Journal of Periodontal and Implant Science

Korean Academy of Periodontology (대한치주과학회)
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Identification of venular capillary remodelling: a possible link to the development of periodontitis?

  • Townsend, David (Periodontology Unit, UCL Eastman Dental Institute, UCL, University of London)
  • Received : 2021.02.03
  • Accepted : 2021.08.23
  • Published : 2022.02.28
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Abstract

Purpose: The present study measured changes in arteriolar and venular capillary flow and structure in the gingival tissues during the development of plaque-induced gingival inflammation by combining dynamic optical coherence tomography (OCT), laser perfusion, and capillaroscopic video imaging. Methods: Gingival inflammation was induced in 21 healthy volunteers over a 3-week period. Gingival blood flow and capillary morphology were measured by dynamic OCT, laser perfusion imaging, and capillaroscopy, including a baseline assessment of capillary glycocalyx thickness. Venular capillary flow was estimated by analysis of the perfusion images and mean blood velocity/acceleration in the capillaroscopic images. Readings were recorded at baseline and weekly over the 3 weeks of plaque accumulation and 2 weeks after brushing was resumed. Results: Perfusion imaging demonstrated a significant reduction of gingival blood flow after 1 and 2 weeks of plaque accumulation (P<0.05), but by 3 weeks of plaque accumulation there was a more mixed picture, with reduced flow in some participants and increased flow in others. Participants with reduced flux at 3 weeks also demonstrated venular-type flow as determined by perfusion images and evidence of the development of venular capillaries as assessed by the velocity/acceleration ratio in capillaroscopic images. After brushing resumed, these venular capillaries were broken down and replaced by arteriolar capillaries. Conclusions: After 3 weeks of plaque accumulation, there was wide variation in microvascular reactions between the participants. Reduced capillary flow was associated with the development of venular capillaries in some individuals. This is noteworthy, as an early increase in venous capillaries is a key vascular feature of cardiovascular disease, psoriasis, Sjögren syndrome, and rheumatoid arthritis-diseases with a significant association with the development of severe gingival inflammation, which leads to periodontitis. Future investigations of microvascular changes in gingival inflammation might benefit from accurate capillary flow velocity measurements to assess the development of venular capillaries.

Keywords

Acknowledgement

This research forms part of a PhD thesis supported by Health Education England.

References

  1. Matheny JL, Abrams H, Johnson DT, Roth GI. Microcirculatory dynamics in experimental human gingivitis. J Clin Periodontol 1993;20:578-83. https://doi.org/10.1111/j.1600-051X.1993.tb00774.x
  2. Hanioka T, Amano A, Inoshita E, Tamagawa H, Shizukuishi S. Changes in oxygen consumption in dog gingiva during induction of experimental periodontitis. J Dent Res 1992;71:466-9. https://doi.org/10.1177/00220345920710030801
  3. Lira-Junior R, Figueredo CM, Bouskela E, Fischer RG. Severe chronic periodontitis is associated with endothelial and microvascular dysfunctions: a pilot study. J Periodontol 2014;85:1648-57. https://doi.org/10.1902/jop.2014.140189
  4. Chapple CC, Kumar RK, Hunter N. Vascular remodelling in chronic inflammatory periodontal disease. J Oral Pathol Med 2000;29:500-6. https://doi.org/10.1034/j.1600-0714.2000.291004.x
  5. Zoellner H, Chapple CC, Hunter N. Microvasculature in gingivitis and chronic periodontitis: disruption of vascular networks with protracted inflammation. Microsc Res Tech 2002;56:15-31. https://doi.org/10.1002/jemt.10009
  6. Brecx MC, Nuki K, Lang NP, Gestach A, Sollberger K. Microvascular volumes in healthy and inflamed gingiva in humans. J Periodontal Res 1992;27:1-7. https://doi.org/10.1111/j.1600-0765.1992.tb02078.x
  7. Townsend D, D'Aiuto F. Periodontal capillary imaging in vivo by endoscopic capillaroscopy. J Med Biol Eng 2010;30:119-23.
  8. Tonetti MS, D'Aiuto F, Nibali L, Donald A, Storry C, Parkar M, et al. Treatment of periodontitis and endothelial function. N Engl J Med 2007;356:911-20. https://doi.org/10.1056/NEJMoa063186
  9. Hansonson B, Lindhe J, Branemark P. Microvascular topography and function in clinically healthy and chronically inflamed dento-gingival tissues--a vital microscopic study in dogs. Periodontics 1986;6:264-71.
  10. Kerdvongbundit V, Vongsavan N, Soo-Ampon S, Hasegawa A. Microcirculation and micromorphology of healthy and inflamed gingivae. Odontology 2003;91:19-25. https://doi.org/10.1007/s10266-003-0024-z
  11. Nuki K, Hock J. The organisation of the gingival vasculature. J Periodontal Res 1974;9:305-13. https://doi.org/10.1111/j.1600-0765.1974.tb00686.x
  12. Sanz M, Del Castillo AM, Jepsen S, Gonzalez-Juanatey JR, D'Aiuto F, Bouchard P, et al. Periodontitis and cardiovascular diseases. Consensus report. Glob Heart 2020;15:1. https://doi.org/10.5334/gh.400
  13. Fazekas R, Molnar E, Lohinai Z, Dinya E, Toth Z, Windisch P, et al. Functional characterization of collaterals in the human gingiva by laser speckle contrast imaging. Microcirculation 2018;25:e12446. https://doi.org/10.1111/micc.12446
  14. Molnar E, Molnar B, Lohinani Z, Toth Z, Benyo Z, Hricisak L, et al. Evaluation of laser speckle contrast imaging for the assessment of oral mucosal blood flow following periodontal plastic surgery: an exploratory study. Biomed Res Int 2017;2017:4042902. https://doi.org/10.1155/2017/4042902
  15. Ohsugi Y, Nagashima Y, Nakatsu S, Sato K, Chiba A, Fujinaka H, et al. Age-related changes in gingival blood flow parameters measured using laser speckle flowmetry. Microvasc Res 2019;122:6-12. https://doi.org/10.1016/j.mvr.2018.10.010
  16. Braverman IM, Sibley J. Role of the microcirculation in the treatment and pathogenesis of psoriasis. J Invest Dermatol 1982;78:12-7. https://doi.org/10.1111/1523-1747.ep12497850
  17. Braverman IM. The cutaneous microcirculation. J Investig Dermatol Symp Proc 2000;5:3-9. https://doi.org/10.1046/j.1087-0024.2000.00010.x
  18. Buschmann I, Pries A, Styp-Rekowska B, Hillmeister P, Loufrani L, Henrion D, et al. Pulsatile shear and Gja5 modulate arterial identity and remodeling events during flow-driven arteriogenesis. Development 2010;137:2187-96. https://doi.org/10.1242/dev.045351
  19. Azaripour A, Lagerweij T, Scharfbillig C, Jadczak AE, Swaan BV, Molenaar M, et al. Three-dimensional histochemistry and imaging of human gingiva. Sci Rep 2018;8:1647. https://doi.org/10.1038/s41598-018-19685-4
  20. Townsend D, D'Aiuto F, Deanfield J. Vascular fragility and the endothelial glycocalyx in the tissues lining the healthy gingival crevice. J Periodontol 2016;87:672-9. https://doi.org/10.1902/jop.2016.150568
  21. Townsend D, D'Aiuto F, Deanfield J. In vivo capillary loop hemoglobin spectroscopy in labial, sublingual, and periodontal tissues. Microcirculation 2015;22:475-84. https://doi.org/10.1111/micc.12218
  22. Turesky S, Gilmore ND, Glickman I. Reduced plaque formation by the chloromethyl analogue of victamine C. J Periodontol 1970;41:41-3. https://doi.org/10.1902/jop.1970.41.1.41
  23. Nieuwdorp M, Meuwese MC, Mooij HL, Ince C, Broekhuizen LN, Kastelein JJ, et al. Measuring endothelial glycocalyx dimensions in humans: a potential novel tool to monitor vascular vulnerability. J Appl Physiol (1985) 2008;104:845-52. https://doi.org/10.1152/japplphysiol.00440.2007
  24. McWhirter JL, Noguchi H, Gompper G. Deformation and clustering of red blood cells in microcapillary flow. Soft Matter 2011;7:10967-77. https://doi.org/10.1039/c1sm05794d
  25. Vink H, Duling BR. Identification of distinct luminal domains for macromolecules, erythrocytes, and leukocytes within mammalian capillaries. Circ Res 1996;79:581-9. https://doi.org/10.1161/01.RES.79.3.581
  26. Cekici A, Kantarci A, Hasturk H, Van Dyke TE. Inflammatory and immune pathways in the pathogenesis of periodontal disease. Periodontol 2000 2014;64:57-80. https://doi.org/10.1111/prd.12002
  27. Nemeth E, Kulkarni GV, McCulloch CA. Proliferative responses of endothelial cell populations to experimentally induced inflammatory lesions of gingival connective tissue in the cynomolgus monkey (Macaca fascicularis). Anat Rec 1994;239:9-17. https://doi.org/10.1002/ar.1092390103
  28. Olczak T, Simpson W, Liu X, Genco CA. Iron and heme utilization in Porphyromonas gingivalis. FEMS Microbiol Rev 2005;29:119-44. https://doi.org/10.1016/j.femsre.2004.09.001
  29. Chen J, Yaniz-Galende E, Kagan HJ, Liang L, Hekmaty S, Giannarelli C, et al. Abnormalities of capillary microarchitecture in a rat model of coronary ischemic congestive heart failure. Am J Physiol Heart Circ Physiol 2015;308:H830-40. https://doi.org/10.1152/ajpheart.00583.2014
  30. Graceffa D, Amorosi B, Miani E, Bonifati C, Chimenti M, Perricone R, et al. Capillaroscopy in psoriatic and rheumatoid arthritis: a useful tool for differential diagnosis. Arthritis (Egypt) 2013;2013:957480. https://doi.org/10.1155/2013/957480
  31. Kuryliszyn-Moskal A. Cytokines and soluble CD4 and CD8 molecules in rheumatoid arthritis: relationship to systematic vasculitis and microvascular capillaroscopic abnormalities. Clin Rheumatol 1998;17:489-95. https://doi.org/10.1007/BF01451285
  32. Cutolo M, Sulli A, Secchi ME, Paolino S, Pizzorni C. Nailfold capillaroscopy is useful for the diagnosis and follow-up of autoimmune rheumatic diseases. A future tool for the analysis of microvascular heart involvement? Rheumatology (Oxford) 2006;45 Suppl 4:iv43-6. https://doi.org/10.1093/rheumatology/kel310
  33. Lin TC, Tseng CF, Wang YH, Yu HC, Chang YC. Patients with chronic periodontitis present increased risk for primary Sjogren syndrome: a nationwide population-based cohort study. PeerJ 2018;6:e5109. https://doi.org/10.7717/peerj.5109
  34. Monson CA, Porfirio G, Riera R, Tweed JA, Petri V, Nagib AN. Periodontal aspects for psoriasis: a systematic review. Clin Res Dermatol 2016;3:1-8. https://doi.org/10.15226/2378-1726/3/6/00147
  35. Qiao P, Shi Q, Zhang R, E L, Wang P, Wang J, et al. Psoriasis patients suffer from worse periodontal status-a meta-analysis. Front Med (Lausanne) 2019;6:212.
  36. Su NY, Huang JY, Hu CJ, Yu HC, Chang YC. Increased risk of periodontitis in patients with psoriatic disease: a nationwide population-based retrospective cohort study. PeerJ 2017.5:e4064.
  37. Thurston G, Murphy TJ, Baluk P, Lindsey JR, McDonald DM. Angiogenesis in mice with chronic airway inflammation: strain-dependent differences. Am J Pathol 1998;153:1099-112. https://doi.org/10.1016/S0002-9440(10)65654-4
  38. Ezaki T, Baluk P, Thurston G, La Barbara A, Woo C, McDonald DM. Time course of endothelial cell proliferation and microvascular remodeling in chronic inflammation. Am J Pathol 2001;158:2043-55. https://doi.org/10.1016/S0002-9440(10)64676-7