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Journal of Orthopaedic Surgery and Research

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Open Access 01-12-2018 | Research article

Effect of lycopene on titanium implant osseointegration in ovariectomized rats

Authors: Xiaojie Li, Wenli Xue, Yong Cao, Yanming Long, Mengsheng Xie

Published in: Journal of Orthopaedic Surgery and Research | Issue 1/2018

Abstract

Background

Lycopene prevents bone loss in osteopenic models. However, the role of lycopene in the success rate of dental implants under osteopenic conditions remains unknown. The aim of this study was to evaluate whether lycopene prevents delayed implant osseointegration in an ovariectomized (OVX) rat model.

Methods

Thirty female Sprague-Dawley rats were randomly divided into the following groups: OVX with vehicle (OVX group), OVX with lycopene (OVX + lycopene group) and sham-operated with vehicle (sham group). Twelve weeks after ovariectomy or sham operation, titanium implants were placed into the distal metaphysis of the bilateral femurs of each rat. These rats were subsequently gavaged with lycopene (50 mg/kg/day) or vehicle. After 12 weeks of gavage, all rats were sacrificed, and specimens were harvested. Sample osseointegration was evaluated by biomechanical testing, 3D micro-computed tomography (micro-CT) analysis and histomorphometric analysis.

Results

Compared with the OVX group, the OVX + lycopene group showed a 69.3% increase in the maximum push-out force (p < 0.01). Micro-CT data for the femurs in the OVX + lycopene group showed significantly higher bone volume, trabecular thickness and less trabecular space than did those in the OVX group. The bone area (BA) around the implant and bone contact (BC) with the implant were increased by 72.3% (p < 0.01) and 51.4% (p < 0.01) in the OVX + lycopene group, respectively, compared with those in the OVX group. There was no significant difference in the mechanical test, micro-CT scanning and histomorphometric data between the OVX + lycopene and sham groups (p > 0.05).

Conclusions

Lycopene improved implant osseointegration, fixation and bone formation under osteopenic conditions, suggesting that lycopene is a promising therapeutic agent to prevent delayed implant osseointegration and bone loss under osteopenic conditions.

Liddelow G, Klineberg I. Patient-related risk factors for implant therapy. A critique of pertinent literature. Aust Dent J. 2011;56(4):417–26; quiz 441. https://doi.org/10.1111/j.1834-7819.2011.01367.x.CrossRefPubMed

French D, Larjava H, Ofec R. Retrospective cohort study of 4591 Straumann implants in private practice setting, with up to 10-year follow-up. Part 1: multivariate survival analysis. Clin Oral Implants Res. 2015;26(11):1345–54. https://doi.org/10.1111/clr.12463.CrossRefPubMed

French D, Larjava H, Tallarico M. Retrospective study of 1087 anodized implants placed in private practice: risk indicators associated with implant failure and relationship between bone levels and soft tissue health. Implant Dent. 2018. https://doi.org/10.1097/id.0000000000000743.

Goiato MC, dos Santos DM, Santiago JF Jr, Moreno A, Pellizzer EP. Longevity of dental implants in type IV bone: a systematic review. Int J Oral Maxillofac Surg. 2014;43(9):1108–16. https://doi.org/10.1016/j.ijom.2014.02.016.CrossRefPubMed

Phetfong J, Sanvoranart T, Nartprayut K, Nimsanor N, Seenprachawong K, Prachayasittikul V, Supokawej A. Osteoporosis: the current status of mesenchymal stem cell-based therapy. Cell Mol Biol Lett. 2016;21:12. https://doi.org/10.1186/s11658-016-0013-1.CrossRefPubMedPubMedCentral

Giro G, Chambrone L, Goldstein A, Rodrigues JA, Zenobio E, Feres M, Figueiredo LC, Cassoni A, Shibli JA. Impact of osteoporosis in dental implants: a systematic review. World J Orthop. 2015;6(2):311–5. https://doi.org/10.5312/wjo.v6.i2.311.CrossRefPubMedPubMedCentral

de Medeiros F, Kudo GAH, Leme BG, Saraiva PP, Verri FR, Honorio HM, Pellizzer EP, Santiago Junior JF. Dental implants in patients with osteoporosis: a systematic review with meta-analysis. Int J Oral Maxillofac Surg. 2018;47(4):480–91. https://doi.org/10.1016/j.ijom.2017.05.021.CrossRefPubMed

Merheb J, Temmerman A, Rasmusson L, Kubler A, Thor A, Quirynen M. Influence of skeletal and local bone density on dental implant stability in patients with osteoporosis. Clin Implant Dent Relat Res. 2016;18(2):253–60. https://doi.org/10.1111/cid.12290.CrossRefPubMed

Aro HT, Alm JJ, Moritz N, Makinen TJ, Lankinen P. Low BMD affects initial stability and delays stem osseointegration in cementless total hip arthroplasty in women: a 2-year RSA study of 39 patients. Acta Orthop. 2012;83(2):107–14. https://doi.org/10.3109/17453674.2012.678798.CrossRefPubMedPubMedCentral

10.

Mavrogenis AF, Dimitriou R, Parvizi J, Babis GC. Biology of implant osseointegration. J Musculoskelet Neuronal Interact. 2009;9(2):61–71.PubMed

11.

Li Y, He S, Hua Y, Hu J. Effect of osteoporosis on fixation of osseointegrated implants in rats. J Biomed Mater Res B Appl Biomater. 2017;105(8):2426–32. https://doi.org/10.1002/jbm.b.33787.CrossRefPubMed

12.

Ross RD, Hamilton JL, Wilson BM, Sumner DR, Virdi AS. Pharmacologic augmentation of implant fixation in osteopenic bone. Curr Osteoporos Rep. 2014;12(1):55–64. https://doi.org/10.1007/s11914-013-0182-z.CrossRefPubMed

13.

Khan M, Cheung AM, Khan AA. Drug-related adverse events of osteoporosis therapy. Endocrinol Metab Clin N Am. 2017;46(1):181–92. https://doi.org/10.1016/j.ecl.2016.09.009.CrossRef

14.

Prasad G, Dhillon MS, Khullar M, Nagi ON. Evaluation of oxidative stress after fractures. A preliminary study. Acta Orthop Belg. 2003;69(6):546–51.PubMed

15.

Sheweita SA, Khoshhal KI. Calcium metabolism and oxidative stress in bone fractures: role of antioxidants. Curr Drug Metab. 2007;8(5):519–25.CrossRef

16.

Bednarek-Tupikowska G, Tworowska U, Jedrychowska I, Radomska B, Tupikowski K, Bidzinska-Speichert B, Milewicz A. Effects of oestradiol and oestroprogestin on erythrocyte antioxidative enzyme system activity in postmenopausal women. Clin Endocrinol. 2006;64(4):463–8. https://doi.org/10.1111/j.1365-2265.2006.02494.x.CrossRef

17.

Ilyas A, Odatsu T, Shah A, Monte F, Kim HK, Kramer P, Aswath PB, Varanasi VG. Amorphous silica: a new antioxidant role for rapid critical-sized bone defect healing. Adv Healthc Mater. 2016;5(17):2199–213. https://doi.org/10.1002/adhm.201600203.CrossRefPubMed

18.

De Franca NA, Camargo MB, Lazaretti-Castro M, Martini LA. Antioxidant intake and bone status in a cross-sectional study of Brazilian women with osteoporosis. Nutr Health. 2013;22(2):133–42. https://doi.org/10.1177/0260106014563445.CrossRefPubMed

19.

Zhang J, Munger RG, West NA, Cutler DR, Wengreen HJ, Corcoran CD. Antioxidant intake and risk of osteoporotic hip fracture in Utah: an effect modified by smoking status. Am J Epidemiol. 2006;163(1):9–17. https://doi.org/10.1093/aje/kwj005.CrossRefPubMed

20.

Wang XD. Lycopene metabolism and its biological significance. Am J Clin Nutr. 2012;96(5):1214S–22S. https://doi.org/10.3945/ajcn.111.032359.CrossRefPubMedPubMedCentral

21.

Rao AV, Rao LG. Carotenoids and human health. Pharmacol Res. 2007;55(3):207–16. https://doi.org/10.1016/j.phrs.2007.01.012.CrossRefPubMed

22.

Kelkel M, Schumacher M, Dicato M, Diederich M. Antioxidant and anti-proliferative properties of lycopene. Free Radic Res. 2011;45(8):925–40. https://doi.org/10.3109/10715762.2011.564168.CrossRefPubMed

23.

Mackinnon ES, Rao AV, Rao LG. Dietary restriction of lycopene for a period of one month resulted in significantly increased biomarkers of oxidative stress and bone resorption in postmenopausal women. J Nutr Health Aging. 2011;15(2):133–8.CrossRef

24.

Mackinnon ES, Rao AV, Josse RG, Rao LG. Supplementation with the antioxidant lycopene significantly decreases oxidative stress parameters and the bone resorption marker N-telopeptide of type I collagen in postmenopausal women. Osteoporos Int. 2011;22(4):1091–101. https://doi.org/10.1007/s00198-010-1308-0.CrossRefPubMed

25.

Sahni S, Hannan MT, Blumberg J, Cupples LA, Kiel DP, Tucker KL. Protective effect of total carotenoid and lycopene intake on the risk of hip fracture: a 17-year follow-up from the Framingham Osteoporosis Study. J Bone Miner Res. 2009;24(6):1086–94. https://doi.org/10.1359/jbmr.090102.CrossRefPubMedPubMedCentral

26.

Ardawi MS, Badawoud MH, Hassan SM, Rouzi AA, Ardawi JM, AlNosani NM, Qari MH, Mousa SA. Lycopene treatment against loss of bone mass, microarchitecture and strength in relation to regulatory mechanisms in a postmenopausal osteoporosis model. Bone. 2016;83:127–40. https://doi.org/10.1016/j.bone.2015.10.017.CrossRefPubMed

27.

Yamazaki I, Yamaguchi H. Characteristics of an ovariectomized osteopenic rat model. J Bone Miner Res. 1989;4(1):13–22. https://doi.org/10.1002/jbmr.5650040104.CrossRefPubMed

28.

Ozawa S, Ogawa T, Iida K, Sukotjo C, Hasegawa H, Nishimura RD, Nishimura I. Ovariectomy hinders the early stage of bone-implant integration: histomorphometric, biomechanical, and molecular analyses. Bone. 2002;30(1):137–43.CrossRef

29.

Duarte PM, Cesar Neto JB, Goncalves PF, Sallum EA, Nociti j F. Estrogen deficiency affects bone healing around titanium implants: a histometric study in rats. Implant Dent. 2003;12(4):340–6.CrossRef

30.

Alghamdi HS, van den Beucken JJ, Jansen JA. Osteoporotic rat models for evaluation of osseointegration of bone implants. Tissue Eng Part C Methods. 2014;20(6):493–505. https://doi.org/10.1089/ten.TEC.2013.0327.CrossRefPubMed

31.

Alghamdi HS, Cuijpers VM, Wolke JG, van den Beucken JJ, Jansen JA. Calcium-phosphate-coated oral implants promote osseointegration in osteoporosis. J Dent Res. 2013;92(11):982–8. https://doi.org/10.1177/0022034513505769.CrossRefPubMed

32.

Ying G, Bo L, Yanjun J, Lina W, Binquan W. Effect of a local, one time, low-dose injection of zoledronic acid on titanium implant osseointegration in ovariectomized rats. Arc Med Sci. 2016;12(5):941–9. https://doi.org/10.5114/aoms.2016.61908.CrossRef

33.

Edwards MH, Dennison EM, Aihie Sayer A, Fielding R, Cooper C. Osteoporosis and sarcopenia in older age. Bone. 2015;80:126–30. https://doi.org/10.1016/j.bone.2015.04.016.CrossRefPubMedPubMedCentral

34.

Virdi AS, Irish J, Sena K, Liu M, Ke HZ, McNulty MA, Sumner DR. Sclerostin antibody treatment improves implant fixation in a model of severe osteoporosis. J Bone Joint Surg Am. 2015;97(2):133–40. https://doi.org/10.2106/JBJS.N.00654.CrossRefPubMed

35.

Johnston BD, Ward WE. The ovariectomized rat as a model for studying alveolar bone loss in postmenopausal women. Biomed Res Int. 2015;2015:635023. https://doi.org/10.1155/2015/635023.CrossRefPubMedPubMedCentral

36.

Gao Y, Luo E, Hu J, Xue J, Zhu S, Li J. Effect of combined local treatment with zoledronic acid and basic fibroblast growth factor on implant fixation in ovariectomized rats. Bone. 2009;44(2):225–32. https://doi.org/10.1016/j.bone.2008.10.054.CrossRefPubMed

37.

Dikicier E, Karacayli U, Dikicier S, Gunaydin Y. Effect of systemic administered zoledronic acid on osseointegration of a titanium implant in ovariectomized rats. J Craniomaxillofac Surg. 2014;42(7):1106–11. https://doi.org/10.1016/j.jcms.2014.01.039.CrossRefPubMed

38.

Rao AV, Ray MR, Rao LG. Lycopene. Adv Food Nutr Res. 2006;51:99–164. https://doi.org/10.1016/s1043-4526(06)51002-2.CrossRefPubMed

39.

Mellert W, Deckardt K, Gembardt C, Schulte S, Van Ravenzwaay B, Slesinski R. Thirteen-week oral toxicity study of synthetic lycopene products in rats. Food Chem Toxicol. 2002;40(11):1581–8.CrossRef

40.

Michael McClain R, Bausch J. Summary of safety studies conducted with synthetic lycopene. Regul Toxicol Pharmacol. 2003;37(2):274–85.CrossRef

41.

Rao LG, Mackinnon ES, Josse RG, Murray TM, Strauss A, Rao AV. Lycopene consumption decreases oxidative stress and bone resorption markers in postmenopausal women. Osteoporos Int. 2007;18(1):109–15. https://doi.org/10.1007/s00198-006-0205-z.CrossRefPubMed

42.

Liang H, Yu F, Tong Z, Zeng W. Lycopene effects on serum mineral elements and bone strength in rats. Molecules. 2012;17(6):7093–102. https://doi.org/10.3390/molecules17067093.CrossRefPubMed

43.

Iimura Y, Agata U, Takeda S, Kobayashi Y, Yoshida S, Ezawa I, Omi N. The protective effect of lycopene intake on bone loss in ovariectomized rats. J Bone Miner Metab. 2015;33(3):270–8. https://doi.org/10.1007/s00774-014-0596-4.CrossRefPubMed

44.

Kim L, Rao AV, Rao LG. Lycopene II--effect on osteoblasts: the carotenoid lycopene stimulates cell proliferation and alkaline phosphatase activity of SaOS-2 cells. J Med Food. 2003;6(2):79–86. https://doi.org/10.1089/109662003322233468.CrossRefPubMed

45.

Rao LG, Krishnadev N, Banasikowska K, Rao AV. Lycopene I--effect on osteoclasts: lycopene inhibits basal and parathyroid hormone-stimulated osteoclast formation and mineral resorption mediated by reactive oxygen species in rat bone marrow cultures. J Med Food. 2003;6(2):69–78. https://doi.org/10.1089/109662003322233459.CrossRefPubMed

46.

Liu Y, Hu J, Liu B, Jiang X, Li Y. The effect of osteoprotegerin on implant osseointegration in ovariectomized rats. Arch Med Sci. 2017;13(2):489–95. https://doi.org/10.5114/aoms.2017.65468.CrossRefPubMedPubMedCentral

47.

Veprik A, Khanin M, Linnewiel-Hermoni K, Danilenko M, Levy J, Sharoni Y. Polyphenols, isothiocyanates, and carotenoid derivatives enhance estrogenic activity in bone cells but inhibit it in breast cancer cells. Am J Phys Endocrinol Metab. 2012;303(7):E815–24. https://doi.org/10.1152/ajpendo.00142.2011.CrossRef

Title: Effect of lycopene on titanium implant osseointegration in ovariectomized rats
Authors: Xiaojie Li
Wenli Xue
Yong Cao
Yanming Long
Mengsheng Xie
Publication date: 01-12-2018
Publisher: BioMed Central
Published in: Journal of Orthopaedic Surgery and Research / Issue 1/2018
Electronic ISSN: 1749-799X
DOI: https://doi.org/10.1186/s13018-018-0944-5

At a glance: The STEP trials

Springer Medicine

Effect of lycopene on titanium implant osseointegration in ovariectomized rats

Abstract

Background

Methods

Results

Conclusions

At a glance: The STEP trials

Springer Medicine

Abstract

Background

Methods

Results

Conclusions

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