Skip to main content
Top
Published in: BMC Oral Health 1/2023

Open Access 01-12-2023 | Osteoporosis | Research

Non-invasive diagnostic potential of salivary miR-25-3p for periodontal disease and osteoporosis among a cohort of elderly patients with type 2 diabetes mellitus

Authors: Jing Ni, Qiong Zhang, Fei Lei

Published in: BMC Oral Health | Issue 1/2023

Login to get access

Abstract

Objective

Osteoporosis (OP) and periodontal disease (PD) are two common health issues that threaten the older population and potentially connected each other in the context of type 2 diabetes mellitus (T2DM). Dysregulated expression of microRNAs (miRNAs) may contribute to the development and progression of both OP and PD among elderly T2DM patients. The present study aimed to evaluate the accuracy of miR-25-3p expression for the detection of OP and PD when compared to a mixed group of patients with T2DM.

Methods

The study recruited 45 T2DM patients with normal bone mineral density (BMD) and healthy periodontium, 40 type 2 diabetic osteoporosis patients coexistent with PD, 50 type 2 diabetic osteoporosis patients with healthy periodontium, and 52 periodontally healthy individuals. miRNA expression measurements in the saliva were determined by real-time PCR.

Results

The salivary expression of miR-25-3p was higher in type 2 diabetic osteoporosis patients than patients with T2DM only and healthy individuals (P < 0.05). Among type 2 diabetic osteoporosis patients, those with PD exhibited a higher salivary expression of miR-25-3p than those with healthy periodontium (P < 0.05). Among type 2 diabetic patients with healthy periodontium, a higher salivary expression of miR-25-3p was noted in those with OP than those without (P < 0.05). We also found a higher salivary expression of miR-25-3p in T2DM patients than healthy individuals (P < 0.05). It was revealed that the salivary expression of miR-25-3p was increased as the T scores of BMD of patients were lowered, the PPD and CAL values of patients were enhanced. The salivary expression of miR-25-3p used as a test to predict a diagnosis of PD among type 2 diabetic osteoporosis patients, a diagnosis of OP among type 2 diabetic patients, and a diagnosis of T2DM among healthy individuals produced AUC of 0.859. 0.824, and 0.886, respectively.

Conclusion

The findings obtained from the study support salivary miR-25-3p confers non-invasive diagnostic potential for PD and OP among a cohort of elderly T2DM patients.
Literature
1.
go back to reference Ahmad E, Lim S, Lamptey R, Webb DR, Davies MJ: Type 2 diabetes. Lancet 2022, 400(10365):1803–1820.CrossRefPubMed Ahmad E, Lim S, Lamptey R, Webb DR, Davies MJ: Type 2 diabetes. Lancet 2022, 400(10365):1803–1820.CrossRefPubMed
2.
go back to reference Bjornstad P, Chao LC, Cree-Green M, Dart AB, King M, Looker HC, Magliano DJ, Nadeau KJ, Pinhas-Hamiel O, Shah AS et al: Youth-onset type 2 diabetes mellitus: an urgent challenge. Nat Rev Nephrol 2022. Bjornstad P, Chao LC, Cree-Green M, Dart AB, King M, Looker HC, Magliano DJ, Nadeau KJ, Pinhas-Hamiel O, Shah AS et al: Youth-onset type 2 diabetes mellitus: an urgent challenge. Nat Rev Nephrol 2022.
3.
go back to reference Sheu A, Greenfield JR, White CP, Center JR: Assessment and treatment of osteoporosis and fractures in type 2 diabetes. Trends Endocrinol Metab 2022, 33(5):333–344.CrossRefPubMed Sheu A, Greenfield JR, White CP, Center JR: Assessment and treatment of osteoporosis and fractures in type 2 diabetes. Trends Endocrinol Metab 2022, 33(5):333–344.CrossRefPubMed
4.
go back to reference Paschou SA, Dede AD, Anagnostis PG, Vryonidou A, Morganstein D, Goulis DG: Type 2 diabetes and osteoporosis: a guide to Optimal Management. J Clin Endocrinol Metab 2017, 102(10):3621–3634.CrossRefPubMed Paschou SA, Dede AD, Anagnostis PG, Vryonidou A, Morganstein D, Goulis DG: Type 2 diabetes and osteoporosis: a guide to Optimal Management. J Clin Endocrinol Metab 2017, 102(10):3621–3634.CrossRefPubMed
5.
go back to reference Zhu L, Zhou C, Chen S, Huang D, Jiang Y, Lan Y, Zou S, Li Y: Osteoporosis and alveolar bone health in Periodontitis Niche: a predisposing factors-centered review. Cells 2022, 11(21). Zhu L, Zhou C, Chen S, Huang D, Jiang Y, Lan Y, Zou S, Li Y: Osteoporosis and alveolar bone health in Periodontitis Niche: a predisposing factors-centered review. Cells 2022, 11(21).
6.
go back to reference Wu CZ, Yuan YH, Liu HH, Li SS, Zhang BW, Chen W, An ZJ, Chen SY, Wu YZ, Han B et al: Epidemiologic relationship between periodontitis and type 2 diabetes mellitus. BMC Oral Health 2020, 20(1):204.CrossRefPubMedPubMedCentral Wu CZ, Yuan YH, Liu HH, Li SS, Zhang BW, Chen W, An ZJ, Chen SY, Wu YZ, Han B et al: Epidemiologic relationship between periodontitis and type 2 diabetes mellitus. BMC Oral Health 2020, 20(1):204.CrossRefPubMedPubMedCentral
8.
go back to reference Polizzi A, Santonocito S, Lo Giudice A, Alibrandi A, De Pasquale R, Isola G: Analysis of the response to two pharmacological protocols in patients with oral lichen planus: a randomized clinical trial. Oral Dis 2023, 29(2):755–763.CrossRefPubMed Polizzi A, Santonocito S, Lo Giudice A, Alibrandi A, De Pasquale R, Isola G: Analysis of the response to two pharmacological protocols in patients with oral lichen planus: a randomized clinical trial. Oral Dis 2023, 29(2):755–763.CrossRefPubMed
9.
go back to reference Pereira FM, Rodrigues VP, de Oliveira AE, Brito LM, Lopes FF: Association between periodontal changes and osteoporosis in postmenopausal women. Climacteric 2015, 18(2):311–315.CrossRefPubMed Pereira FM, Rodrigues VP, de Oliveira AE, Brito LM, Lopes FF: Association between periodontal changes and osteoporosis in postmenopausal women. Climacteric 2015, 18(2):311–315.CrossRefPubMed
10.
go back to reference Grieco GE, Besharat ZM, Licata G, Fignani D, Brusco N, Nigi L, Formichi C, Po A, Sabato C, Dardano A et al: Circulating microRNAs as clinically useful biomarkers for type 2 diabetes Mellitus: miRNomics from bench to bedside. Transl Res 2022, 247:137–157.CrossRefPubMed Grieco GE, Besharat ZM, Licata G, Fignani D, Brusco N, Nigi L, Formichi C, Po A, Sabato C, Dardano A et al: Circulating microRNAs as clinically useful biomarkers for type 2 diabetes Mellitus: miRNomics from bench to bedside. Transl Res 2022, 247:137–157.CrossRefPubMed
11.
go back to reference Wang X, Pei Z, Hao T, Ariben J, Li S, He W, Kong X, Chang J, Zhao Z, Zhang B: Prognostic analysis and validation of diagnostic marker genes in patients with osteoporosis. Front Immunol 2022, 13:987937.CrossRefPubMedPubMedCentral Wang X, Pei Z, Hao T, Ariben J, Li S, He W, Kong X, Chang J, Zhao Z, Zhang B: Prognostic analysis and validation of diagnostic marker genes in patients with osteoporosis. Front Immunol 2022, 13:987937.CrossRefPubMedPubMedCentral
13.
go back to reference Isola G, Santonocito S, Distefano A, Polizzi A, Vaccaro M, Raciti G, Alibrandi A, Li Volti G: Impact of periodontitis on gingival crevicular fluid miRNAs profiles associated with cardiovascular disease risk. J Periodontal Res 2023, 58(1):165–174.CrossRefPubMed Isola G, Santonocito S, Distefano A, Polizzi A, Vaccaro M, Raciti G, Alibrandi A, Li Volti G: Impact of periodontitis on gingival crevicular fluid miRNAs profiles associated with cardiovascular disease risk. J Periodontal Res 2023, 58(1):165–174.CrossRefPubMed
14.
go back to reference Curro M, Matarese G, Isola G, Caccamo D, Ventura VP, Cornelius C, Lentini M, Cordasco G, Ientile R: Differential expression of transglutaminase genes in patients with chronic periodontitis. Oral Dis 2014, 20(6):616–623.CrossRefPubMed Curro M, Matarese G, Isola G, Caccamo D, Ventura VP, Cornelius C, Lentini M, Cordasco G, Ientile R: Differential expression of transglutaminase genes in patients with chronic periodontitis. Oral Dis 2014, 20(6):616–623.CrossRefPubMed
15.
go back to reference Byun JS, Lee HY, Tian J, Moon JS, Choi J, Lee SH, Kim YG, Yi HS: Effect of salivary exosomal mir-25-3p on Periodontitis with insulin resistance. Front Immunol 2021, 12:775046.CrossRefPubMed Byun JS, Lee HY, Tian J, Moon JS, Choi J, Lee SH, Kim YG, Yi HS: Effect of salivary exosomal mir-25-3p on Periodontitis with insulin resistance. Front Immunol 2021, 12:775046.CrossRefPubMed
16.
go back to reference Yu D, Li Z, Cao J, Shen F, Wei G: microRNA-25-3p suppresses osteogenic differentiation of BMSCs in patients with osteoporosis by targeting ITGB3. Acta Histochem 2022, 124(6):151926.CrossRefPubMed Yu D, Li Z, Cao J, Shen F, Wei G: microRNA-25-3p suppresses osteogenic differentiation of BMSCs in patients with osteoporosis by targeting ITGB3. Acta Histochem 2022, 124(6):151926.CrossRefPubMed
17.
go back to reference Huang Y, Ren K, Yao T, Zhu H, Xu Y, Ye H, Chen Z, Lv J, Shen S, Ma J: MicroRNA-25-3p regulates osteoclasts through nuclear factor I X. Biochem Biophys Res Commun 2020, 522(1):74–80.CrossRefPubMed Huang Y, Ren K, Yao T, Zhu H, Xu Y, Ye H, Chen Z, Lv J, Shen S, Ma J: MicroRNA-25-3p regulates osteoclasts through nuclear factor I X. Biochem Biophys Res Commun 2020, 522(1):74–80.CrossRefPubMed
18.
go back to reference Chen J, Li K, Pang Q, Yang C, Zhang H, Wu F, Cao H, Liu H, Wan Y, Xia W et al: Identification of suitable reference gene and biomarkers of serum miRNAs for osteoporosis. Sci Rep 2016, 6:36347.CrossRefPubMedPubMedCentral Chen J, Li K, Pang Q, Yang C, Zhang H, Wu F, Cao H, Liu H, Wan Y, Xia W et al: Identification of suitable reference gene and biomarkers of serum miRNAs for osteoporosis. Sci Rep 2016, 6:36347.CrossRefPubMedPubMedCentral
19.
go back to reference Sun H, Saeedi P, Karuranga S, Pinkepank M, Ogurtsova K, Duncan BB, Stein C, Basit A, Chan JCN, Mbanya JC et al: IDF Diabetes Atlas: Global, regional and country-level diabetes prevalence estimates for 2021 and projections for 2045. Diabetes Res Clin Pract 2022, 183:109119.CrossRefPubMed Sun H, Saeedi P, Karuranga S, Pinkepank M, Ogurtsova K, Duncan BB, Stein C, Basit A, Chan JCN, Mbanya JC et al: IDF Diabetes Atlas: Global, regional and country-level diabetes prevalence estimates for 2021 and projections for 2045. Diabetes Res Clin Pract 2022, 183:109119.CrossRefPubMed
20.
go back to reference Yoshimura N, Iidaka T, Horii C, Muraki S, Oka H, Kawaguchi H, Nakamura K, Akune T, Tanaka S: Trends in osteoporosis prevalence over a 10-year period in Japan: the ROAD study 2005–2015. J Bone Miner Metab 2022, 40(5):829–838.CrossRefPubMed Yoshimura N, Iidaka T, Horii C, Muraki S, Oka H, Kawaguchi H, Nakamura K, Akune T, Tanaka S: Trends in osteoporosis prevalence over a 10-year period in Japan: the ROAD study 2005–2015. J Bone Miner Metab 2022, 40(5):829–838.CrossRefPubMed
21.
go back to reference Germen M, Baser U, Lacin CC, Firatli E, Issever H, Yalcin F: Periodontitis Prevalence, Severity, and risk factors: a comparison of the AAP/CDC Case Definition and the EFP/AAP classification. Int J Environ Res Public Health 2021, 18(7). Germen M, Baser U, Lacin CC, Firatli E, Issever H, Yalcin F: Periodontitis Prevalence, Severity, and risk factors: a comparison of the AAP/CDC Case Definition and the EFP/AAP classification. Int J Environ Res Public Health 2021, 18(7).
22.
go back to reference Verhulst MJL, Teeuw WJ, Bizzarro S, Muris J, Su N, Nicu EA, Nazmi K, Bikker FJ, Loos BG: A rapid, non-invasive tool for periodontitis screening in a medical care setting. BMC Oral Health 2019, 19(1):87.CrossRefPubMedPubMedCentral Verhulst MJL, Teeuw WJ, Bizzarro S, Muris J, Su N, Nicu EA, Nazmi K, Bikker FJ, Loos BG: A rapid, non-invasive tool for periodontitis screening in a medical care setting. BMC Oral Health 2019, 19(1):87.CrossRefPubMedPubMedCentral
23.
go back to reference Tonetti MS, Greenwell H, Kornman KS: Staging and grading of periodontitis: Framework and proposal of a new classification and case definition. J Periodontol 2018, 89 Suppl 1:S159-S172.PubMed Tonetti MS, Greenwell H, Kornman KS: Staging and grading of periodontitis: Framework and proposal of a new classification and case definition. J Periodontol 2018, 89 Suppl 1:S159-S172.PubMed
24.
go back to reference Zhang X, Xu Y, Li F, Chen M: Associations between bone mineral density and subclinical peripheral arterial disease in elderly men with type 2 diabetes mellitus. Osteoporos Int 2022, 33(8):1715–1724.CrossRefPubMed Zhang X, Xu Y, Li F, Chen M: Associations between bone mineral density and subclinical peripheral arterial disease in elderly men with type 2 diabetes mellitus. Osteoporos Int 2022, 33(8):1715–1724.CrossRefPubMed
25.
go back to reference Angelescu MA, Andronic O, Dima SO, Popescu I, Meivar-Levy I, Ferber S, Lixandru D: miRNAs as biomarkers in diabetes: moving towards Precision Medicine. Int J Mol Sci 2022, 23(21). Angelescu MA, Andronic O, Dima SO, Popescu I, Meivar-Levy I, Ferber S, Lixandru D: miRNAs as biomarkers in diabetes: moving towards Precision Medicine. Int J Mol Sci 2022, 23(21).
26.
go back to reference Saxena S, Venugopal R, Chandrayan Rao R, Yuwanati MB, Awasthi H, Jain M: Association of chronic periodontitis and type 2 diabetes mellitus with salivary Del-1 and IL-17 levels. J Oral Biol Craniofac Res 2020, 10(4):529–534.CrossRefPubMedPubMedCentral Saxena S, Venugopal R, Chandrayan Rao R, Yuwanati MB, Awasthi H, Jain M: Association of chronic periodontitis and type 2 diabetes mellitus with salivary Del-1 and IL-17 levels. J Oral Biol Craniofac Res 2020, 10(4):529–534.CrossRefPubMedPubMedCentral
27.
go back to reference Vasu S, Kumano K, Darden CM, Rahman I, Lawrence MC, Naziruddin B: MicroRNA signatures as future biomarkers for diagnosis of Diabetes States. Cells 2019, 8(12). Vasu S, Kumano K, Darden CM, Rahman I, Lawrence MC, Naziruddin B: MicroRNA signatures as future biomarkers for diagnosis of Diabetes States. Cells 2019, 8(12).
28.
go back to reference Gattuso G, Crimi S, Lavoro A, Rizzo R, Musumarra G, Gallo S, Facciponte F, Paratore S, Russo A, Bordonaro R et al: Liquid Biopsy and circulating biomarkers for the diagnosis of precancerous and cancerous oral lesions. Noncoding RNA 2022, 8(4). Gattuso G, Crimi S, Lavoro A, Rizzo R, Musumarra G, Gallo S, Facciponte F, Paratore S, Russo A, Bordonaro R et al: Liquid Biopsy and circulating biomarkers for the diagnosis of precancerous and cancerous oral lesions. Noncoding RNA 2022, 8(4).
30.
go back to reference Giannobile WV, Beikler T, Kinney JS, Ramseier CA, Morelli T, Wong DT: Saliva as a diagnostic tool for periodontal disease: current state and future directions. Periodontol 2000 2009, 50:52–64. Giannobile WV, Beikler T, Kinney JS, Ramseier CA, Morelli T, Wong DT: Saliva as a diagnostic tool for periodontal disease: current state and future directions. Periodontol 2000 2009, 50:52–64.
31.
32.
go back to reference Shen Z, Yu Y, Yang Y, Xiao X, Sun T, Chang X, Tang W, Zhu Y, Han X: miR-25 and miR-92b regulate insulin biosynthesis and pancreatic beta-cell apoptosis. Endocrine 2022, 76(3):526–535.CrossRefPubMed Shen Z, Yu Y, Yang Y, Xiao X, Sun T, Chang X, Tang W, Zhu Y, Han X: miR-25 and miR-92b regulate insulin biosynthesis and pancreatic beta-cell apoptosis. Endocrine 2022, 76(3):526–535.CrossRefPubMed
33.
go back to reference Sakshi S, Jayasuriya R, Ganesan K, Xu B, Ramkumar KM: Role of circRNA-miRNA-mRNA interaction network in diabetes and its associated complications. Mol Ther Nucleic Acids 2021, 26:1291–1302.CrossRefPubMedPubMedCentral Sakshi S, Jayasuriya R, Ganesan K, Xu B, Ramkumar KM: Role of circRNA-miRNA-mRNA interaction network in diabetes and its associated complications. Mol Ther Nucleic Acids 2021, 26:1291–1302.CrossRefPubMedPubMedCentral
Metadata
Title
Non-invasive diagnostic potential of salivary miR-25-3p for periodontal disease and osteoporosis among a cohort of elderly patients with type 2 diabetes mellitus
Authors
Jing Ni
Qiong Zhang
Fei Lei
Publication date
01-12-2023
Publisher
BioMed Central
Published in
BMC Oral Health / Issue 1/2023
Electronic ISSN: 1472-6831
DOI
https://doi.org/10.1186/s12903-023-02992-2

Other articles of this Issue 1/2023

BMC Oral Health 1/2023 Go to the issue