Physical activity and Mediterranean diet based on olive tree phenolic compounds from two different geographical areas have protective effects on early osteoarthritis, muscle atrophy and hepatic steatosis

  • Marta Anna Szychlinska
  • Paola Castrogiovanni
  • Francesca Maria Trovato
  • Houda Nsir
  • Mokhtar Zarrouk
  • Debora Lo Furno
  • Michelino Di Rosa
  • Rosa Imbesi
  • Giuseppe Musumeci
Original Contribution
  • 24 Downloads

Abstract

Purpose

Osteoarthitis (OA) leads to progressive loss of articular cartilage, pain and joint disability. An acute injury constitutes an important risk factor for early OA, determining an inflammatory process responsible of cartilage degeneration and muscle atrophy, due to the joint pain and immobility. The study aims to assess the effects of conjugation of physical activity and diet enriched by olive tree compounds [extra virgin olive oil (EVOO) and olive leaf extract (OLE)], on the musculoskeletal system in OA rat model.

Methods

OA was induced by anterior cruciate ligament transection and confirmed by Mankin and OARSI scores. Rats were subjected to physical activity on treadmill 5 days a week for 10 min daily and fed with experimental diets (standard diet enriched with Sicilian EVOO, Tunisian EVOO and Tunisian EVOO-OLE) for 12 weeks. Immunohistochemistry was used to evaluate IL-6 and lubricin expression in cartilage tissue and ELISA was used to quantify these proteins in serum at different time points. Histology and histomorphometry analysis were done to valuate liver steatosis, muscle atrophy and cartilage pathological changes.

Results

Compared to the OA group, the experimental groups showed general increased lubricin and decreased IL-6 expression, significant muscle hypertrophy and no signs of liver steatosis, suggesting the beneficial effects of physical activity coupled with EVOO-enriched diets on rat articular cartilage. Interestingly, the best result was shown for Sicilian EVOO-enriched diet.

Conclusion

In conclusion, the conjugation of physical activity and EVOO-enriched diet determines a significant articular cartilage recovery process in early OA.

Keywords

Osteoarthritis Muscle atrophy Physical activity Olive oil Olive leaf extract Lubricin Inflammation 

Notes

Acknowledgements

This study was supported by the University Research Project Grant (Triennial Research Plan 2016–2018), Department of Biomedical and Biotechnological Sciences (BIOMETEC), University of Catania, Italy. The authors would like to thank “Oleificio Guccione di Divita Vito e G. SAS” for providing us the extra virgin Sicilian olive oil and Prof. Iain Halliday for commenting and making corrections to the paper.

Compliance with ethical standards

Conflict of interest

The authors declare no conflict of interest.

References

  1. 1.
    Musumeci G, Loreto C, Imbesi R, Trovato FM, Di Giunta A, Lombardo C et al (2014) Advantages of exercise in rehabilitation, treatment and prevention of altered morphological features in knee osteoarthritis. A narrative review. Histol Histopathol 29:707–719Google Scholar
  2. 2.
    Leonardi R, Loreto C, Barbato E, Caltabiano R, Lombardo C, Musumeci G et al (2008) MMP-13 (collagenase 3) localization in human temporomandibular joint discs with internal derangement. Acta Histochem 110:314–318CrossRefGoogle Scholar
  3. 3.
    Musumeci G, Szychlinska MA, Mobasheri A (2015) Age-related degeneration of articular cartilage in the pathogenesis of osteoarthritis: molecular markers of senescent chondrocytes. Histol Histopathol 30:1–12Google Scholar
  4. 4.
    Slemenda C, Brandt KD, Heilman DK, Mazzuca S, Braunstein EM, Katz BP et al (1997) Quadriceps weakness and osteoarthritis of the knee. Ann Intern Med 127:97–104CrossRefGoogle Scholar
  5. 5.
    Valderrabano V, von Tscharner V, Nigg BM, Hintermann B, Goepfert B, Fung TS et al (2006) Lower leg muscle atrophy in ankle osteoarthritis. J Orthop Res 24:2159–2169CrossRefGoogle Scholar
  6. 6.
    Rice DA, McNair PJ (2010) Quadriceps arthrogenic muscle inhibition: neural mechanisms and treatment perspectives. Semin Arthritis Rheum 40:250–266CrossRefGoogle Scholar
  7. 7.
    Castrogiovanni P, Trovato FM, Loreto C, Nsir H, Szychlinska MA, Musumeci G (2016) Nutraceutical Supplements in the Management and Prevention of Osteoarthritis. Int J Mol Sci 17:pii E2042CrossRefGoogle Scholar
  8. 8.
    Dinu M, Pagliai G, Casini A, Sofi F (2017) Mediterranean diet and multiple health outcomes: an umbrella review of meta-analyses of observational studies and randomised trials. Eur J Clin Nutr 72:30–43Google Scholar
  9. 9.
    Visioli F, Poli A, Gall C (2002) Antioxidant and other biological activities of phenols from olives and olive oil. Med Res Rev 22:65–75CrossRefGoogle Scholar
  10. 10.
    Abaza L, Taamalli A, Nsir H, Zarrouk M (2015) Olive tree (Olea europeae L.) leaves: importance and advances in the analysis of phenolic compounds. Antioxidants (Basel) 4:682–698CrossRefGoogle Scholar
  11. 11.
    Şahin S, Samli R, Tan ASB, Barba FJ, Chemat F, Cravotto G et al (2017) Solvent-free microwave-assisted extraction of polyphenols from olive tree leaves: antioxidant and antimicrobial properties. Molecules 22:piiE1056CrossRefGoogle Scholar
  12. 12.
    Leonardi R, Loreto C, Talic N, Caltabiano R, Musumeci G (2012) Immunolocalization of lubricin in the rat periodontal ligament during experimental tooth movement. Acta Histochem 114:700–704CrossRefGoogle Scholar
  13. 13.
    Leonardi R, Rusu MC, Loreto F, Loreto C, Musumeci G (2012) Immunolocalization and expression of lubricin in the bilaminar zone of the human temporomandibular joint disc. Acta Histochem 114:1–5CrossRefGoogle Scholar
  14. 14.
    Musumeci G, Trovato FM, Loreto C, Leonardi R, Szychlinska MA, Castorina S, Mobasheri A (2014) Lubricin expression in human osteoarthritic knee meniscus and synovial fluid: a morphological, immunohistochemical and biochemical study. Acta Histochem 116:965–972CrossRefGoogle Scholar
  15. 15.
    Szychlinska MA, Leonardi R, Al-Qahtani M, Mobasheri A, Musumeci G (2016) Altered joint tribology in osteoarthritis: Reduced lubricin synthesis due to the inflammatory process. New horizons for therapeutic approaches. Ann Phys Rehabil Med 59:149–156CrossRefGoogle Scholar
  16. 16.
    Pichler K, Loreto C, Leonardi R, Reuber T, Weinberg AM, Musumeci G (2013) RANKL is downregulated in bone cells by physical activity (treadmill and vibration stimulation training) in rat with glucocorticoid-induced osteoporosis. Histol Histopathol 28:1185–1196Google Scholar
  17. 17.
    Musumeci G (2015) Effects of exercise on physical limitations and fatigue in rheumatic diseases. World J Orthop 6:762–769CrossRefGoogle Scholar
  18. 18.
    Aiello FC, Trovato FM, Szychlinska MA, Imbesi R, Castrogiovanni P, Loreto C et al (2017) Molecular links between diabetes and osteoarthritis: the role of physical activity. Curr Diabetes Rev 13:50–58CrossRefGoogle Scholar
  19. 19.
    Roubenoff R (2007) Physical activity, inflammation, and muscle loss. Nutr Rev 65:S208-12CrossRefGoogle Scholar
  20. 20.
    Szychlinska MA, Trovato FM, Di Rosa M, Malaguarnera L, Puzzo L, Leonardi R et al (2016) Co-expression and co-localization of cartilage glycoproteins CHI3L1 and Lubricin in osteoarthritic cartilage: morphological, immunohistochemical and gene expression profiles. Int J Mol Sci 17:359CrossRefGoogle Scholar
  21. 21.
    Altiok E, Bayçin D, Bayraktar O, Ülkü S (2008) Isolation of polyphenols from the extracts of olive leaves (Olea europaea L.) by adsorption on silk fibroin. Sep Purif Technol 62:342–348CrossRefGoogle Scholar
  22. 22.
    Barbieri S, Bendini A, Valli E, Gallina-Toschi T (2015) Do consumers recognize the positive sensorial attributes of extra virgin olive oils related with their composition? A case study on conventional and organic products. J Food Compost Anal 44:186–195CrossRefGoogle Scholar
  23. 23.
    Musumeci G, Castrogiovanni P, Trovato FM, Imbesi R, Giunta S, Szychlinska MA et al (2015) Physical activity ameliorates cartilage degeneration in a rat model of aging: a study on lubricin expression. Scand J Med Sci Sports 25:e222-30CrossRefGoogle Scholar
  24. 24.
    Musumeci G, Trovato FM, Pichler K, Weinberg AM, Loreto C, Castrogiovanni P (2013) Extra-virgin olive oil diet and mild physical activity prevent cartilage degeneration in an osteoarthritis model: an in vivo and in vitro study on lubricin expression. J Nutr Biochem 24:2064–2075CrossRefGoogle Scholar
  25. 25.
    Castrogiovanni P, Musumeci G, Trovato FM, Avola R, Magro G, Imbesi R (2014) Effects of high-tryptophan diet on pre- and postnatal development in rats: a morphological study. Eur J Nutr 53:297–308CrossRefGoogle Scholar
  26. 26.
    Musumeci G, Loreto C, Clementi G, Fiore CE, Martinez G (2011) An in vivo experimental study on osteopenia in diabetic rats. Acta Histochem 113:619–625CrossRefGoogle Scholar
  27. 27.
    Ostergaard K, Petersen J, Andersen CB, Bendtzen K, Salter DM (1997) Histologic/histochemical grading system for osteoarthritic articular cartilage: reproducibility and validity. Arthritis Rheum 40:1766–1771CrossRefGoogle Scholar
  28. 28.
    Gerwin N, Bendele AM, Glasson S, Carlson CS (2010) The OARSI histopathology initiative - recommendations for histological assessments of osteoarthritis in the rat. Osteoarthr Cartil 18:S24-34CrossRefGoogle Scholar
  29. 29.
    Musumeci G, Castrogiovanni P, Mazzone V, Szychlinska MA, Castorina S, Loreto C (2014) Histochemistry as a unique approach for investigating normal and osteoarthritic cartilage. Eur J Histochem 58:2371CrossRefGoogle Scholar
  30. 30.
    Loreto C, Lo Castro E, Musumeci G, Loreto F, Rapisarda G, Rezzani R (2012) Aquaporin 1 expression in human temporomandibular disc. Acta Histochem 114(7):744–748CrossRefGoogle Scholar
  31. 31.
    Kaneko S, Satoh T, Chiba J, Ju C, Inoue K, Kagawa J (2000) Interleukin-6 and interleukin-8 levels in serum and synovial fluid of patients with osteoarthritis. Cytokines Cell Mol Ther 6:71–79CrossRefGoogle Scholar
  32. 32.
    Livshits G, Zhai G, Hart DJ, Kato BS, Wang H, Williams FM et al (2009) Interleukin-6 is a significant predictor of radiographic knee osteoarthritis: the Chingford Study. Arthritis Rheum 60:2037–2045CrossRefGoogle Scholar
  33. 33.
    Nasi S, So A, Combes C, Daudon M, Busso N (2016) Interleukin-6 and chondrocyte mineralisation act in tandem to promote experimental osteoarthritis. Ann Rheum Dis 75:1372–1379CrossRefGoogle Scholar
  34. 34.
    Yang Y, Wang Y, Kong Y, Zhang X, Bai L (2017) The effects of different frequency treadmill exercise on lipoxin A4 and articular cartilage degeneration in an experimental model of monosodium iodoacetate-induced osteoarthritis in rats. PLoS One 12:e0179162CrossRefGoogle Scholar
  35. 35.
    Al-Hashem F, El Karib AO, Bin-Jaliah I, Dallak M, Sakr HF, Eid RA et al (2017) Exercise protects against insulin-dependent diabetes-induced osteoarthritis in rats: A scanning electron microscopy study. Ultrastruct Pathol 41:252–257CrossRefGoogle Scholar
  36. 36.
    King MR, Haussler KK, Kawcak CE, McIlwraith CW, Reiser RF, Frisbie DD et al (2017) Biomechanical and histologic evaluation of the effects of underwater treadmill exercise on horses with experimentally induced osteoarthritis of the middle carpal joint. Am J Vet Res 78:558–569CrossRefGoogle Scholar
  37. 37.
    Chang NJ, Lee KW, Chu CJ, Shie MY, Chou PH, Lin CC et al (2017) A preclinical assessment of early continuous passive motion and treadmill therapeutic exercises for generating chondroprotective effects after anterior cruciate ligament rupture. Am J Sports Med 45:2284–2293Google Scholar
  38. 38.
    Musumeci G, Trovato MF, Imbesi R, Castrogiovanni P (2014) Effects of dietary extra-virgin olive oil on oxidative stress resulting from exhaustive exercise in rat skeletal muscle: a morphological study. Acta Histochem 116:61–69CrossRefGoogle Scholar
  39. 39.
    Yarla NS, Polito A, Peluso I (2018) Effects of Olive Oil on TNF-α and IL-6 in Humans: Implication in Obesity and Frailty. Endocr Metab Immune Disord Drug Targets 18:63–74Google Scholar
  40. 40.
    Medina-Remón A, Casas R, Tressserra-Rimbau A, Ros E, Martínez-González MA, Fitó M et al (2017) PREDIMED. Study Investigators. Polyphenol intake from a Mediterranean diet decreases inflammatory biomarkers related to atherosclerosis: a substudy of the PREDIMED trial. Br J Clin Pharmacol 83:114–128CrossRefGoogle Scholar
  41. 41.
    Impellizzeri D, Esposito E, Mazzon E, Paterniti I, Di Paola R, Morittu VM et al (2011) Oleuropein aglycone, an olive oil compound, ameliorates development of arthritis caused by injection of collagen type II in mice. J Pharmacol Exp Ther 339:859–869CrossRefGoogle Scholar
  42. 42.
    Gong D, Geng C, Jiang L, Wang L, Yoshimura H, Zhong L (2012) Mechanisms of olive leaf extract-ameliorated rat arthritis caused by kaolin and carrageenan. Phytother Res Mar 26:397–402Google Scholar
  43. 43.
    Rosillo M, Alcaraz MJ, Sánchez-Hidalgo M, Fernández-Bolaños JG, Alarcón-de-la-Lastra C, Ferrándiz ML (2014) Anti-inflammatory and joint protective effects of extra-virgin olive-oil polyphenol extract in experimental arthritis. J Nutr Biochem 25:1275–1281CrossRefGoogle Scholar
  44. 44.
    Rosillo MA, Sánchez-Hidalgo M, González-Benjumea A, Fernández-Bolaños JG, Lubberts E, Alarcón-de-la-Lastra C (2015) Preventive effects of dietary hydroxytyrosol acetate, an extra virgin olive oil polyphenol in murine collagen-induced arthritis. Mol Nutr Food Res 59:2537–2546CrossRefGoogle Scholar
  45. 45.
    Rosillo MA, Sánchez-Hidalgo M, Sánchez-Fidalgo S, Aparicio-Soto M, Villegas I, Alarcón-de-la-Lastra C (2016) Dietary extra-virgin olive oil prevents inflammatory response and cartilage matrix degradation in murine collagen-induced arthritis. Eur J Nutr 55:315–325CrossRefGoogle Scholar
  46. 46.
    Hunter DJ, Eckstein F (2009) Exercise and osteoarthritis. J Anat 214:197–207CrossRefGoogle Scholar
  47. 47.
    Herzog W, Longino D (2007) The role of muscles in joint degeneration and osteoarthritis. J Biomech 40:S54-63CrossRefGoogle Scholar
  48. 48.
    Ikeda S, Tsumura H, Torisu T (2005) Age-related quadriceps-dominant muscle atrophy and incident radiographic knee osteoarthritis. J Orthop Sci 10:121–126CrossRefGoogle Scholar
  49. 49.
    Gutiérrez-Rosales F, Ríos JJ, Gómez-Rey ML (2003) Main polyphenols in the bitter taste of virgin olive oil. Structural confirmation by on-line high-performance liquid chromatography electrospray ionization mass spectrometry. J Agric Food Chem 51:6021–6025CrossRefGoogle Scholar
  50. 50.
    Bouayed J, Bohn T (2010) Exogenous antioxidants–double-edged swords in cellular redox state: Health beneficial effects at physiologic doses versus deleterious effects at high doses. Oxid Med Cell Longev 3:228–237CrossRefGoogle Scholar
  51. 51.
    Liu RH (2003) Health benefits of fruit and vegetables are from additive and synergistic combinations of phytochemicals. Am J Clin Nutr 78:517S-20SGoogle Scholar
  52. 52.
    Wang X, Li H, Zheng A, Yang L, Liu J, Chen C et al (2014) Mitochondrial dysfunction-associated OPA1 cleavage contributes to muscle degeneration: preventative effect of hydroxytyrosol acetate. Cell Death Dis 5:e1521CrossRefGoogle Scholar
  53. 53.
    Bronnikov GE, Kulagina TP, Aripovskii AV, Kramarova LI (2015) Correction of mitochondrial enzyme activities in the skeletal muscles of old rats in response to addition of olive oil to the ration. Bull Exp Biol Med 159:266–268CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Marta Anna Szychlinska
    • 1
  • Paola Castrogiovanni
    • 1
  • Francesca Maria Trovato
    • 2
  • Houda Nsir
    • 3
  • Mokhtar Zarrouk
    • 3
  • Debora Lo Furno
    • 4
  • Michelino Di Rosa
    • 1
  • Rosa Imbesi
    • 1
  • Giuseppe Musumeci
    • 1
    • 5
    • 6
  1. 1.Human Anatomy and Histology Section, Department of Biomedical and Biotechnological Sciences, School of MedicineUniversity of CataniaCataniaItaly
  2. 2.Department of Clinical and Experimental MedicineUniversity of CataniaCataniaItaly
  3. 3.Biotechnology Laboratory of olive Tree, Centre of Biotechnology of Borj CedreyaUniversity of CarthageCarthageTunisia
  4. 4.Section of Physiology, Department of Biomedical and Biotechnological SciencesUniversity of CataniaCataniaItaly
  5. 5.Department of Health, Institut des Etudes UniversitariesUniPoliSIVeyrasSwitzerland
  6. 6.School of the Sport of the Italian National Olympic Committee “CONI” SicilySicilyItaly

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