Effect of thyroid function on periodontitis in U.S. population

doi:10.21203/rs.3.rs-3139548/v1

Download PDF

Research Article

Effect of thyroid function on periodontitis in U.S. population

https://doi.org/10.21203/rs.3.rs-3139548/v1

This work is licensed under a CC BY 4.0 License

Version 1

posted

You are reading this latest preprint version

Background

Thyroid dysfunction can lead to bone metabolism disorders and osteoporosis. Periodontitis is the most common oral disease, with alveolar bone resorption destruction as one of the main characteristics, and is associated with a variety of systemic diseases. Clinical and animal studies have shown that people with thyroid disorders are also at higher risk for osteoporosis. The progression of periodontitis may be accelerated by thyroid dysfunction because it may influence immune factor production and bone metabolism, which in turn inhibits alveolar osteogenesis and promotes bone resorption. This study analyze the correlative linkages between periodontitis and thyroid function.

Methods

This study used public data in two cycles of NHANES(2009–2010 and 2011–2012) for analysis. Participants were split into two groups on the basis of their status of periodontal condition: those without periodontitis and those who had it. We looked into the connection between periodontitis and thyroid function using a weighted logistic regression model. Then, using subgroup analysis, the potential contributing factors were explored.

Results

A total of 2352 subjects were included, and multiple regression models showed that after adjusting for all covariates, the low TSH level group was significantly associated with a 0.1-unit increase in periodontitis (adjusted for OR 1.48, 95% CI 1.01–2.17; p for trend = 0.048). According to the findings of the subgroup analysis, relationships between the two is remarkable despite variations in sex, age, vitamin D levels, and smoking status.

Conclusion

Periodontitis and thyroid function are tightly coupled, and that the onset of periodontitis is highly correlated with low TSH levels.

Clinical relevance: Patients with low serum TSH levels are more likely to have periodontitis. Stomatologists should focus more on thyroid disease patients, consider how systemic illnesses affect oral health, and enhance the standard of diagnosis and treatment.

Thyroid dysfunction

Periodontitis

NHANES

Cross-sectional study

Periodontitis is a chronic inflammatory disease characterized by plaque biofilm initiation factor and periodontal support tissue destruction. It may result in alveolar bone absorption, tooth loosening and even tooth loss. Alveolar bone absorption is one of its main characteristics[1]. As the sixth most common illness in the globe, which seriously affects the physical and mental health of patients[2]. Numerous systemic disorders, such as diabetes, cardiovascular disease, lung disease, and a host of others have a significant link to periodontitis[3]. Inflammation or other immune reactions to the periodontitis pathogens could be a possible explanation for the link between systemic illness and periodontitis[4].

The thyroid gland is the largest endocrine organ and secretes thyroid hormone to regulate various physiological activities. Abnormal thyroid gland function can result in a decrease or increase in thyroid hormone levels, which may be pathologically secreted into the blood and lead to bone metabolism disorders and osteoporosis[5]. In hypothyroidism, for instance, the activity of osteoblasts and osteoclasts is reduced, leading to low-conversion osteoporosis[6]. In the condition of hyperthyroidism, the rate of bone resorption surpasses that of bone formation, leading to a decline in bone density. This disease is called high conversion osteoporosis[7]. Since alveolar bone density loss and resorption is one of the important characteristics of periodontitis and those with thyroid dysfunction are at greater risk for osteoporosis[8]. Therefore, it is reasonable to speculate that thyroid dysfunction is related to periodontal health.

However, most of the existing literature is based on retrospective and cross-sectional case reports and review analyses, few high-quality studies have been conducted on periodontitis and thyroid dysfunction[9]. Thyroid dysfunction is a widespread health issue, and comprehending its impact on periodontitis could be essential in mitigating the associated morbidity.

Thus, in this investigation, the association between thyroid function and periodontitis was examined using data from two cycles of the NHANES.

2.1 Data and participants

The data used in our study are all from two cycles of NHANES, (2009–2010 and 2011–2012). All participants got thorough evaluations, including physical and laboratory tests, as well as standardized interviews with questions pertaining to socioeconomics, demographics, and health. The Declaration of Helsinki was followed for conducting this study, which received permission from the NCHS Institutional Review Board. Before any of the subjects were investigated, they all gave their consent.

2.2 Definitions of Periodontitis

We used updated CDC/AAP definitions to monitor periodontitis[10], periodontal states were classified into four categories by objective clinical measurement of attachment loss and periodontal pocket depth: no periodontitis, mild, moderate, and severe periodontitis. In our study, patients with periodontitis were collectively referred to as patients with periodontitis regardless of the degree of periodontitis.

2.3 Study variables

Thyroid peroxidase antibodies (TPO Ab), Free thyroxine (T4) and thyroid stimulating hormone (TSH) data were obtained from the “Thyroid profile” in the laboratory data from 2009–2010 and from 2011–2012 NHANES. In this study, TSH levels being used to assess thyroid function since it is the most sensitive indicator and can be altered by even small changes in free T4 concentrations[11]. According to the thyroid stimulating hormone levels of patients, using a tertile-based approach divided into three groups (First tertile: 1.9-5.4mIU/L, Second tertile: 1.19-1.19mIU/L, Third tertile: 0.24-1.19mIU/L11)[12].

Other covariates included sex, age, race, smoking and drinking status, hypertension, body mass index (BMI), fasting blood glucose and the Vit D levels. Race was classified as others, other Hispanic, non-Hispanic white and non-Hispanic black. Study-participants' smoking status was rated as current, former, and never smokers. Never drinking and currently drinking were the two categories for drinking status. Hypertension is defined as having a systolic blood pressure of more than 140 mm Hg and a diastolic blood pressure of more than 90 mm Hg. As in earlier studies, the Vit D levels were spilt into four categories: normal, insufficient, deficient, and severely deficient (≥ 75 nmol/ml, 50to74.9 nmol/ml, 50to74.9nmol/ml, and < 25 nmol/ml)[13].

2.4 Statistical analysis

Participants were split into two groups: those who did not have periodontitis and those who did. The independent and chi-squared tests, respectively, were used to examine the differences between continuous and categorical variables. A series of weighted logistic regressions were carried out to investigate the possible and independent relationship between periodontitis and serum TSH levels. Model 1 is an unadjusted model, while Model 2 is adjusted for sex, age, Free T4, TPO Ab, fasting blood glucose, and smoking status. Model 3 was further adjusted for Vit D levels, drinking status, and BMI based on Model 2, and Model 4 was additionally adjusted for race and hypertension based on Model 3. To investigate potential associations in heterogeneity, subgroup analyses on basis of included characteristics were carried out. All data management steps and analyses were performed in statistical software packages R (http://www.R-project. org, The R Foundation) and Free Statistical software version 1.7.

3.1 General Characteristics

For this study, data from two cycles (2009–2010 and 2011–2012) of the NHANES database were obtained, comprising a total of 20,293 individuals. A total of 17437 participants without records of thyroid profiles or periodontal examinations were excluded. Based on the NHANES 2009–2010 and 2011–2012 clinical reference ranges (NHANES 2009–2010 Laboratory Methods (cdc.gov), NHANES 2011–2012 Laboratory Methods (cdc.gov)), we excluded primary hypothyroidism (Free T4 < 0.6 ng/dL and TSH > 5.4 mIU/L), subclinical hypothyroidism (0.6 ≤ Free T4 ≤ 1.6 ng/dL, TSH > 5.4 mIU/L) and primary hyperthyroidism (Free T4 > 1.6 ng/dL and TSH < 0.24 mIU/L), All study participants had normal TSH levels.

In the end, the analysis consisted of 2352 participants who were categorized into two groups based on their periodontal health status: those with no periodontitis (n = 704) and those with periodontitis (n = 1648). Figure 1 shows the flowchart of the inclusion and exclusion criteria.

Socio-demographic characteristics of the study population are displayed in Table 1. The results indicate that there were no notable distinctions observed between the two groups concerning hypertension (p = 0.821), Free T4 levels (P = 0.931) and TPO Ab (p = 0.74). Other variables, such as sex, age, race, smoking and drinking habits, body mass index (BMI), fasting glucose levels, and Vit D levels, on the other hand, showed significant differences (all P-values 0.05).

3.2 Factors linked to periodontal disease

The entire study population underwent univariate regression analysis to identify the factors that are linked to periodontitis. The analysis revealed that periodontitis was positively associated with sex, non-Hispanic white race, smoking, low Vitamin D levels, high fasting glucose levels, and BMI (all P < 0.05, Table 2).

3.3 Association between periodontitis and serum TSH levels.

Multiple logistic regression analyses were used to assess the effect of serum TSH levels on periodontitis, and the results was summarized in Table 3. TSH levels were substantially linked to periodontitis development in the non-adjusted model.(OR = 1.27, 95% CI: 1.02– 1.58, Model 1). After adjusting for sex, age, Free T4, TPO Ab, fasting glucose and smoking status, Compared with the levels of TSH in the first tertile, the odds ratio (OR) for periodontitis at levels of TSH in the third tertile was 1.53 (95%CI 1.11–2.12, Model 2). After further adjusting for BMI, drinking and the Vit D levels, the incidence of periodontitis in the third tertile is still significantly higher than that in the first tertile (OR = 1.56, 95% CI 1.10–2.23, Model 3). After further correction for race and hypertension, participants in the third tertile had a 1.48 times higher incidence of periodontitis (95% CI: 1.01–2.17, p for trend = 0.048).

3.4 Subgroup sensitivity and additional analyses

According to the subgroup analyses in this study, it was found that there were no discernible differences in TSH levels among sex, age, smoking status, and the Vit D levels. The results of subgroup analyses are presented and shown in Fig. 2.

Multivariable adjusted associations between periodontitis and serum TSH levels among participant subgroups

The purpose of this study was to examine the correlation between thyroid function and periodontitis, as well as its influencing factors, by analyzing data collected from 1648 individuals without periodontitis and 704 individuals with periodontitis. The study found that after taking various confounding factors into account, people with lower serum TSH levels had a higher prevalence of periodontitis.

Recent evidence is mounting that there is a significant positive correlation between thyroid dysfunction and periodontitis. As early as 1969, Schneider et al. observed periodontal changes in adult rats with hypothyroidism[14]. Feitosa et al., in their study of a rat model with ligature-induced periodontitis, discovered that hypothyroidism was linked to an increase in bone loss related to periodontitis[15]. According to Yerke et al., Individuals who suffer from hypothyroidism exhibit more deep periodontal probing teeth when compared to those who do not have thyroid disease[16]. In cases of thyroid dysfunction, overproduction of cytokines disrupts tissue repair and triggers bone resorption, as noted by Vitaliy et al., it can result in significant damage to the entire periodontal apparatus, thereby leading to the progression of periodontitis[17].

Among the leading factors of the pathogenesis of periodontitis, one is microbial factor – Bacteria can colonize the cervical surface of the teeth by forming bacterial plaques and invade the periodontal tissue. The invasion of these microorganisms and inflammation can increase osteoclasts accumulation and activation, resulting in the degradation of organic matrix and destruction of bone tissue[18], the other is unbalanced host response. When microbes invade, the response of the host includes recruiting inflammatory cells, generating prostaglandins and cytokines, elaborating lytic enzymes, and activating osteoclasts. These processes can cause alveolar bone resorption and loss of attachment[19]. Traditionally, it has been believed that B and T lymphocytes, as well as neutrophils and macrophages, play a major role in regulating the immunological response of the host[20]. The periodontal tissue is infiltrated by immune cells, which generate numerous inflammatory mediators such as interleukin(IL), tumor necrosis factor-α (TNF-α), arachidonic acid metabolites, and proteolytic enzymes[21]. The inflammatory mediators produced by infiltrated immune cells stimulate the formation of osteoclasts, which are regarded to be the primary kind of cells responsible for bone resorption. This process is considered as a crucial mechanism in the progression of periodontitis[22]. The pathogenesis of periodontal disease involves numerous inflammatory factors, such as TNF-α and IL-1[23], which play a vital role in its pathogenesis. Research has demonstrated that TNF-α and IL-1β levels are increased in gum tissue affected by periodontitis. After periodontal disease treatment, the levels of these cytokines decreased in the affected sites. These results suggest that TNFα and IL-1β could play significant roles in the pathogenesis of periodontitis [24] [25]. TNF-α, which belongs to the tumor necrosis factor family, has been considered to a signal that is linked to an increased presence of osteoclasts[26]. The main function of TNF superfamily protein RANKL is to encourage the formation and activation of osteoclasts while also inhibiting their apoptosis[27]. TNF-α operates through an autocrine mechanism to mediate RANKL, thereby stimulating the differentiation of osteoclasts[28]. Moreover, The synthesis of TNF-α in gum tissue stimulates the production of other pro-inflammatory cytokines such as IL-1[29]. The main form of IL-1 is multifunctional IL-1β. Studies have proved that the content of IL-1 in periodontal tissue and gingival crevicular fluid will be elevated with the progression of periodontitis[30]. The increased secretion of IL-1 could be related to the disruption of the reverse mechanism that restricts inflammation, resulting in the creation of substantial pockets within the gingival sulcus and the degradation of periodontal tissue. IL-1 can also mediate TNF osteoclast by enhancing RANKL expression and osteoclast precursor differentiation[31].

The pituitary gland releases a hormone called thyroid-stimulating hormone (TSH), which encourages the thyroid gland to create and release thyroid hormone. TSH acts on the follicular cells of the thyroid gland, which are in charge of the synthesis and secretion of thyroid hormone[32]. Then, TH combines with corresponding targets to participate in a variety of raw metabolic activities, Bone is a TH target organ, and TH secretion disorder will disrupts the normal metabolism of bone tissue, eventually leading to lesions[33]. In addition to TH, TSH can also directly affect bone tissue remodeling [34]. TSH can reduce osteoclast occurrence by acting on its TSHR G-protein-coupled receptor[35]. Osteoporosis development is correlated with decreased TSHR expression[36]. In the case of TSHR-deficient mice, Etsuko Abe et al. found severe osteoporosis when they analyzed BMD measurements of Piximus. Supplementing TSHR null animals with thyroid extract did not restore the BMD change, indicating that T3 or T4 did not cause the bone loss[36]. In cell models, TSH acts directly on bone tissue and inhibits osteoclast function through TNF-α mediation[37]. Furthermore, TSH has been demonstrated to directly downregulate TNF-α transcription produced by IL-1 or RANKL treatments [38]. In a separate study conducted by Yamoah K et al., TNF-α expression was increased in osteoclast progenitor cells of TSHR-deficient mice. TSHR-deficient mice are more likely to suffer from osteoporosis,[36] indicating that excessive TNF-α production may be a significant factor in the onset of this disease.

The above cytokines and signaling pathways can be directly or indirectly regulated by TSH, so thyroid dysfunction may affect bone metabolism through the above pathways, causing osteoporosis and then contribute to the development of periodontitis.

A cross-sectional study discovered a strong link between periodontitis and thyroid function in a Korean population[39]. While these findings are similar to our own research, but with significant differences in thyroid-stimulating hormone levels across ethnic groups and geographic locations[40]. Our study used the NHANES database including four major races, Moreover, we adjusted the Vit D levels, which was not found in the previous study.

Vitamin D is essential for maintaining bone homeostasis and regulating the body's metabolism of calcium and phosphorus. Vitamin D also regulates TSH secretion[41]. Research investigating the connection between levels of vitamin D and thyroid-stimulating hormone (TSH) in individuals with healthy thyroid function has typically demonstrated a negative correlation between the two[42]. And researchs have already indicated that insufficient vitamin D levels may heighten the risk of developing thyroid-related illnesses. Circulating vitamin D levels were discovered to be considerably lower in patients with chronic periodontitis compared to healthy controls, according to a systematic review and meta-analysis[43]. These results suggest that vitamin D may play a pathophysiological role in connecting periodontitis with dysfunction of the thyroid gland. With the exception of the severely deficient group,the subgroup analysis in this study clearly shows that low levels of TSH are risk factors for periodontitis.

This study is not without limitations. Firstly, Given the cross-sectional design of NHANES, any associations observed do not necessarily imply causation due to the inherent constraints of the study design. Secondly, There may still be some residual biases that we were cannot account for, despite our best efforts to adjust for confounding factors through a careful literature review. Because some potential explanatory variables were not available, or were only accessible for data gathered by NHANES in a given year. Were therefore excluded from the analysis, such as dietary intake and C-reactive protein levels. Thus, regression analyses in this study were restricted to only those important variables that were consistently available from all two NHANES datasets released in the 2009–2010 and 2011–2012 cycles, such as common demographic factors, BMI, fasting blood glucose, smoking, Vit D levels, and so forth. Thirdly, as we were unable to account for urinary iodine levels in this investigation due to the lack of data for the majority of participants, this the TSH levels may have been impacted. Fourthly, this study did not further categorize the severity of periodontitis, and more research is needed to fully understand how the severity of periodontitis is influenced by TSH levels.

To sum up, Periodontitis were significantly correlated with TSH levels. Our findings imply that stomatologists should focus more on thyroid disease patients, consider how systemic illnesses affect oral health, and enhance the standard of diagnosis and treatment.

Funding

This work was supported by the Science and Technology Project of Jilin Provincial Department of Finance ( No: jcsz2020304-20，jcsz2020304-21); Jilin Provincial Science and Technology Development Plan Project (No: 20220203149SF), without any financial interest or benefit

Authors and Affiliations

[1] The First Department of Oral and Maxillofacial Surgery & Oral Plastic and Aesthetic Surgery, Hospital of Stomatology, Jilin University, Changchun 130021, China.

[2] The First Department of Oral and Maxillofacial Surgery & Oral Plastic and Aesthetic Surgery, Hospital of Stomatology, Jilin University, Changchun 130021, China.

[3] The First Department of Oral and Maxillofacial Surgery & Oral Plastic and Aesthetic Surgery, Hospital of Stomatology, Jilin University, Changchun 130021, China.

[4] The First Department of Oral and Maxillofacial Surgery & Oral Plastic and Aesthetic Surgery, Hospital of Stomatology, Jilin University, Changchun 130021, China.

[5] The First Department of Oral and Maxillofacial Surgery & Oral Plastic and Aesthetic Surgery, Hospital of Stomatology, Jilin University, Changchun 130021, China.

[6] The First Department of Oral and Maxillofacial Surgery & Oral Plastic and Aesthetic Surgery, Hospital of Stomatology, Jilin University, Changchun 130021, China.

[7] The First Department of Oral and Maxillofacial Surgery & Oral Plastic and Aesthetic Surgery, Hospital of Stomatology, Jilin University, Changchun 130021, China.

Author Contribution

All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by Wang han, Zhang mingjun and Li nannan. The first draft of the manuscript was written by .Wang han, Xiao miao, Chen ka, Palizi abulikemu and Shi hongli. All authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Informed consent

No informed consent was required for this study because we used deidentified information from the survey databases.

Conflict of interest

The authors declare that they have no conflicts of interest.

Khajuria, D.K., Zahra, S.F., Razdan, R. Effect of locally administered novel biodegradable chitosan based risedronate/zinc-hydroxyapatite intra-pocket dental film on alveolar bone density in rat model of periodontitis. J. Biomater. Sci.-Polym. Ed. 2018, 29, 74-91.
Tonetti, M.S., Jepsen, S., Jin, L.J., Otomo-Corgel, J. Impact of the global burden of periodontal diseases on health, nutrition and wellbeing of mankind: A call for global action. J. Clin. Periodontol. 2017, 44, 456-62.
Kassebaum, N.J., Bernabe, E., Dahiya, M., Bhandari, B., Murray, C.J.L., Marcenes, W. Global Burden of Severe Periodontitis in 1990-2010: A Systematic Review and Metaregression. J. Dent. Res. 2014, 93, 1045-53.
Hajishengallis, G. Immunomicrobial pathogenesis of periodontitis: keystones, pathobionts, and host response. Trends Immunol. 2014, 35, 3-11.
Lu, M., Yang, C.B., Gao, L., Zhao, J.J. Mechanism of subclinical hypothyroidism accelerating endothelial dysfunction. Exp. Ther. Med. 2015, 9, 3-10.
Keller, J., Catala-Lehnen, P., Huebner, A.K., Jeschke, A., Heckt, T., Lueth, A., et al. Calcitonin controls bone formation by inhibiting the release of sphingosine 1-phosphate from osteoclasts. Nat. Commun. 2014, 5, 13.
Lademann, F., Tsourdi, E., Hofbauer, L.C., Rauner, M. Thyroid Hormone Actions and Bone Remodeling - The Role of the Wnt Signaling Pathway. Exp. Clin. Endocrinol. Diabet. 2020, 128, 450-4.
Ahn, H.Y. Effects of Abnormal Thyroid Function Status to Bone Metabolism. International Journal of Thyroidology. 2018, 11, 21-5.
Aldulaijan, H.A., Cohen, R.E., Stellrecht, E.M., Levine, M.J., Yerke, L.M. Relationship between hypothyroidism and periodontitis: A scoping review. Clin. Exp. Dent. Res. 2020, 6, 147-57.
Anand, P.S., Kamath, K.P. Re: Update of the Case Definitions for Population-Based Surveillance of Periodontitis. Eke PI, Page RC, Wei L, Thornton-Evans G, Genco RJ. (J Periodontol 2012; 83: 1449-1454.). J. Periodont. 2014, 85, 765-6.
Sheehan, M.T. Biochemical Testing of the Thyroid: TSH is the Best and, Oftentimes, Only Test Needed - A Review for Primary Care. Clinical medicine & research. 2016, 14, 83-92.
Webster, G.M., Rauch, S.A., Ste Marie, N., Mattman, A., Lanphear, B.P., Venners, S.A. Cross-Sectional Associations of Serum Perfluoroalkyl Acids and Thyroid Hormones in US Adults: Variation According to TPOAb and Iodine Status (NHANES 2007-2008). Environ. Health Perspect. 2016, 124, 935-42.
Yetley, E.A., Pfeiffer, C.M., Schleicher, R.L., Phinney, K.W., Lacher, D.A., Christakos, S., et al. NHANES Monitoring of Serum 25-Hydroxyvitamin D: A Roundtable Summary. Journal of Nutrition. 2010, 140, 2030S-45S.
Schneider, L.C. Periodontal disease in hypothyroid adult rats. Archives of oral biology. 1969, 14, 1169-75.
Feitosa, D.S., Marques, M.R., Casati, M.Z., Sallum, E.A., Nociti, F.H., de Toledo, S. The influence of thyroid hormones on periodontitis-related bone loss and tooth-supporting alveolar bone: a histological study in rats. J. Periodont. Res. 2009, 44, 472-8.
Yerke, L., Levine, M., Cohen, R. MON-616 Potential Relationship between Hypothyroidism and Periodontal Disease Severity. Journal of the Endocrine Society. 2019, 3.
Shcherba, V., Krynytska, I., Marushchak, M., Korda, M. Does thyroid dysfunction influence inflammatory mediators in experimental periodontitis? Endocrine regulations. 2021, 55, 131-41.
Kornman, K.S., Page, R.C., Tonetti, M.S. The host response to the microbial challenge in periodontitis: assembling the players. Periodontol. 2000. 1997, 14, 33-53.
Ishikawa, I. Host responses in periodontal diseases: a preview. Periodontol. 2000. 2007, 43, 9-13.
Nguyen, C.M., Kim, J.W.M., Quan, V.H., Nguyen, B.H., Tran, S.D. Periodontal associations in cardiovascular diseases: The latest evidence and understanding. Journal of oral biology and craniofacial research. 2015, 5, 203-6.
Boyce, B.F., Xing, L.P. Osteoclasts, no longer osteoblast slaves. Nat. Med. 2006, 12, 1356-8.
Bartold, P.M., Cantley, M.D., Haynes, D.R. Mechanisms and control of pathologic bone loss in periodontitis. Periodontol. 2000. 2010, 53, 55-69.
Graves, D.T., Cochran, D. The contribution of interleukin-1 and tumor necrosis factor to periodontal tissue destruction. J. Periodont. 2003, 74, 391-401.
Alexander, M.B., Damoulis, P.D. The role of cytokines in the pathogenesis of periodontal disease. Current opinion in periodontology. 1994, 39-53.
Holmlund, A., Hanstrom, L., Lerner, U.H. Bone resorbing activity and cytokine levels in gingival crevicular fluid before and after treatment of periodontal disease. J. Clin. Periodontol. 2004, 31, 475-82.
Ishihara, Y., Nishihara, T., Kuroyanagi, T., Shirozu, N., Yamagishi, E., Ohguchi, M., et al. Gingival crevicular interleukin-1 and interleukin-1 receptor antagonist levels in periodontally healthy and diseased sites. J. Periodont. Res. 1997, 32, 524-9.
Khosla, S. Minireview: The OPG/RANKL/RANK system. Endocrinology. 2001, 142, 5050-5.
Zou, W., Hakim, I., Tschoep, K., Endres, S., Bar-Shavit, Z. TNF-alpha mediates RANK ligand stimulation of osteoclast differentiation by an autocrine mechanism. J. Bone Miner. Res. 2000, 15, S174-S.
Pan, W.Y., Wang, Q.X., Chen, Q.M. The cytokine network involved in the host immune response to periodontitis. International Journal of Oral Science. 2019, 11.
Batra, P., Das, S., Patel, P. Comparative evaluation of Gingival Crevicular Fluid (GCF) levels of Interleukin-34 levels in periodontally healthy and in patients with chronic and aggressive periodontitis- A cross-sectional study. Saudi Dental Journal. 2019, 31, 316-21.
Wei, S., Kitaura, H., Zhou, P., Ross, F.P., Teitelbaum, S.L. IL-1 mediates TNF-induced osteoclastogenesis. J. Clin. Invest. 2005, 115, 282-90.
Davis, P. New insights into thyroid hormone actions and lipid metabolism. Curr. Opin. Endocrinol. Diabetes Obes. 2010, 17, 395-.
Langdahl, B.L., Eriksen, E.F. The influence of thyroid hormones on bone turnover in health and osteopetrosis. European journal of endocrinology. 1998, 139, 10-1.
Nagata, M., Suzuki, A., Sekiguchi, S., Ono, Y., Nishiwaki-Yasuda, K., Itoi, T., et al. Subclinical hypothyroidism is related to lower heel QUS in postmenopausal women. Endocr. J. 2007, 54, 625-30.
Inoue, M., Tawata, M., Yokomori, N., Endo, T., Onaya, T. Expression of thyrotropin receptor on clonal osteoblast-like rat osteosarcoma cells. Thyroid : official journal of the American Thyroid Association. 1998, 8, 1059-64.
Abe, E., Marians, R.C., Yu, W.Q., Wu, X.B., Ando, T., Li, Y.N., et al. TSH is a negative regulator of skeletal remodeling. Cell. 2003, 115, 151-62.
Baliram, R., Latif, R., Zaidi, M., Davies, T.F. Expanding the Role of Thyroid-Stimulating Hormone in Skeletal Physiology. Front. Endocrinol. 2017, 8, 9.
Yamoah, K., Brebene, A., Baliram, R., Inagaki, K., Dolios, G., Arabi, A., et al. High-mobility group box proteins modulate tumor necrosis factor-alpha expression in osteoclastogenesis via a novel deoxyribonucleic acid sequence. Mol. Endocrinol. 2008, 22, 1141-53.
Song, E., Park, M.J., Kim, J.A., Roh, E., Yu, J.H., Kim, N.H., et al. Implication of thyroid function in periodontitis: a nationwide population-based study. Sci Rep. 2021, 11, 8.
Hollowell, J.G., Staehling, N.W., Flanders, W.D., Hannon, W.H., Gunter, E.W., Spencer, C.A., et al. Serum TSH, T(4), and thyroid antibodies in the United States population (1988 to 1994): National Health and Nutrition Examination Survey (NHANES III). J. Clin. Endocrinol. Metab. 2002, 87, 489-99.
Sar, M., Stumpf, W.E., DeLuca, H.F. Thyrotropes in the pituitary are target cells for 1,25 dihydroxy vitamin D3. Cell and tissue research. 1980, 209, 161-6.
Barchetta, I., Baroni, M.G., Leonetti, F., De Bernardinis, M., Bertoccini, L., Fontana, M., et al. TSH levels are associated with vitamin D status and seasonality in an adult population of euthyroid adults. Clin. Exper. Med. 2015, 15, 389-96.
Nettore, I.C., Albano, L., Ungaro, P., Colao, A., Macchia, P.E. Sunshine vitamin and thyroid. Rev. Endocr. Metab. Disord. 2017, 18, 347-54.

Tables 1 to 3 are available in the Supplementary Files section.

No competing interests reported.

Download PDF

Version 1

posted

You are reading this latest preprint version

Effect of thyroid function on periodontitis in U.S. population

Status:

Version 1

Abstract

Figures

1. INTRODUCTION

2. METHODS

2.1 Data and participants

2.2 Definitions of Periodontitis

2.3 Study variables

2.4 Statistical analysis

3. RESULTS

3.1 General Characteristics

3.2 Factors linked to periodontal disease

3.3 Association between periodontitis and serum TSH levels.

3.4 Subgroup sensitivity and additional analyses

4. DISCUSSION

Declarations

References

Tables

Additional Declarations

Supplementary Files

Status:

Version 1