less bony fragmentation in their subchondral bone than did the MIA-treated animals. We demonstrated that the number of osteophytes in the GSPE treated rats was lower than the number of osteophytes in the saline treated rats.Taken together, it seems that the antioxidant property of GSPE mainly contributes to its antinociceptive effects through repairing articular damage via the downregulation of ROS and MMP13 production. Moderation of iodoacetate-induced experimental osteoarthritis in rats by matrix metalloproteinase inhibitors. Tumor necrosis factor-alpha (TNF-alpha) enhances functional thermal and chemical responses of TRP cation channels in human synoviocytes. These results suggest that GSPE has an antinociceptive effect.In conclusion, we demonstrated that treatment with GSPE attenuates the MIA-induced pain and histologic changes in the knee joint. The antinociceptive and antiarthritic effects of GSPE were mediated by inhibition of cartilage damage, synovitis and subchondral bone fracture, the reduced production of nitrotyrosine and MMP13 and the suppression of osteoclastogenesis.
Our data also suggests that the beneficial effects of GSPE treatment in MIA-induced arthritis are secondary to its antioxidant effects.
The animals were housed two per cage in a room with controlled temperature conditions (21-22?) and a reversed light-dark cycle (12 h:12 h) and they had free access to sterile food and water. All the experimental procedures were examined and approved by the Animal Research Ethics Committee at the Catholic University of Korea.Development of OA and GSPE treatmentThe animals were randomized and assigned to treatment groups before the study began. OA was induced by intra-articular injection of 50 µl of 4 mg sodium iodoacetate (Sigma, St. Biochemical and metabolic abnormalities in articular cartilage from osteo-arthritic human hips. GSPE dissolved in saline was given orally three times per week for 4 weeks after the MIA injection. The rats were placed on a metal mesh surface in an acrylic chamber in a temperature-controlled room (-22?) and they were allowed to acclimatize for 15 min before the testing began. Vasoactive intestinal peptide (VIP) is a modulator of joint pain in a rat model of osteoarthritis. An adjustable angled mirror was used to place the stimulating microfilament (0.5 mm diameter) below the plantar surface of the hind paw.
When the instrument was activated, a fine plastic monofilament advanced at a constant speed and touched the paw in the proximal metatarsal region. Chondroprotective effects of a proanthocyanidin rich Amazonian genonutrient reflects direct inhibition of matrix metalloproteinases and upregulation of IGF-1 production by human chondrocytes. The filament exerted a gradually increasing force on the plantar surface, starting below the threshold of detection and increasing until the stimulus became painful and the rat removed its paw. The force required to elicit a paw withdrawal reflex was recorded automatically and measured in grams. Plasma 3-nitrotyrosine is a biomarker in animal models of arthritis: Pharmacological dissection of iNOS' role in disease. A maximum force of 50 g and a ramp speed of 20 s were used for all the aesthesiometry tests.Weight-bearing assessmentHind limb weight bearing was measured using an incapacitance tester (Linton Instrumentation, Norfolk, UK) that include a dual-channel weight averager. Grape seed proanthocyanidins improved cardiac recovery during reperfusion after ischemia in isolated rat hearts.
Liquid chromatography tandem mass spectrometry identification of proanthocyanidins in rat plasma after oral administration of grape seed extract. The knee joints, including the patella and joint capsule, were resected and kept in the same fixative for an additional 48 h at 4?.
Differential effects of IH636 grape seed proanthocyanidin extract and a DNA repair modulator 4-aminobenzamide on liver microsomal cytochrome 4502E1-dependent aniline hydroxylation. The new collagenase, collagenase-3, is expressed and synthesized by human chondrocytes but not by synoviocytes. The slides for immunohistochemistry were deparaffinized and rehydrated using a graded series of ethanol solutions. The sections were depleted of endogenous peroxidase activity by adding methanolic H2O2 and then they were blocked with normal goat serum for 30 min. The tibia and femur bones were separated and all excess soft tissue was removed by careful dissection under a dissecting microscope. The articular surface of each specimen was rinsed with PBS and painted with India ink diluted in saline.
The cartilage surfaces of the femoral condyle and the tibial plateau were examined using a microscope.Microcomputerized tomography (Micro-CT)Micro-CT was used to develop three-dimensional images of bone. John's wort, Harpagophytum procumbens extract and Grape seed proanthocyanidins extract in mice. After scanning, the cross-sectional slices were reconstructed and three-dimensional analyses were performed using CTAn SkyScan software.
Each scan result was reconstructed using the same threshold values to distinguish bone and air.

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