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Investigation of the Effect of Linoleic Acid on Vascularization in Experimentally Induce Zoledronic Acid-Related Osteonecrosis in Rats

Year 2021, Volume: 6 Issue: 3, 122 - 126, 31.12.2021
https://doi.org/10.24880/maeuvfd.970180

Abstract

Bisphosphonate-related osteonecrosis of the jaw (BRONJ) is an increasingly common pathological condition whose pathophysiology is not fully understood and can be difficult to manage. The unique biological effects of conjugated linoleic acid (CLA) include angiogenic, anticarcinogenic, antiatherosclerotic, antioxidative, immunomodulative and antibacterial effects. The aim of this study is to compare the osteonecrosis areas created by tooth extraction with the control group using scanning electron microscopy (SEM) after the administration of zoledronic acid (ZA), CLA and a combination of both in the rat jaw. A total of 50 Wistar Albino male rats weighing 400-450 grams were used. The groups were randomly divided into 5 groups: the control group, the sham group, the group that received ZA, the groups that received CLA with ZA (100 mg / kg and 200 mg / kg), and the study lasted a total of 10 weeks. Regardless of the use of ZA, it was observed by SEM that vascularization was impaired in all groups with tooth extraction. Neovascularization did not occur in the groups where CLA was applied, regardless of the dose. It was concluded that SEM analysis and corrosion casts technique can be considered as an alternative method in such studies due to its accessibility and low cost in observing dental vascularization. However, no definite conclusion could be reached about the neovascularization efficiency of CLA within the period evaluated after tooth extraction.

Supporting Institution

Hatay Mustafa Kemal University

Project Number

Project No: 19.M.058

Thanks

The authors would like to thank undergraduate students Yusuf Bal and Özlem Güzey for their support during the feeding of the rats. This study was supported by Hatay Mustafa Kemal University Scientific Research Projects (BAP) (Project No: 19.M.058). This study was supported by Hatay Mustafa Kemal University Scientific Research Projects (BAP) (Project No: 19.M.058).

References

  • 1. Rodan GA, Fleisch HA. Bisphosphonates: mechanisms of action. J Clin Invest. 1996;97:2692-6.
  • 2. Lewiecki EM. Safety of long-term bisphosphonate therapy for the management of osteoporosis. Drugs. 2011;71:791-814.
  • 3. Harrington JT, Ste-Marie LG, Brandi ML, Civitelli R, Fardellone P, Grauer A, et al. Risedronate rapidly reduces the risk for nonvertebral fractures in women with postmenopausal osteoporosis. Calcif Tissue Int. 2004;74:129–35.
  • 4. Pols HA, Felsenberg D, Hanley DA, Stepán J, Muñoz-Torres M, Wilkin TJ, et al. Multinational, placebo-controlled, randomized trial of the effects of alendronate on bone density and fracture risk in postmenopausal women with low bone mass: results of the FOSIT study. Fosamax International Trial Study Group. Osteoporos Int. 1999;9(5):461-8.
  • 5. Vahtsevanos K, Kyrgidis A, Verrou E, Katodritou E, Triaridis S, Andreadis CG, et al. Longitudinal cohort study of risk factors in cancer patients of bisphosphonate-related osteonecrosis of the jaw. J Clin Oncol. 2009;27(32):5356-62.
  • 6. Walter C, Al-Nawas B, Frickhofen N, GammH, Beck J, Reinsch L, et al. Prevalence of bisphosphonate associated osteonecrosis of the jaws in multiple myeloma patients. Head Face Med. 2010;6:11.
  • 7. Woo SB, Hellstein JW, Kalmar JR. Narrative [corrected] review: bisphosphonates and osteonecrosis of the jaws. Ann Intern Med. 2006;144:753–61.
  • 8. Ruggiero SL, Dodson TB, Assael LA, Landesberg R, Marx RE, Mehrotra B; Task Force on Bisphosphonate-Related Osteonecrosis of the Jaws, American Association of Oral and Maxillofacial Surgeons. American Association of Oral and Maxillofacial Surgeons position paper on bisphosphonate-related osteonecrosis of the jaw - 2009 update. Aust Endod J. 2009;35(3):119-30.
  • 9. Marx RE, Cillo JE Jr, Ulloa JJ. Oral bisphosphonate-induced osteonecrosis: risk factors, prediction of risk using serum CTX testing, prevention, and treatment. J Oral Maxillofac Surg. 2007;65:2397–410.
  • 10. Marx RE, Sawatari Y, Fortin M, Broumand V. Bisphosphonate-induced exposed bone (osteonecrosis/osteopetrosis) of the jaws: risk factors, recognition, prevention, and treatment. J Oral Maxillofac Surg. 2005;63:1567–75.
  • 11. Boonyapakorn T, Schirmer I, Reichart PA, Sturm I, Massenkeil G. Bisphosphonate-induced osteonecrosis of the jaws: prospective study of 80 patients with multiple myeloma and other malignancies. Oral Oncol. 2008;44:857–69.
  • 12. Pabst A, Ziebart T, Ackermann M, Konerding M, Walter C. Bisphosphonates’ Antiangiogenic Potency in the Development of Bisphosphonate-Associated Osteonecrosis of the Jaws: Influence on Microvessel Sprouting in an in Vivo 3d Matrigel Assay. Clin Oral Investig 2014;18(3):1015-22.
  • 13. Petcu EB, Ivanovski S, Wright RG, Slevin M, Miroiu RI, Brinzaniuc K. Bisphosphonate-related osteonecrosis of jaw (BRONJ): an anti-angiogenic side-effect? Diagn Pathol. 2012;7:78.
  • 14. Sharma D, Ivanovski S, Slevin M, Hamlet S, Pop TS, Brinzaniuc K, et al. Bisphosphonate related osteonecrosis of jaw (BRONJ): diagnostic criteria and possible pathogenic mechanisms of an unexpected antiangiogenic side effect. Vasc Cell. 2013;5(1):1.
  • 15. Wehrhan F, Stockmann P, Nkenke E, Schlegel KA, Guentsch A, Wehrhan T, et al. Differential impairment of vascularization and angiogenesis in bisphosphonate-associated osteonecrosis of the jaw-related mucoperiosteal tissue. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2011;112:216–21.
  • 16. Stresing V, Fournier PG, Bellahcene A, Benzaid I, Monkkonen H, Colombel M, et al. Nitrogen-containing bisphosphonates can inhibit angiogenesis in vivo without the involvement of farnesyl pyrophosphate synthase. Bone. 2011;48:259–66.
  • 17. Rasmusson L, Abtahi J. Bisphosphonate associated osteonecrosis of the jaw: an update on pathophysiology, risk factors, and treatment. Int J Dent. 2014:471035.
  • 18. Reid IR, Bolland MJ, Grey AB. Is bisphosphonate associated osteonecrosis of the jaw caused by soft tissue toxicity? Bone. 2007;41:318–20.
  • 19. Risérus U, Arner P, Brisman K, Vessby B. Treatment with dietary trans 10 cis 12 conjugated linoleic acid causes isomer-spesific insulin resistance in obese men with the metabolic syndrome. Diabetes Care. 2002;25(9):1516-21.
  • 20. Ercoşkun H, Uğuz Ş, Kıralan M. Conjugated linoleic acid. Gıda Mühendisliği Dergisi 2005;(19):42-6.
  • 21. Samson FP, Patrick AT, Fabunmi TE, Yahaya MF, Madu J, He W, et al. Oleic Acid, Cholesterol, and Linoleic Acid as Angiogenesis Initiators. ACS Omega. 2020;5:20575-85.
  • 22. Camacho-Alonso F, López-Jornet P, Vicente-Hernández A. Short-term effect of zoledronic acid upon fracture resistance of the mandibular condyle and femoral head in an animal model. Med Oral Patol Oral Cir Bucal. 2013;18:421-6.
  • 23. Kün-Darbois J-D, Libouban H, Mabilleau G, Pascaretti-Grizon F, Chappard D. Bone Mineralization and Vascularization in Bisphosphonate-Related Osteonecrosis of the Jaw: An ExperimentalStudy in the Rat. Clin Oral Investig. 2018;22(9):2997-3006.
  • 24. Geddes RI, Hayashi K, Bongers Q, Wehber M, Anderson IM, Jansen AD, et al. Conjugated Linoleic Acid Administration Induces Amnesia in Male Sprague Dawley Rats and Exacerbates Recovery from Functional Deficits Induced by a Controlled Cortical Impact Injury. PLoSOne. 2017;12(1):e0169494.
  • 25. Dodson TB. Intravenous bisphosphonate therapy and bisphosphonate-related osteonecrosis of the jaws. J Oral Maxillofac Surg. 2009;67(5):44–52.
  • 26. Barba-Recreo P, Del Castillo Pardo de Vera JL, García-Arranz M, Yébenes L, Burgueño M. Zoledronic acid - related osteonecrosis of the jaws. Experimental model with dental extractions in rats. J Craniomaxillofac Surg. 2014;42(6):744-50.
  • 27. Conte Neto N, Spolidorio LC, Andrade CR, Bastos AS, Guimaraes M, Marcantonio E Jr. Experimental development of bisphosphonate-related osteonecrosis of the jaws in rodents. Int J Exp Pathol. 2013;94:65–73.
  • 28. Lopez-Jornet P, Camacho-Alonso F, Molina-Minano F, Gomez-Garcia F, Vicente-Ortega V. An experimental study of bisphosphonate-induced jaws osteonecrosis in Sprague Dawley rats. J Oral Pathol Med. 2010;39:697–702.
  • 29. Biasotto M, Chiandussi S, Zacchigna S, Moimas S, Dore F, Pozzato G, et al. A novel animal model to study non-spontaneous bisphosphonates osteonecrosis of jaw. J Oral Pathol Med. 2010;39(5):390-6.
  • 30. Hoff AO, Toth BB, Altundag K, Johnson MM, Warneke CL, Hu M, et al. Frequency and risk factors associated with osteonecrosis of the jaw in cancer patients treated with intravenous bisphosphonates. J Bone Miner Res. 2008;23(6):826-36.
  • 31. Ficarra G, Beninati F. Bisphosphonte-related osteonecrosis of the jaws: the point of view of the oral pathologist. Clin Cases Miner Bone Metab. 2007;4:53-7.
  • 32. Bedogni A, Blandamura S, Lokmic Z, Palumbo C, Ragazzo M, Ferrari F, et al. Bisphosphonate-Associated Jaw bone Osteonecrosis: A Correlation between Imaging Techniques and Histopathology. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2008;105(3):358-64.
  • 33. Arce K, Assael LA, Weissman JL, Markiewicz MR. Imaging findings in bisphosphonate-related osteonecrosis of jaws. J Oral Maxillofac Surg. 2009;67(5):75-84.
  • 34. Lametschwandtner A, Lametschwandtner U, Weiger T. Scanning electron microscopy of vascular corrosion casts--technique and applications: updated review. Scanning Microsc. 1990;4(4):889-940; discussion 941.
  • 35. Verli FD, Rossi‐Schneider TR, Schneider FL, Yurgel LS, de Souza MAL. Vascular Corrosion Casting Technique Steps. Scanning. 2007; 29(3):128-32.
  • 36. Aharinejad S, Franz P, Firbas W, Fakhari M. Mandibular and molar vascularization in guinea pigs. Scanning electron microscopic study of corrosion casts. Anat Rec. 1990;228(4):471-7.
  • 37. Yoshida S, Ohshima H, Kobayashi S. Vascularization of the enamel organ in developing molar teeth of rats – scanning electron microscope study of corrosion casts. Okajimas Folia Anat Jpn. 1989;66:99–112.
  • 38. Tsukada H, Ishikawa H, Nakamura S, Yoshida S. Developmental changes of the vasculature in the periodontal ligament of rat molars: a scanning electron microscopic study of microcorrosion casts. J Periodontal Res. 2000;35:201–7.
  • 39. Selliseth NJ, Selvig KA. Microvasculature of the dorsum of the rat tongue: a scanning electron microscopic study using corrosion casts. Scand J Dent Res. 1993;101(6):391-7.
  • 40. Selliseth NJ, Selvig KA. The vasculature of the periodontal ligament. A scanning electron microscopic study using corrosion casts in the rat. J Periodontol. 1994:65:1079-87.
  • 41. Rossi-Schneider TR, Verli FD, Yurgel LS, De Souza MA, Cherubini K. Contribution to the study of the vasculature of submandibular and sublingual glands and lymph nodes of rats by corrosion cast technique combined with scanning electron microscopy. Microsc Res Tech. 2008;71(10):737-41.
  • 42. Aghaloo TL, Kang B, Sung EC, Shoff M, Ronconi M, Gotcher JE, et al. Periodontal disease and bisphosphonates induce osteonecrosis of the jaws in the rat. J Bone Miner Res. 2011;26:1871–82.
  • 43. Chung WO, Dommisch H, Yin L, Dale BA. Expression of defensins in gingiva and their role in periodontal health and disease. Curr Pharm Des. 2007;13:3073–83.
  • 44. Slade GD, Beck JD. Plausibility of periodontal disease estimates from NHANES III. J Public Health Dent. 1999;59:67–72.
  • 45. Taubman MA, Nash DA. The scientific and public-health imperative for a vaccine against dental caries. Nat Rev Immunol. 2006;6:555–63.
  • 46. Allen MR, Burr DB. The pathogenesis of bisphosphonate-related osteonecrosis of the jaw: so many hypotheses, so few data. J Oral Maxillofac Surg. 2009;67(5):61–70.
  • 47. Samson FP, Fabunmi TE, Patrick AT, Jee D, Gutsaeva DR, Jahng WJ. Fatty Acid Composition and Stoichiometry Determine the Angiogenesis Microenvironment. ACS Omega 2021.https://dx.doi.org/10.1021/acsomega.1c00196
  • 48. Kang JX, Liu A. The role of the tissue omega-6/omega-3 fatty acid ratio in regulating tumor angiogenesis. Cancer Metastasis Rev. 2013;32:201–10.
  • 49. Wang QY, Dai J, Kuang B, Zhang J, Yu SB, Duan YZ, Wang MQ. Osteochondral angiogenesis in rat mandibular condyles with osteoarthritis-like changes. Arch Oral Biol. 2012;57(6):620-9.
  • 50. Widyastuti, Rubianto M, Soetjipto. Induction of Angiogenesis Process in Mandible Using Anadara granosa Shell Graft (Experimental Laboratory Study on Rattus norvegicus). In: IOP Conference Series: Earth and Environmental Science. IOP Publishing 2018;217:012033.
  • 51. Luthfi M, Juliastuti WS, Risky YA, Wijayanti EH, Rachmawati AE, Asyhari NPO. Expression of fibroblast cells after extraction of wistar rat teeth after topical application of okra fruit (Abelmoschus esculentus) gel. Infect Dis Rep. 2020;12(1):8726.
  • 52. Rowe NM, Mehara BJ, Luchs JS, Dudziak ME, Steinbrech DS, Illei PB, et al. Angiogenesis during mandibular distraction osteogenesis. Ann Plast Surg. 1999;42:470–5.
Year 2021, Volume: 6 Issue: 3, 122 - 126, 31.12.2021
https://doi.org/10.24880/maeuvfd.970180

Abstract

Project Number

Project No: 19.M.058

References

  • 1. Rodan GA, Fleisch HA. Bisphosphonates: mechanisms of action. J Clin Invest. 1996;97:2692-6.
  • 2. Lewiecki EM. Safety of long-term bisphosphonate therapy for the management of osteoporosis. Drugs. 2011;71:791-814.
  • 3. Harrington JT, Ste-Marie LG, Brandi ML, Civitelli R, Fardellone P, Grauer A, et al. Risedronate rapidly reduces the risk for nonvertebral fractures in women with postmenopausal osteoporosis. Calcif Tissue Int. 2004;74:129–35.
  • 4. Pols HA, Felsenberg D, Hanley DA, Stepán J, Muñoz-Torres M, Wilkin TJ, et al. Multinational, placebo-controlled, randomized trial of the effects of alendronate on bone density and fracture risk in postmenopausal women with low bone mass: results of the FOSIT study. Fosamax International Trial Study Group. Osteoporos Int. 1999;9(5):461-8.
  • 5. Vahtsevanos K, Kyrgidis A, Verrou E, Katodritou E, Triaridis S, Andreadis CG, et al. Longitudinal cohort study of risk factors in cancer patients of bisphosphonate-related osteonecrosis of the jaw. J Clin Oncol. 2009;27(32):5356-62.
  • 6. Walter C, Al-Nawas B, Frickhofen N, GammH, Beck J, Reinsch L, et al. Prevalence of bisphosphonate associated osteonecrosis of the jaws in multiple myeloma patients. Head Face Med. 2010;6:11.
  • 7. Woo SB, Hellstein JW, Kalmar JR. Narrative [corrected] review: bisphosphonates and osteonecrosis of the jaws. Ann Intern Med. 2006;144:753–61.
  • 8. Ruggiero SL, Dodson TB, Assael LA, Landesberg R, Marx RE, Mehrotra B; Task Force on Bisphosphonate-Related Osteonecrosis of the Jaws, American Association of Oral and Maxillofacial Surgeons. American Association of Oral and Maxillofacial Surgeons position paper on bisphosphonate-related osteonecrosis of the jaw - 2009 update. Aust Endod J. 2009;35(3):119-30.
  • 9. Marx RE, Cillo JE Jr, Ulloa JJ. Oral bisphosphonate-induced osteonecrosis: risk factors, prediction of risk using serum CTX testing, prevention, and treatment. J Oral Maxillofac Surg. 2007;65:2397–410.
  • 10. Marx RE, Sawatari Y, Fortin M, Broumand V. Bisphosphonate-induced exposed bone (osteonecrosis/osteopetrosis) of the jaws: risk factors, recognition, prevention, and treatment. J Oral Maxillofac Surg. 2005;63:1567–75.
  • 11. Boonyapakorn T, Schirmer I, Reichart PA, Sturm I, Massenkeil G. Bisphosphonate-induced osteonecrosis of the jaws: prospective study of 80 patients with multiple myeloma and other malignancies. Oral Oncol. 2008;44:857–69.
  • 12. Pabst A, Ziebart T, Ackermann M, Konerding M, Walter C. Bisphosphonates’ Antiangiogenic Potency in the Development of Bisphosphonate-Associated Osteonecrosis of the Jaws: Influence on Microvessel Sprouting in an in Vivo 3d Matrigel Assay. Clin Oral Investig 2014;18(3):1015-22.
  • 13. Petcu EB, Ivanovski S, Wright RG, Slevin M, Miroiu RI, Brinzaniuc K. Bisphosphonate-related osteonecrosis of jaw (BRONJ): an anti-angiogenic side-effect? Diagn Pathol. 2012;7:78.
  • 14. Sharma D, Ivanovski S, Slevin M, Hamlet S, Pop TS, Brinzaniuc K, et al. Bisphosphonate related osteonecrosis of jaw (BRONJ): diagnostic criteria and possible pathogenic mechanisms of an unexpected antiangiogenic side effect. Vasc Cell. 2013;5(1):1.
  • 15. Wehrhan F, Stockmann P, Nkenke E, Schlegel KA, Guentsch A, Wehrhan T, et al. Differential impairment of vascularization and angiogenesis in bisphosphonate-associated osteonecrosis of the jaw-related mucoperiosteal tissue. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2011;112:216–21.
  • 16. Stresing V, Fournier PG, Bellahcene A, Benzaid I, Monkkonen H, Colombel M, et al. Nitrogen-containing bisphosphonates can inhibit angiogenesis in vivo without the involvement of farnesyl pyrophosphate synthase. Bone. 2011;48:259–66.
  • 17. Rasmusson L, Abtahi J. Bisphosphonate associated osteonecrosis of the jaw: an update on pathophysiology, risk factors, and treatment. Int J Dent. 2014:471035.
  • 18. Reid IR, Bolland MJ, Grey AB. Is bisphosphonate associated osteonecrosis of the jaw caused by soft tissue toxicity? Bone. 2007;41:318–20.
  • 19. Risérus U, Arner P, Brisman K, Vessby B. Treatment with dietary trans 10 cis 12 conjugated linoleic acid causes isomer-spesific insulin resistance in obese men with the metabolic syndrome. Diabetes Care. 2002;25(9):1516-21.
  • 20. Ercoşkun H, Uğuz Ş, Kıralan M. Conjugated linoleic acid. Gıda Mühendisliği Dergisi 2005;(19):42-6.
  • 21. Samson FP, Patrick AT, Fabunmi TE, Yahaya MF, Madu J, He W, et al. Oleic Acid, Cholesterol, and Linoleic Acid as Angiogenesis Initiators. ACS Omega. 2020;5:20575-85.
  • 22. Camacho-Alonso F, López-Jornet P, Vicente-Hernández A. Short-term effect of zoledronic acid upon fracture resistance of the mandibular condyle and femoral head in an animal model. Med Oral Patol Oral Cir Bucal. 2013;18:421-6.
  • 23. Kün-Darbois J-D, Libouban H, Mabilleau G, Pascaretti-Grizon F, Chappard D. Bone Mineralization and Vascularization in Bisphosphonate-Related Osteonecrosis of the Jaw: An ExperimentalStudy in the Rat. Clin Oral Investig. 2018;22(9):2997-3006.
  • 24. Geddes RI, Hayashi K, Bongers Q, Wehber M, Anderson IM, Jansen AD, et al. Conjugated Linoleic Acid Administration Induces Amnesia in Male Sprague Dawley Rats and Exacerbates Recovery from Functional Deficits Induced by a Controlled Cortical Impact Injury. PLoSOne. 2017;12(1):e0169494.
  • 25. Dodson TB. Intravenous bisphosphonate therapy and bisphosphonate-related osteonecrosis of the jaws. J Oral Maxillofac Surg. 2009;67(5):44–52.
  • 26. Barba-Recreo P, Del Castillo Pardo de Vera JL, García-Arranz M, Yébenes L, Burgueño M. Zoledronic acid - related osteonecrosis of the jaws. Experimental model with dental extractions in rats. J Craniomaxillofac Surg. 2014;42(6):744-50.
  • 27. Conte Neto N, Spolidorio LC, Andrade CR, Bastos AS, Guimaraes M, Marcantonio E Jr. Experimental development of bisphosphonate-related osteonecrosis of the jaws in rodents. Int J Exp Pathol. 2013;94:65–73.
  • 28. Lopez-Jornet P, Camacho-Alonso F, Molina-Minano F, Gomez-Garcia F, Vicente-Ortega V. An experimental study of bisphosphonate-induced jaws osteonecrosis in Sprague Dawley rats. J Oral Pathol Med. 2010;39:697–702.
  • 29. Biasotto M, Chiandussi S, Zacchigna S, Moimas S, Dore F, Pozzato G, et al. A novel animal model to study non-spontaneous bisphosphonates osteonecrosis of jaw. J Oral Pathol Med. 2010;39(5):390-6.
  • 30. Hoff AO, Toth BB, Altundag K, Johnson MM, Warneke CL, Hu M, et al. Frequency and risk factors associated with osteonecrosis of the jaw in cancer patients treated with intravenous bisphosphonates. J Bone Miner Res. 2008;23(6):826-36.
  • 31. Ficarra G, Beninati F. Bisphosphonte-related osteonecrosis of the jaws: the point of view of the oral pathologist. Clin Cases Miner Bone Metab. 2007;4:53-7.
  • 32. Bedogni A, Blandamura S, Lokmic Z, Palumbo C, Ragazzo M, Ferrari F, et al. Bisphosphonate-Associated Jaw bone Osteonecrosis: A Correlation between Imaging Techniques and Histopathology. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2008;105(3):358-64.
  • 33. Arce K, Assael LA, Weissman JL, Markiewicz MR. Imaging findings in bisphosphonate-related osteonecrosis of jaws. J Oral Maxillofac Surg. 2009;67(5):75-84.
  • 34. Lametschwandtner A, Lametschwandtner U, Weiger T. Scanning electron microscopy of vascular corrosion casts--technique and applications: updated review. Scanning Microsc. 1990;4(4):889-940; discussion 941.
  • 35. Verli FD, Rossi‐Schneider TR, Schneider FL, Yurgel LS, de Souza MAL. Vascular Corrosion Casting Technique Steps. Scanning. 2007; 29(3):128-32.
  • 36. Aharinejad S, Franz P, Firbas W, Fakhari M. Mandibular and molar vascularization in guinea pigs. Scanning electron microscopic study of corrosion casts. Anat Rec. 1990;228(4):471-7.
  • 37. Yoshida S, Ohshima H, Kobayashi S. Vascularization of the enamel organ in developing molar teeth of rats – scanning electron microscope study of corrosion casts. Okajimas Folia Anat Jpn. 1989;66:99–112.
  • 38. Tsukada H, Ishikawa H, Nakamura S, Yoshida S. Developmental changes of the vasculature in the periodontal ligament of rat molars: a scanning electron microscopic study of microcorrosion casts. J Periodontal Res. 2000;35:201–7.
  • 39. Selliseth NJ, Selvig KA. Microvasculature of the dorsum of the rat tongue: a scanning electron microscopic study using corrosion casts. Scand J Dent Res. 1993;101(6):391-7.
  • 40. Selliseth NJ, Selvig KA. The vasculature of the periodontal ligament. A scanning electron microscopic study using corrosion casts in the rat. J Periodontol. 1994:65:1079-87.
  • 41. Rossi-Schneider TR, Verli FD, Yurgel LS, De Souza MA, Cherubini K. Contribution to the study of the vasculature of submandibular and sublingual glands and lymph nodes of rats by corrosion cast technique combined with scanning electron microscopy. Microsc Res Tech. 2008;71(10):737-41.
  • 42. Aghaloo TL, Kang B, Sung EC, Shoff M, Ronconi M, Gotcher JE, et al. Periodontal disease and bisphosphonates induce osteonecrosis of the jaws in the rat. J Bone Miner Res. 2011;26:1871–82.
  • 43. Chung WO, Dommisch H, Yin L, Dale BA. Expression of defensins in gingiva and their role in periodontal health and disease. Curr Pharm Des. 2007;13:3073–83.
  • 44. Slade GD, Beck JD. Plausibility of periodontal disease estimates from NHANES III. J Public Health Dent. 1999;59:67–72.
  • 45. Taubman MA, Nash DA. The scientific and public-health imperative for a vaccine against dental caries. Nat Rev Immunol. 2006;6:555–63.
  • 46. Allen MR, Burr DB. The pathogenesis of bisphosphonate-related osteonecrosis of the jaw: so many hypotheses, so few data. J Oral Maxillofac Surg. 2009;67(5):61–70.
  • 47. Samson FP, Fabunmi TE, Patrick AT, Jee D, Gutsaeva DR, Jahng WJ. Fatty Acid Composition and Stoichiometry Determine the Angiogenesis Microenvironment. ACS Omega 2021.https://dx.doi.org/10.1021/acsomega.1c00196
  • 48. Kang JX, Liu A. The role of the tissue omega-6/omega-3 fatty acid ratio in regulating tumor angiogenesis. Cancer Metastasis Rev. 2013;32:201–10.
  • 49. Wang QY, Dai J, Kuang B, Zhang J, Yu SB, Duan YZ, Wang MQ. Osteochondral angiogenesis in rat mandibular condyles with osteoarthritis-like changes. Arch Oral Biol. 2012;57(6):620-9.
  • 50. Widyastuti, Rubianto M, Soetjipto. Induction of Angiogenesis Process in Mandible Using Anadara granosa Shell Graft (Experimental Laboratory Study on Rattus norvegicus). In: IOP Conference Series: Earth and Environmental Science. IOP Publishing 2018;217:012033.
  • 51. Luthfi M, Juliastuti WS, Risky YA, Wijayanti EH, Rachmawati AE, Asyhari NPO. Expression of fibroblast cells after extraction of wistar rat teeth after topical application of okra fruit (Abelmoschus esculentus) gel. Infect Dis Rep. 2020;12(1):8726.
  • 52. Rowe NM, Mehara BJ, Luchs JS, Dudziak ME, Steinbrech DS, Illei PB, et al. Angiogenesis during mandibular distraction osteogenesis. Ann Plast Surg. 1999;42:470–5.
There are 52 citations in total.

Details

Primary Language English
Subjects Health Care Administration
Journal Section Research Articles
Authors

Ziya Yurtal 0000-0001-6080-1860

Gözde Serindere 0000-0001-7439-3554

Ceren Aktuna Belgin 0000-0001-7780-3395

Lutfi Takcı 0000-0002-8865-8186

Project Number Project No: 19.M.058
Publication Date December 31, 2021
Submission Date July 12, 2021
Published in Issue Year 2021 Volume: 6 Issue: 3

Cite

APA Yurtal, Z., Serindere, G., Aktuna Belgin, C., Takcı, L. (2021). Investigation of the Effect of Linoleic Acid on Vascularization in Experimentally Induce Zoledronic Acid-Related Osteonecrosis in Rats. Veterinary Journal of Mehmet Akif Ersoy University, 6(3), 122-126. https://doi.org/10.24880/maeuvfd.970180