Immunohystochemical analysis of collagen-I and collagen-III incidence in different forms of infective endocarditis: the role of underlying heart disease or the influence of infection?

Authors: Gryaznov D.V. 1,2, 2, Kovalev S.A. 1,2, 2, Zhdanov A.I. 2, Vorontsova Z.A. 1, Lavrenov A.L. 1, Pershin E.V. 3, Zolotareva S.N. 1, Kinshov A.N. 1, Nekrasova N.V. 1

Company: 1 Voronezh Burdenko State Medical University; Studencheskaya ulitsa, 10, Voronezh, 394036, Russian Federation;
2 Voronezh Regional Clinical Hospital #1 Moskovskiy prospect, 151, Voronezh, 394066, Russian Federation;
3 Voronezh Regional Bureau of Pathological Anatomy; Moskovskiy prospect, 151, Voronezh, 394066, Russian Federation

For correspondence:  Sign in or register.

Type:  Original articles


DOI: https://doi.org/10.24022/1997-3187-2018-12-2-100-119

For citation: Gryaznov D.V., Kovalev S.A., Zhdanov A.I., Vorontsova Z.A., Pershin E.V., Lavrenov A.L., Zolotareva S.N., Kinshov A.N., Nekrasova N.V. Immunohystochemical analysis of collagen-I and collagen-III incidence in different forms of infective endocarditis: the role of underlying heart disease or the influence of infection? Creative Cardiology. 2018; 12 (2): 100–19 (in Russ.). DOI: 10.24022/1997-3187-2018-12-2-100-119

Received / Accepted:  May 14, 2018 / May 21, 2018

Keywords: extracellular matrix infective endocarditis collagen-I collagen-III expression

Download
Full text:  

 

Abstract

Objective. Collagen-I (C-I) and Collagen-III (C-III) fibers are major components of heart valves extracellular matrix. The aim of study was to evaluate the influence of different forms of infective endocarditis (IE) on the expression of these proteins in human heart valves.

Methods. The data of 60 surgical patients with IE and 28 surgical patients with non-infective heart valve disease was compared. Immunohistochemistry with Anti-Collagen antibodies was performed. Protein expression was estimated via calculation of optical density of stain.

Results. Comparing general IE and control groups no difference in C-I expression was identified, and the level of C-III in IE group was significantly lower. Studying of collagen expression in subgroup with acute IE revealed the decrease of both C-I and C-III. In subacute IE the level of C-I was higher and the level of C-III was lower than in control group (p < 0.0001 in all comparisons). The lowest C-I and C-III level was found at subgroups with calcified aortic stenosis (CAS) (pC-I=0.003; pC-III=0.019) and at tricuspid valve (TV) samples (pC-I<0.0001; pC-III<0.0001). The level of both proteins was low in patients with secondary endocarditis with underlying CAS (pC-I<0.0001; pC-III<0.0001), C-III expression was also poor in cases of TV infective lesion (p<0.0001) and in mitral valve prolapse without and with IE (p=0.04; p=0.024).

Conclusion. The main IE hallmark was the decrease of C-III. The distribution of C-I and C-III in IE is under the influence of localization of valve lesion, underlying heart disease, form, activity and stage of the infection.

Acknowledgements. The study had no sponsorship.
Conflict of interest. The authors declare no conflict of interest.

References

  1. Habib G., Lancellotti P., Antunes M.J., Bongiorni M.G., Casalta J.P., Del Zotti F. et al. 2015 ESC Guidelines for the management of infective endocarditis: The task force for the management of infective endocarditis of the European Society of Cardiology (ESC). Endorsed by: European Association for Cardio-Thoracic Surgery (EACTS), the European Association of Nuclear Medicine (EANM). Eur. Heart J. 2015; 36 (44): 3075–128. DOI: 10.1093/eurheartj/ehv319

  2. Millar B.C., Habib G., Moore J.E. New diagnostic approaches in infective endocarditis. Heart. 2016; 102 (10): 796–807. DOI: 10.1136/heartjnl-2014-307021.

  3. Nishimura R.A., Otto C.M., Bonow R.O., Mack M.J., Carabello B.A., McLeod C.J. et al. 2017 AHA/ACC Focused Update of the 2014 AHA/ACC Guideline for the Management of Patients With Valvular Heart Disease: A Report of the American College of Cardiology/American Heart Association Task Force on Clinical Practice Guidelines. Circulation. 2017; 135 (22). DOI: 10.1161/CIR.0000000000000503.

  4. Tyurin V.P. Infective endocarditis: Guidelines. Moscow: GEOTAR–Media; 2012 (in Russ.).

  5. Shevchenko Yu.L. Surgical treatment of infective endocarditis and basics of pyoseptic cardiac surgery. Moscow: Dinastiya; 2015 (in Russ).

  6. Lepidi H., Durack D.T., Raoult D. Diagnostic methods current best practices and guidelines for histologic evaluation in infective endocarditis. Infect. Dis. Clin. North Am. 2002; 16 (2): 339–61. https://www.ncbi.nlm.nih.gov/pubmed/12092476 (дата обращения 20.01.2018).

  7. El Accaoui R.N., Gould S.T., Hajj G.P., Chu Y., Davis M.K., Kraft D.C. et al. Aortic valve sclerosis in mice deficient in endothelial nitric oxide synthase. Am. J. Physiol. Heart Circ. Physiol. 2014; 306 (9): H1302–13. DOI: 10.1152/ajpheart.00392.2013.

  8. Nomura R., Otsugu M., Naka S., Teramoto N., Matsumoto-Nakano A.M., Ooshima T. et al. Contribution of the interaction of streptococcus mutans serotype k strains with fibrinogen to the pathogenicity of infective endocarditis. Infect. Immun. 2014; 82 (12): 5223–34. DOI: 10.1128/IAI.02164-14.

  9. Pepe G., Nistri S., Giusti B., Sticchi E., Attanasio M., Porciani C. Identification of fibrillin 1 gene mutations in patients with bicuspid aortic valve (BAV) without Marfan syndrome. BMC Med. Gen. 2014; 15: 23. DOI: 10.1186/1471-2350-15-23.

  10. Nallapareddy S.R., Singh K.V., Murray B.E. Contribution of the collagen adhesin Acm to pathogenesis of Enterococcus faecium in experimental endocarditis. Infect. Immun. 2008; 76 (9): 4120–28. DOI: 10.1128/IAI.00376-08.

  11. Gava E., de Castro C.H., Ferreira A.J., Colleta H., Melo M.B., Alenina N. et al. Angiotensin-(1-7) receptor Mas is an essential modulator of extracellular matrix protein expression in the heart. Regul. Pept. 2012; 175: 30–42. DOI: 10.1016/j.regpep.2012.01.001

  12. Nus M., MacGrogan D., Martínez-Poveda B., Benito Y., Casanova J.C. Diet-Induced aortic valve disease in mice haploinsufficient for the notch pathway effector RBPJK/CSL. Arterioscler. Thromb. Vasc. Biol. 2011; 31: 1580–88. DOI: 10.1161/ATVBAHA.111.227561.

  13. Petrov G., Regitz-Zagrosek V., Lehmkuhl E., Krabatsch T., Dunkel A., Dandel M. et al. Regression of myocardial hypertrophy after aortic valve replacement, faster in women? Circulation. 2010; S23–8. DOI: 10.1161/CIRCULATIONAHA.109.927764.

  14. Gasanov A.G., Bershova T.V. The role of extracellular matrix changes in occurrence of cardiovascular diseases. Biomeditsinskaya Khimiya. 2009; 55 (2): 155–68 (in Russ). Available at: https://elibrary.ru/item.asp?id=12590537 (accessed February 18, 2018).

  15. Fleischer K.J., Nousari H.C., Anhalt G.J., Stone C.D., Laschinger J.C. Immunohistochemical abnormalities of fibrillin in cardiovascular tissues in Marfan's syndrome. Ann. Thorac. Surg. 1997; 63 (4): 1012–17. https://www.ncbi.nlm.nih.gov/pubmed/9124898 (дата обращения 27.02.2017).

  16. LiX.,QiY.,LiY.,ZhangS.,GuoS.,ChuS.etal. Impact of mineralocorticoid receptor antagonists on changes in cardiac structure and function of left ventricular dysfunction. A meta-analysis of randomized controlled trials. Circ. Heart Fail. 2013; 6: 156–65. DOI: 10.1161/CIRCHEARTFAILURE.112.000074.

  17. Zemtsovskiy E.V., Malev E.G., Reeva S.V., Lune- va E.B., Parfenova N.N., Lobanov M.Yu. et al. Diagnosis of genetical abnormalities of connective tissue. Overall results and prospects. Russian Journal of Cardiology. 2013; 4: 38–43 (in Russ.). DOI: 10.15829/1560-4071-2013-4-38-43.

  18. Banerjee T., Mukherjee S., Ghosh S., Biswas M., Dutta S., Pattari S. et al. Clinical significance of markers of collagen metabolism in rheumatic mitral valve disease. PLoS One. 2014; 9 (3): e90527. DOI: 10.1371/journal.pone.0090527.

  19. Votteler M., Berrio D.A., Horke A., Sabatier L., Reinhardt D.P., Nsair A. et al. Elastogenesis at the onset of human cardiac valve development. Development. 2013; 140 (11): 2345–53. DOI: 10.1242/dev.093500.

  20. Leopold J.A. Cellular mechanisms of aortic valve calcification. Circ. Cardiovasc. Interv. 2012; 5 (4): 605–14. DOI: 10.1161/CIRCINTERVENTIONS.112.971028.

  21. Nataatmadja M., West M., West J., Summers K., Walker P., Nagata M. et al. Abnormal extracellular matrix protein transport associated with increased apoptosis of vascular smooth muscle cells in Marfan syndrome and bicuspid aortic valve tho- racic aortic aneurysm. Circulation. 2003; II329–34. https://www.ncbi.nlm.nih.gov/pubmed/12970255 (дата обращения 03.12.2018).

  22. Sádaba J.R., Martínez-Martínez E., Arrieta V., Álvarez V., Fernández-Celis A., Ibarrola J. et al. Role for Galectin-3 in calcific aortic valve stenosis. J. Am. Heart Assoc. 2016; 5 (11): e004360. DOI: 10.1161/JAHA.116.004360.

  23. Tsamis A., Krawiec J.T., Vorp D.A. Elastin and col- lagen fibre microstructure of the human aorta in ageing and disease: a review. J. R. Soc. Interface. 2012; 10: 1004. DOI: 10.1098/rsif.2012.1004.

  24. Balachandran K., Bakay M.A., Connolly J.M., Zhang X., Yoganathan A.P., Levy R.J. Aortic valve cyclic stretch causes increased remodeling activity and enhanced serotonin receptor responsiveness. Ann. Thorac. Surg. 2011; 92 (1): 147–53. DOI: 10.1016/j.athoracsur.2011.03.084.

  25. Stephens E.H., Nguyen T.C., Itoh A., Ingels N.B., Jr., Miller C., Grande-Allen K.J. The effects of mitral regurgitation alone are sufficient for leaflet remod- eling. Circulation. 2008; 118 (14): S243–9. DOI: 10.1161/CIRCULATIONAHA.

  26. De Buyzere M.L., De Scheerder I.K., Delanghe J.R., Robbrecht J.H., Clement D.L., Wieme R.J. Measurement of autoimmune response against collagen types I, III, and IV by enzyme-linked immunosorbent assay, and its application in infective endocarditis. Clin. Chem. 1989; 35 (2): 246–50. https://www.ncbi.nlm.nih.gov/pubmed/2914369 (дата обращения 25.12.2017).

  27. Dougherty G. Digital image processing for medical applications. California State University, Channel Islands. Cambridge University Press; 2009.

  28. Qiu J.S.G., Ilyas M., Dolman G. A Semi-automat- ic image analysis tool for biomarker detection in immunohistochemistry analysis. International Conference on Image and Graphics (ICIG). 2013; 937–42. DOI: 10.1109/ICIG.2013.197.

  29. Chen J.-H., Simmons C.A., Towler D.A. Cellmatrix interactions in the pathobiology of calcific aortic valve disease. Critical roles for matricellular, matricrine, and matrixmechanics cues. Circ. Res. 2011; 108: 1510–24. DOI: 10.1161/CIRCRESAHA.110.234237.

  30. Dupuis L., Osinska H., Weinstein M.B., Hinton R.B., Christine B. Insufficient versican cleavage and SMAD2 phosphorylation results in bicuspid aortic and pulmonary valves. J. Mol. Cell. Cardiol. 2013; 60: 50–9. DOI: 10.1016/j.yjmcc.2013.03.010.

About Authors

Chief Editor

Leo A. Bockeria, MD, PhD, DSc, Professor, Academician of Russian Academy of Sciences, President of Bakoulev National Medical Research Center for Cardiovascular Surgery