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Oleuropein Or Rutin Consumption Decreases the Spontaneous Development of Osteoarthritis in the Hartley Guinea Pig

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Oleuropein Or Rutin Consumption Decreases the Spontaneous Development of Osteoarthritis in the Hartley Guinea Pig Osteoarthritis and Cartilage 23 (2015) 94e102 Oleuropein or rutin consumption decreases the spontaneous development of osteoarthritis in the Hartley guinea pig M.-N. Horcajada y a, C. Sanchez z a, F. Membrez Scalfo y, P. Drion x, F. Comblain z, * S. Taralla k, A.-F. Donneau ¶, E.A. Offord y, Y. Henrotin z # y Nestle Research Center, Nutrition and Health Research, Vers-Chez-les-Blanc, Lausanne 26 1000, Switzerland z Bone and Cartilage Research Unit, Arthropole,^ University of Liege, Institute of Pathology, CHU Sart-Tilman, 4000 Liege, Belgium x GIGA CHU Animal Facility, University of Liege, 4000 Liege, Belgium k Artialis SA, 4000 Liege Belgium ¶ Public Health Department, University of Liege, 4000 Liege, Belgium # Department of Physical Therapy and Rehabilitation, Princess Paola Hospital, Marche-en-famenne, Belgium article info summary Article history: Objective: To assess the potential protective effects of three polyphenols oleuropein, rutin and curcumin, Received 10 February 2014 on joint ageing and osteoarthritis (OA) development. Accepted 28 August 2014 Design: Sixty 4-week-old DunkineHartley guinea pigs were randomized into four groups and received daily during 31 weeks either standard guinea pig diet (control group) or a standard guinea pig diet Keywords: enriched with oleuropein (0.025%), rutin (0.5%) or rutin/curcumin (0.5%/0.25%) association. Biomarkers Osteoarthritis of OA (Coll2-1, Coll2-1NO2, Fib3-1, Fib3-2, ARGS), as well as inflammation prostaglandin E2 (PGE2) were Phytonutrients quantified in the serum. Histological assessments of knee cartilage and synovial membrane were per- Oleuropein fi Rutin formed at week 4 ( ve young reference guinea pigs) and week 35. fi Guinea pigs Results: At week 35, guinea pigs in the control group spontaneously developed signi cant cartilage lesions with mild synovial inflammation. The histological scores of cartilage lesions and synovitis were well correlated with the increased level of serum biomarkers. Histologically, all treatments significantly reduced the cartilage degradation score (P < 0.01), but only oleuropein significantly decreased the synovial histo- logical score (P < 0.05) and serum PGE2 levels (P < 0.01) compared to the control group. Coll2-1 was decreased by rutin and the combination of rutin/curcumin, Fib3-1 and Fib3-2 were only decreased by the rutin/curcumin mixture, while Coll2-1NO2 was significantly decreased by all treatments (P < 0.05). Conclusion: Oleuropein and rutin ± curcumin significantly slowed down the progression of spontaneous OA lesions in guinea pigs. While no additive effect was seen in the curcumin þ rutin group, the differ- ential effects of oleuropein and rutin on inflammatory and cartilage catabolic markers suggest an interesting combination for future studies in OA protection. © 2014 Osteoarthritis Research Society International. Published by Elsevier Ltd. All rights reserved. Introduction Osteoarthritis (OA) is a high prevalence disease with an important socio-economic impact. OA is characterized by fibril- * Address correspondence and reprint requests to: Y. Henrotin, Bone and Carti- lations, fissures, and even in late stage of the disease, disap- lage Unit Research, University of Liege, Sart Tilman, B-4000 Liege, Belgium. Tel: þ32 pearance of cartilage. Furthermore, cartilage degradation is 42427797. associated with structural and metabolic changes in other joint E-mail addresses: [email protected] (M.-N. Horcajada), [email protected] (C. Sanchez), [email protected] tissues such as subchondral bone sclerosis and synovial mem- 1 (F. Membrez Scalfo), [email protected] (P. Drion), [email protected] brane inflammation . Numerous models have been proposed to (F. Comblain), [email protected] (S. Taralla), [email protected] investigate the natural course of the disease and to study the (A.-F. Donneau), [email protected] (E.A. Offord), yhenrotin@ effects of treatments. Among these models, DunkineHartley ulg.ac.be (Y. Henrotin). guinea pigs developing spontaneous OA is very attractive because a Authors have equally contributed to the work. http://dx.doi.org/10.1016/j.joca.2014.08.016 1063-4584/© 2014 Osteoarthritis Research Society International. Published by Elsevier Ltd. All rights reserved. M.-N. Horcajada et al. / Osteoarthritis and Cartilage 23 (2015) 94e102 95 it mimics well the pathophysiological processes observed in Table I primary human OA2. Composition of the experimental diets The appearance of joint pathology in both guinea pigs and Control in (%) Oleuropein (%) Rutin (%) Rutin þ humans is age-related and subject to a variety of well-recognized curcumin (%) OA risk factors including body weight, ligament laxity and high Corn starch* 46.4 46.38 45.9 45.65 bone turnover. Spontaneous lesions in the knee are bilateral and are Soy proteiny 18.7 18.7 18.7 18.7 more pronounced in the medial compartment in the area not DL-methioninez 1.0 1.0 1.0 1.0 x covered by the meniscus. Bone cysts (2e3 months old), sub- Sucrose 5.0 5.0 5.0 5.0 Cellulosek 10.0 10.0 10.0 10.0 e chondral bone thickening and osteophytes (3 12 months old) are Guar gumz 2.5 2.5 2.5 2.5 3 preceded by type II collagen fibril disruption (2 months old) , his- Mineral mix¶ 7.5 7.5 7.5 7.5 tological proteoglycan loss (4e6 months old) and cartilage fibril- Vitamin mix¶ 1.0 1.0 1.0 1.0 e z lations (8e12 months old)2,4 7. The involvement of interleukin (IL)- Choline bitartrate 0.5 0.5 0.5 0.5 b Ascorbic acidz 0.4 0.4 0.4 0.4 1 and matrix metalloproteinases (MMP-3 and-13) in this degen- Kliba diet 3420# 3.0 3.0 3.0 3.0 8 erative process has been shown . Palm oilz 0.8 0.8 0.8 0.8 Some epidemiological studies have reported an association be- Soybean oil** 3.04 3.04 3.04 3.04 tween long-term consumption of diets rich in polyphenols and Linseed oilz 0.16 0.16 0.16 0.16 yy protection against chronic diseases9 but few studies have investi- Oleuropein 0 0.025 0 0 Rutinz 0 0 0.5 0.5 gated the effects of such compounds on cartilage and no long-term Curcuminz 0 0 0 0.25 10,11 studies on OA have been carried out with phytonutrients . yy Extrasynthese, Genay, France. fl * Nevertheless, antioxidant and anti-in ammatory properties of Schweizerhall Chemie, Basel, Switzerland. y polyphenols make them interesting candidates to study their po- Solae, Grand-Saconnex, Switzerland. z tential protective effect on cartilage. Recently, data from clinical Sigma Aldrich, Buchs, Switzerland. x Howeg, Aaberg, Switzerland. studies suggest that curcumin improved joint function, reduced k 12,13 Christ Water Technology Group, Basel, Switzerland. pain and type II collagen degradation in OA patients . ¶ Vital AG, Oberentfelden, Switzerland according to mineral (no250001) and The leaves and fruit of the olive plant (Olea europaea L.) are rich vitamin (no 350001) mix composition from Dyets, Inc., Bethlehem, PA. in polyphenols exhibiting a range of beneficial effects including # Provimi Kliba AG, Kaiseraugst, Switzerland. ** antioxidant, anti-inflammatory, antiatherogenic and anticarcino- Florin, Muttenz, Switzerland. genic properties14, the most bioactive ones being oleuropein and hydroxytyrosol. It has recently been demonstrated that oleuropein 0.5% of rutin and 0.25% of curcumin (n ¼ 15) until week 35 (Table I). protects against collagen II-induced arthritis in mice15. Rutin The daily dose consumed during 31 weeks corresponds approxi- (quercetin-3-O-rutinoside) is a flavonoid ubiquitously found in mately to an intake of 12.5 mg/kg body weight for oleuropein, plants. Quercetin, the circulating aglycone form of rutin, is 250 mg/kg for rutin (thus 125 mg total equivalent aglycon) and considered to be a strong antioxidant due to its ability to scavenge 125 mg/kg for curcumin. The number of animal per group was free radicals16,17. choose according to the Osteoarthritis Research Society Interna- The aim of the current study was to investigate if these poly- tional (OARSI) recommendation18 to provide 80% power to detect a phenols would exert a protective effect on cartilage and influence significant change in response to a hypothetical treatment capable of the natural course of spontaneous OA in DunkineHartley guinea achieving a 30% treatment difference compared to untreated ani- pigs. Primary outcome was the improvement of global OA histo- mals, with statistical significance of P ¼ 0.05. logical score, and secondary outcomes were the variation of serum Animals were weighed every week. Food intake was controlled levels of biomarkers prostaglandin E2, fibulin-3 fragments (Fib3-1 at weeks 9, -15, -21, -26 and -34. and Fib3-2), collagen (Coll2-1 and Coll2-1NO2) and aggrecan (ARGS) neoepitopes. Blood sampling Methods At week 4, -10, -16, -22 and -28, 500 ml of blood was collected at All experimental procedures and protocols used in this investi- the superficial veins of the ears, in the morning, under ketamine gation were reviewed and approved by the Institutional Animal Care (32 mg/kg)/xylazine (3 mg/kg) subcutaneous anaesthesia. and Use Ethics Committee of the University of Liege (Belgium), At week 4 for the young reference group and at week 35 for the reference 1207. The “Guide for the Care and Use of Laboratory Ani- other groups, 2 ml of blood was collected by intracardiac puncture, mals,” prepared by the Institute of Laboratory Animal Resources, under general anaesthesia (sodium pentobarbital 200 mg/kg, National Research Council, and published by the National Academy intraperitonealy), just before dead. Press, was followed carefully as well as European and local legisla- Blood was then centrifuged at 2000Â g for 5 min, and serum tion. Sixty-five 3-week-old male DunkineHartley guinea pigs were stored at À80 C until analysis. obtained from Charles River Laboratories (Paris, France).
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