Prevalence of Carotid Artery Calcification in Hemodialysis Patients: A Case–Control Study

Abstract

The aim of this study is to determine the prevalence of carotid artery calcification (CAC) in panoramic dental radiographs of chronic hemodialysis patients and to compare the values obtained with the healthy group. Panoramic radiographs of 76 patients (38 with hemodialysis and 38 with control) (age range 15–79 years; mean age 52.89 years) were examined. CAC was defined as the presence of heterogeneous nodular opacities in the soft tissue in C3–C4 intervertebral area on panoramic radiographs. Using Chi-squared tests, calcification prevalence rates were statistically compared. The Statistical Package for the Social Sciences (version 20.0; SPSS, Inc., an IBM Company, Chicago, IL, USA) was used. A probability p <0.05 was considered statistically significant. The prevalence of CAC on the right and left sides was 23.7% (18 patients) and 17.1% (13 patients) for all groups in this study, respectively. The prevalence of right and left CAC in the case group was 34.2% and 26.3%, respectively, while these values were 13.2% and 7.9%, respectively, in the control group. These differences between the case-control groups were statistically significant (p<0.05). While the rate of CAC increased with age (p<0.05), gender was not an effective factor on CAC (p>0.05). Age rather than disease was more effective on CAC according to the regression analysis. CAC was higher in hemodialysis patients than control groups. However, it should be considered that the age has a greater effect on CAC. These patients with such calcifications should be referred for further evaluation and treatment of carotid arteries, coronary arteries and vascular risk factors.

Keywords

• Carotid artery calcification
• chronic hemodialysis
• panoramic radiography
• risk factors
• vascular calcification

References

1. 1. Murdeshwar HN, Anjum F. Hemodialysis. 2020.
2. 2. Elliott DA. Hemodialysis. Clinical techniques in small animal practice. 2000;15(3):136-48.
3. 3. Cazzavillan S, Ratanarat R, Segala C, Corradi V, De Cal M, Cruz D, et al. Inflammation and subclinical infection in chronic kidney disease: a molecular approach. Blood purification. 2006;25(1):69-76.
4. 4. Friedlander AH, Baker JD. Panoramic radiography: an aid in detecting patients at risk of cerebrovascular accident. Journal of the American Dental Association (1939). 1994;125(12):1598-603.
5. 5. London GM, Marty C, Marchais SJ, Guerin AP, Metivier F, de Vernejoul M-C. Arterial calcifications and bone histomorphometry in end-stage renal disease. Journal of the American Society of Nephrology. 2004;15(7):1943-51.
6. 6. Cohen SN, Friedlander AH, Jolly DA, Date L. Carotid calcification on panoramic radiographs: an important marker for vascular risk. Oral Surgery, Oral Medicine, Oral Pathology, Oral Radiology, and Endodontology. 2002;94(4):510-4.
7. 7. Kumagai M, Yamagishi T, Fukui N, Chiba M. Carotid artery calcification seen on panoramic dental radiographs in the Asian population in Japan. Dentomaxillofacial Radiology. 2007;36(2):92-6.
8. 8. Sumida Y, Nakayama M, Nagata M, Nakashita S, Suehiro T, Kaizu Y, et al. Carotid artery calcification and atherosclerosis at the initiation of hemodialysis in patients with end-stage renal disease. Clinical Nephrology. 2010;73(5):360-9.

9. 9. Kausar R, Anees S, Mahmood S, Hyder A. Acute Phase Reactants in Hemodialysis Patients in Relation to Ejection Fraction. International Journal of Clinical Biochemistry and Research. 2021;7(4):484-7.
10. 10. Winkelmayer WC, Patrick AR, Li J, Brookhart MA, Setoguchi S. The Increasing Prevalence of Atrial Fibrillation Among Hemodialysis Patients. Journal of the American Society of Nephrology. 2011;22(2):349-57.
11. 11. Okamoto T, Morimoto S, Ikenoue T, Furumatsu Y, Ichihara A. Visceral Fat Level Is an Independent Risk Factor for Cardiovascular Mortality in Hemodialysis Patients. American Journal of Nephrology. 2014;39(2):122-9.
12. 12. Guimarães Henriques JC, Kreich EM, Helena Baldani M, Luciano M, Cezar de Melo Castilho J, Cesar de Moraes L. Panoramic radiography in the diagnosis of carotid artery atheromas and the associated risk factors. The open dentistry journal. 2011;5:79-83.
13. 13. Madden RP, Hodges JS, Salmen CW, Rindal DB, Tunio J, Michalowicz BS, et al. Utility of panoramic radiographs in detecting cervical calcified carotid atheroma. Oral surgery, oral medicine, oral pathology, oral radiology, and endodontics. 2007;103(4):543-8.
14. 14. Ravon NA, Hollender LG, McDonald V, Persson GR. Signs of carotid calcification from dental panoramic radiographs are in agreement with Doppler sonography results. Journal of clinical periodontology. 2003;30(12):1084-90.
15. 15. Hansson GK. Atherosclerosis--an immune disease: The Anitschkov Lecture 2007. Atherosclerosis. 2009;202(1):2-10.
16. 16. Zhdanov VS, Sternby NH. Monitoring of atherosclerosis. International journal of cardiology. 2004;95(1):39-42.
17. 17. Gottlieb MG, Bonardi G, Moriguchi EH. Physiopathology and inflammatory aspects of atherosclerosis [Abstract in English]. Scientia Médica. 2005;15(3).
18. 18. Ross R. Atherosclerosis—an inflammatory disease. New England journal of medicine. 1999;340(2):115-26.
19. 19. Bevc S, Šabić S, Hojs R. Atherosclerosis in hemodialysis patients—the role of microinflammation. Renal failure. 2008;30(10):1012-6.
20. 20. Hojs R. Carotid intima‐media thickness and plaques in hemodialysis patients. Artificial organs. 2000;24(9):691-5.
21. 21. London GM, Guerin AP, Marchais SJ, Pannier B, Safar ME, Day M, et al. Cardiac and arterial interactions in end-stage renal disease. Kidney international. 1996;50(2):600-8.
22. 22. Parfrey PS, Foley RN. The clinical epidemiology of cardiac disease in chronic renal failure. Journal of the American Society of Nephrology. 1999;10(7):1606-15.
23. 23. Inönü E, Nisanci Yilmaz MN, Orhan K, Özemre M, Öğütcü NB, Kal Ö. Prevalence of Carotid Artery Calcification on Digital Panoramic Radiographs in Hemodialysis Patients on Kidney Transplant Waiting List. Experimental and clinical transplantation : official journal of the Middle East Society for Organ Transplantation. 2021;19(11):1149-55.
24. 24. Kansu O, Ozbek M, Avcu N, Gençtoy G, Kansu H, Turgan C. The prevalence of carotid artery calcification on the panoramic radiographs of patients with renal disease. Dentomaxillofacial Radiology. 2005;34(1):16-9.
25. 25. Maia PRL, Medeiros AMC, Pereira HS, Lima KC, Oliveira PT. Presence and associated factors of carotid artery calcification detected by digital panoramic radiography in patients with chronic kidney disease undergoing hemodialysis. Oral Surgery, Oral Medicine, Oral Pathology and Oral Radiology. 2018;126(2):198-204.
26. 26. Almog DM, Horev T, Illig KA, Green RM, Carter LC. Correlating carotid artery stenosis detected by panoramic radiography with clinically relevant carotid artery stenosis determined by duplex ultrasound. Oral Surgery, Oral Medicine, Oral Pathology, Oral Radiology, and Endodontology. 2002;94(6):768-73.
27. 27. Ardhanari S, Alpert MA, Aggarwal K, editors. Cardiovascular disease in chronic kidney disease: risk factors, pathogenesis, and prevention. Advances in Peritoneal dialysis Conference on Peritoneal Dialysis; 2014.
28. 28. Stenvinkel P, Alvestrand A, editors. Review articles: inflammation in end‐stage renal disease: sources, consequences, and therapy. Seminars in dialysis; 2002: Wiley Online Library.
29. 29. Santos J-M-O, Soares G-C, Alves APNN, Kurita LM, Silva P-G-dB, Costa FWG. Prevalence of Carotid Artery Calcifications Among 2,500 Digital Panoramic Radiographs of an Adult Brazilian Population. Medicina Oral Patología Oral Y Cirugia Bucal. 2018:0-.
30. 30. Agaçayak KS, Guler R, Sezgin Karatas P. Relation Between the Incidence of Carotid Artery Calcification and Systemic Diseases. Clin Interv Aging. 2020;15:821-826.
31. 31. Antić S, Draginić N, Jovanović M, Nikolić T, Jeremić N, Živković V, et al. Relation Between Oxidative Stress and Carotid Artery Atherosclerosis in Hemodyalisis Patients. Serbian Journal of Experimental and Clinical Research. 2022;23(3):251-60.
32. 32. Zhang K, Cheng G, Cai X, Chen J, Jiang Y, Wang T, et al. Malnutrition, a New Inducer for Arterial Calcification in Hemodialysis Patients? Journal of Translational Medicine. 2013;11(1).
33. 33. Firincioglulari M, Aksoy S, Orhan K, Rasmussen F. Comparison of Intracranial and Extracranial Carotid Artery Calcifications Between Obstructive Sleep Apnea Patients and Healthy Individuals: A Combined Cone-Beam Computed Tomography and Polysomnographic Study. Radiology Research and Practice. 2022;2022:1-8.
34. 34. Jahansooz JR, Ko AH, Hiroi R, Matsunaga M, Carrazana E, Viereck J. Correlation Between Intracranial Calcification and Extracranial Stenosis of the Internal Carotid Artery. Cureus. 2023.
35. 35. Ibraheem WI, Bhati AK, Alhomood MA, Allayl OA, Qsadi AA, Mohammed TIM, et al. Relationship Between Carotid Artery Calcification and Periodontitis in the Saudi Population: A Retrospective Study. Applied Sciences. 2023;13(22):12370.
36. 36. Uchida K, Sugino N, Yamada S, Kuroiwa H, Yoshinari N, Asano A, et al. Clinical Significance of Carotid Artery Calcification Seen on Panoramic Radiographs. Journal of Hard Tissue Biology. 2014;23(4):461-6.
37. 37. Halwani MAM, Alshahrani MR, Motaen SAI, Asiri M, Alkhairy SIA. Detection of Common Carotid Artery Calcifications in Panoramic Radiographs and Its Relationship to Some Chronic Diseases for Local Population in Abha Southern Kingdom of Saudi Arabia -2017-2018: Prevalence and Reliability. The International Annals of Medicine. 2017;2(1).
38. 38. Lee JS, Kim OS, Chung HJ, Kim YJ, Kweon SS, Lee Y, et al. The Correlation of Carotid Artery Calcification on Panoramic Radiographs and Determination of Carotid Artery Atherosclerosis With Ultrasonography. Oral Surgery Oral Medicine Oral Pathology and Oral Radiology. 2014;118(6):739-45.
39. 39. Tiller R, Bengel W, Rinke S, Ziebolz D. Association Between Carotid Area Calcifications and Periodontal Risk: A Cross Sectional Study of Panoramic Radiographic Findings. BMC Cardiovascular Disorders. 2011;11(1).
40. 40. Johansson E, Ahlqvist J, Garoff M, Karp K, Jäghagen EL, Wester P. Ultrasound Screening for Asymptomatic Carotid Stenosis in Subjects With Calcifications in the Area of the Carotid Arteries on Panoramic Radiographs: A Cross-Sectional Study. BMC Cardiovascular Disorders. 2011;11(1).
41. 41. Saati S, Foroozandeh M, Alafchi B. Radiographic Characteristics of Soft Tissue Calcification on Digital Panoramic Images. Pesquisa Brasileira Em Odontopediatria E Clínica Integrada. 2020;20.
42. 42. Darwin D, Castelino RL, Babu S, Asan MF. Prevalence of Soft Tissue Calcifications in the Maxillofacial Region. Brazilian Journal of Oral Sciences. 2023;22:e237798.
43. 43. Jashari F, Ibrahimi P, Johansson E, Ahlqvist J, Arnerlöv C, Garoff M, et al. Atherosclerotic Calcification Detection: A Comparative Study of Carotid Ultrasound and Cone Beam CT. International Journal of Molecular Sciences. 2015;16(8):19978-88.