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Mandibular biomechanical behavior of rats submitted to chronic intermittent or continuous hypoxia and periodontitis

  • Dentistry • Original Article
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Abstract

Background

The aim of this study was to investigate the effects of exposure to continuous (CH) and intermittent (IH) hypoxia on biomechanical properties of the mandible and periodontal tissue of animals submitted to experimental periodontitis (EP) when applying loads in a hypoxic environment.

Methods

Adult female Wistar rats were exposed during 90 days to IH or CH (simulated high altitude of 4200 m above sea level). Fourteen days prior to the euthanasia, EP was induced to half of the animals of each group.

Results

Only in the rats with EP, IH decreased the maximum capacity of the mandible to withstand load and the limit of elastic load. Indicators of intrinsic properties of the bone material were significantly reduced by both types of hypoxia in rats with EP. Hypoxia enhanced the alveolar bone loss induced by EP in the buccal side of the mandible, without showing additional effects in lingual or interradicular bone. Hypoxia increased prostaglandin E2 content in gingival tissue of healthy animals and further elevated the E2 levels increased by EP.

Conclusions

When periodontitis is present, hypoxic stress induces a decrease in mineral properties that ultimately affects the ability of the mandible to resist load, mainly during intermittent exposure to hypoxia. These effects on bone may be related to the higher levels of prostaglandin E2 reached in the surrounding gingival tissue. The findings of this study may stimulate strategies to prevent unwanted effects of hypoxia on periodontal tissues.

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Abbreviations

IH:

Chronic intermittent hypoxia

CH:

Chronic continuous hypoxia

EP:

Experimental periodontitis

Wf:

Fracture load

Wy:

Limit elastic load

Wy/dy:

Bone rigidity

CSA:

Cross-sectional area

CSMI:

Second moment of inertia of the cross section in relation to the horizontal axis

PGE2 :

Prostaglandin E2

iNOS:

Inducible nitric oxide synthase

References

  1. Arestegui AH, Fuquay R, Sirota J, Swenson ER, Schoene RB, Jefferson JA, Escudero E (2011) High altitude renal syndrome (HARS). J Am SocNephrol 22:1963–1968

    CAS  Google Scholar 

  2. Bozzini CE, Lezón CE, Norese MF, Conti MI, Martínez MP, Olivera MI, Alippi RM (2005) Evidence from catch-up growth and hoarding behavior of rats that exposure to hypobaric air lowers the body-mass set point. Growth Dev Aging 69:81–88

    PubMed  Google Scholar 

  3. Bozzini C, Olivera MI, Huygens P, Alippi RM, Bozzini CE (2009) Long-term exposure to hypobaric hypoxia in rat affects femur cross-sectional geometry and bone tissue material properties. Ann Anat 191:212–217

    Article  Google Scholar 

  4. Conti MI, Terrizzi AR, Lee CM, Mandalunis PM, Bozzini C, Piñeiro AE, Martínez MP (2012) Effects of lead exposure on growth and bone biology in growing rats exposed to simulated high altitude. Bull Environ Contam Toxicol 88:1033–1037

    Article  CAS  Google Scholar 

  5. Martínez MP, Bozzini C, Olivera MI, Dmytrenko G, Conti MI (2011) Aluminum bone toxicity in immature rats exposed to simulated high altitude. J Bone Miner Metab 29:526–534

    Article  Google Scholar 

  6. Siques P, Lopez de Pablo AL, Brito J, Arribas SM, Flores K, Arriaza K, Lopez M (2014) Nitric oxide and superoxide anion balance in rats exposed to chronic and long term intermittent hypoxia. BioMed Res Int 2014:610474

    Article  Google Scholar 

  7. Dou ZJ, Gao XL, Jia YL, Chen J, Yang JJ, Chen Y, Wu SJ, Liu T, Wang MT, Yang C, Zhang N, Wang B (2020) CB1 receptor antagonist rimonabant protects against chronic intermittent hypoxia-induced bone metabolism disorder and destruction in rats. Sleep Breath:2020. https://doi.org/10.1007/s11325-019-02009-9

  8. Xiao LI, Li Y, Zhang G, Gao Y, King Y, Liu M, Tan Y (2012) Detection of bacterial diversity in rat's periodontitis model under imitational altitude hypoxia environment. Arch Oral Biol 57:23–29

    Article  Google Scholar 

  9. Gunaratnam K, Taylor B, Curtis B, Cistulli P (2009) Obstructive sleep apnoea and periodontitis: a novel association? Sleep Breath 13:233–239

    Article  Google Scholar 

  10. Vacas MI, Amer M, Chiarenza AP, Luchelli MA, Mandalunis PM, Elverdin JC (2008) Influence of submandibulectomy on alveolar bone loss in rats. J Periodontol 79:1075–1080

    Article  Google Scholar 

  11. Kuhr A, Popa-Wagner A, Schmoll H, Schwahn C, Kocher T (2004) Observations on experimental marginal periodontitis in rats. J Periodontal Res 39:101–106

    Article  CAS  Google Scholar 

  12. Bozzini C, Picasso E, Champin G, Bozzini CE, Alippi RM (2015) Effect of physical consistency of food on the biomechanical behaviour of the mandible in the growing ra. Eur J Oral Sci 123:350–355

    Article  Google Scholar 

  13. Ferretti JL (1997) Biomechanical properties of bone. From Osteoporosis and Bone Densitometry. Springer Verlag, Berlin, pp 143–161

    Google Scholar 

  14. Ferretti JL, Cointry GR, Capozza RF, Capiglioni R, Chiappe M (2001) Analysis of biomechanical effects on bone and on the bone muscle interactions in small animal models. J Musculoskel Neuron Interact 1:263–274

    CAS  Google Scholar 

  15. Ossola CA, Surkin PN, Pugnaloni A, Mohn CE, Elverdin JC, Fernandez-Solari J (2012) Long-term treatment with methanandamide attenuates LPS-induced periodontitis in rats. Inflamm Res 61:941–948

    Article  CAS  Google Scholar 

  16. Dempster DW, Compston JE, Drezner MK, Glorieux FH, Kanis JA, Malluche H, Pierre J, Meunier PJ, Ott SM, Recker RR, Parffit AM (2013) Standardized nomenclature, symbols, and units for bone histomorphometry: a 2012 update of the report of the ASBMR Histomorphometry nomenclature committee. J Bone Miner Res 28:2–17

    Article  Google Scholar 

  17. Mohn CE, Fernandez-Solari J, De Laurentiis A, Bornstein SR, Ehrhart-Bornstein M, Rettori V (2011) Adrenal gland responses to lipopolysaccharide after stress and ethanol administration in male rats. Stress 14:216–226

    Article  CAS  Google Scholar 

  18. Mohn CE, Troncoso GR, Bozzini C, Conti MI, Fernandez Solari J, Elverdin JC (2018) Changes in PGE2 signaling after submandibulectomy alter post-tooth extraction socket healing. Wound Repair Regen 26:153–162

    Article  Google Scholar 

  19. Bozzini C, Champin GM, Alippi RM, Bozzini CE (2013) Static biomechanics in bone from growing rats exposed chronically to simulated high altitude. High Alt Med Biol 14:367–374

    Article  Google Scholar 

  20. Terrizzi AR, Conti MI, Martínez MP, Fernández-Solari J (2018) The process of acclimation to chronic hypoxia leads to submandibular gland and periodontal alterations: an insight on the role of inflammatory mediators. Mediators Inflamm. https://doi.org/10.1155/2018/6794508

  21. Zhang G, Yan KG, Yu-Qi G, Jun L, Xi W, Ying-Hui T (2013) Periodontitis in a high-altitude hypoxic environment through rat model simulation. Asian J Anim Vet Advan 8:593–603

  22. Yamamoto K, Yamamoto T, Ichioka H, Akamatsu Y, Oseko F, Mazda O, Imanishi J, Kanamura N, Kita M (2011) Effects of mechanical stress on cytokine production in mandible-derived osteoblast. Oral Dis 17:712–719

    Article  CAS  Google Scholar 

  23. Takubo K, Goda N, Yamada W, Iriuchishima H, Ikeda E, Kubota Y, Shima H, Johnson RS, Hirao A, Suematsu M, Suda T (2010) Regulation of the HIF-1alpha level is essential for hematopoietic stem cells. Cell Stem Cell 7:391–402

    Article  CAS  Google Scholar 

  24. Ossola CA, Surkin PN, Mohn CE, Elverdin JC, Fernández-Solari J (2016) Anti-inflammatory and osteoprotective effects of cannabinoid-2 receptor agonist HU-308 in a rat model of lipopolysaccharide-induced periodontitis. J Periodontol 87:725–734

    Article  CAS  Google Scholar 

  25. Herrera BS, Martin-Porto R, Maia-Dantas A, Campi P, Spolidorio LC, Costa SK, Van Dyke TE, Gyurko R, Muscara MN (2011) iNOS- derived nitric oxide stimulates osteoclast activity and alveolar bone loss in ligature-induced periodontitis in rats. J Periodontol 82:1608–1615

    Article  CAS  Google Scholar 

  26. Kats A, Bage T, Georgsson P, Jonsson J, Quezada HC, Gustafsson A, Jansson L, Lindberg C, Nasstrom K, Yucel-Lindberg T (2013) Inhibition of microsomal prostaglandin E synthase-1 by aminothiazoles decreases prtostaglandin E2 synthesis in vitro and ameliorates experimental periodontitis in vivo. FASEB J 27:2328–2341

    Article  CAS  Google Scholar 

  27. Brennan P, Thomas G, Langdon J (2003) The role of nitric oxide in oral diseases. Arch Oral Biol 48:93–100

    Article  CAS  Google Scholar 

  28. Parwani SR, Parwani RN (2015) Nitric oxide and inflammatory periodontal disease. Gen Dent 63:34–40

    PubMed  Google Scholar 

  29. Schulz R, Schmidt D, Blum A, Lopes-Ribeiro X, Lücke C, Mayer K, Olschewski H, Seeger W, Grimminger F (2000) Decreased plasma levels of nitric oxide derivatives in obstructive sleep apnoea: response to CPAP therapy. Thorax 55:1046–1051

    Article  CAS  Google Scholar 

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Acknowledgments

The authors acknowledge the collaboration of physiology laboratory technician Graciela M. Champin from the Department of Physiology, School of Dentistry, University of Buenos Aires.

Funding

This investigation was supported by a research grant from University of Buenos Aires (UBACyT n° 20020150100006BA).

Author information

Authors and Affiliations

  1. Cátedra de Fisiología, Facultad de Odontología, Universidad de Buenos Aires, M.T. de Alvear 2142, 3rd floor “A”, Buenos Aires, Argentina

    Antonela Romina Terrizzi, Giuliana Rugolo, Clarisa Bozzini, María Inés Conti, Javier Fernández-Solari & María Pilar Martínez

  2. CONICET, Consejo Nacional de Investigaciones Científicas y Técnicas, Buenos Aires, Argentina

    Antonela Romina Terrizzi & Javier Fernández-Solari

Authors
  1. Antonela Romina Terrizzi
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  2. Giuliana Rugolo
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  3. Clarisa Bozzini
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  4. María Inés Conti
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  5. Javier Fernández-Solari
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  6. María Pilar Martínez
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Corresponding author

Correspondence to Antonela Romina Terrizzi.

Ethics declarations

Animal studies have been carried out in accordance with the National Institutes of Health Guide for the Care and Use of Laboratory Animals (NIH 8th edition, 2011), and protocols were approved by the Institutional Committee for Care and Handling of Laboratory Animals (CICUAL) of the Faculty of Dentistry, University of Buenos Aires (N° 11/06/2012–23).

The manuscript does not contain clinical studies or patient data.

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The authors declare that they have no conflict of interests.

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Terrizzi, A.R., Rugolo, G., Bozzini, C. et al. Mandibular biomechanical behavior of rats submitted to chronic intermittent or continuous hypoxia and periodontitis. Sleep Breath 25, 519–527 (2021). https://doi.org/10.1007/s11325-020-02158-2

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  • DOI: https://doi.org/10.1007/s11325-020-02158-2

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