Effectiveness of a Salivary Testing System to Screen for Periodontal Disease: A Cross-Sectional Study from the NOSE Study
Abstract
1. Introduction
2. Materials and Methods
2.1. Study Participants
2.2. SMT Measurement
2.3. Periodontal Tissue Examination
2.4. Statistical Analysis
3. Results
3.1. Demographics of Study Participants
3.2. Validity of SMT Measurements
3.3. Combinations of SMT Markers
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
Abbreviations
SMT | Salivary Multi Test |
BOP | Bleeding on probing |
CPI | Community Periodontal Index |
PPV | Positive predictive value |
NPV | Negative predictive value |
ROC | Receiver operating characteristic |
AUC | Area under the curve |
References
- Aida, J.; Ando, Y.; Akhter, R.; Aoyama, H.; Masui, M.; Morita, M. Reasons for permanent tooth extractions in Japan. J. Epidemiol. 2006, 16, 214–219. [Google Scholar] [CrossRef] [PubMed]
- Huang, Z.; Peng, S.; Cen, T.; Wang, X.; Ma, L.; Cao, Z. Association between biological ageing and periodontitis: Evidence from a cross-sectional survey and multi-omics Mendelian randomization analysis. J. Clin. Periodontol. 2024, 51, 1369–1383. [Google Scholar] [CrossRef] [PubMed]
- Mizutani, K.; Minami, I.; Mikami, R.; Kido, D.; Takeda, K.; Nakagawa, K.; Takemura, S.; Saito, N.; Kominato, H.; Sakaniwa, E.; et al. Improvement of periodontal parameters following intensive diabetes care and supragingival dental prophylaxis with type 2 diabetes: A prospective cohort study. J. Clin. Periodontol. 2024, 51, 733–741. [Google Scholar] [CrossRef] [PubMed]
- Montero, E.; Bujaldón, R.; Montanya, E.; Calle-Pascual, A.L.; Rojo-Martínez, G.; Castano, L.; Franch-Nadal, J.; Delgado, E.; Chaves, F.; Alonso, B.; et al. Cross-sectional association between severe periodontitis and diabetes mellitus: A nation-wide cohort study. J. Clin. Periodontol. 2024, 51, 368–379. [Google Scholar] [CrossRef]
- Kida, M.; Kokubo, Y.; Kosaka, T.; Ono, T.; Maeda, Y.; Watanabe, M.; Miyamoto, Y.; Ikebe, K. Relationship between carotid-intima-media thickness and periodontal disease in a Japanese urban population with and without hypertension: The Suita Study. J. Clin. Periodontol. 2023, 50, 265–275. [Google Scholar] [CrossRef]
- Park, S.; Kim, I.; Han, S.J.; Kwon, S.; Min, E.J.; Cho, W.; Koh, H.; Koo, B.N.; Lee, J.S.; Kwon, J.S.; et al. Oral Porphyromonas gingivalis infection affects intestinal microbiota and promotes atherosclerosis. J. Clin. Periodontol. 2023, 50, 1553–1567. [Google Scholar] [CrossRef]
- Norhammar, A.; Näsman, P.; Buhlin, K.; Faire, U.; Ferrannini, G.; Gustafsson, A.; Kjellström, B.; Kvist, T.; Jäghagen, E.L.; Lindahl, B.; et al. Does periodontitis increase the risk for future cardiovascular events? Long-term follow-up of the PAROKRANK Study. J. Clin. Periodontol. 2025, 52, 16–23. [Google Scholar] [CrossRef]
- Sanz, M.; Castillo, A.M.D.; Jepsen, S.; Gonzalez-Juanatey, J.; Aiuto, F.; Bouchard, P.; Chapple, I.; Dietrich, T.; Gotsman, I.; Graziani, F.; et al. Periodontitis and cardiovascular diseases: Consensus report. J. Clin. Periodontol. 2020, 47, 268–288. [Google Scholar] [CrossRef]
- Chen, Z.; Zhong, Y.; Chen, L.; Liu, W.; Lin, C.; Chen, Y.; Wang, X. HGF Aggravated Periodontitis-Associated Gut Barrier and Microbial Dysfunction: Implications for Oral-Gut Axis Regulation. Biology 2025, 14, 496. [Google Scholar] [CrossRef]
- Bie, M.; Wu, P.; Zhou, J.; Li, Y.; Zhao, L. Periodontal health status in cirrhotic patients: A systematic review and meta-analysis. BMC Oral Health 2023, 23, 362. [Google Scholar] [CrossRef]
- López, R.; Retamales, C.; Contreras, C.; Montes, J.; Marin, A.; Vaeth, M.; Baelum, V. Reliability of clinical attachment level recordings: Effects on prevalence, extent, and severity estimates. J. Periodontol. 2003, 74, 512–520. [Google Scholar] [CrossRef] [PubMed]
- Zhang, C.Z.; Cheng, X.Q.; Li, J.Y.; Zhang, P.; Yi, P.; Xu, X.; Zhou, X.D. Saliva in the diagnosis of diseases. Int. J. Oral. Sci. 2016, 8, 133–137. [Google Scholar] [CrossRef] [PubMed]
- Irie, Y.; Tatsukawa, N.; Iwamoto, Y.; Nakano, M.; Ogasawara, T.; Sakurai, K.; Mitsuhata, C.; Kozai, K. Investigation of pediatric specifications for the Salivary Multi Test saliva test system. Pediatr. Dent. J. 2018, 28, 148–153. [Google Scholar] [CrossRef]
- Jung, E.H.; Jun, M.K. Relationship between an oral health risk assessment using a salivary multi-test system and woman’s subjective oral health symptoms and sleep disorder. Tohoku J. Exp. Med. 2021, 254, 213–219. [Google Scholar] [CrossRef]
- Wada, A.; Kabayama, M.; Godai, K.; Kido, M.; Ohata, Y.; Murakami, N.; Nakamura, Y.; Yoshida, H.; Hashimoto, S.; Higashi, M.; et al. Factors influencing the continuation of home blood pressure measurement in community-dwelling older adults: The NOSE study. J. Hypertens. 2024, 42, 694–700. [Google Scholar] [CrossRef]
- von Elm, E.; Altman, D.G.; Egger, M.; Pocock, S.J.; Gøtzsche, P.C.; Vandenbroucke, J.P.; STROBE Initiative. The Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement: Guidelines for reporting of observational studies. J. Clin. Epidemiol. 2008, 61, 344–349. [Google Scholar] [CrossRef]
- Kawamoto, M.; Tanaka, H.; Sakurai, A.; Otagiri, H.; Karasawa, I.; Yamada, S.I.; Kurita, H. Exploration of correlation of oral hygiene and condition with influenza infection. PLoS ONE 2021, 16, e0254981. [Google Scholar] [CrossRef]
- Ainamo, J.; Barmes, D.; Beagrie, G.; Cutress, T.; Martin, J.; Sardo-Infirri, J. Development of the World Health Organization (WHO) Community Periodontal Index of Treatment Needs (CPITN). Int. Dent. J. 1982, 32, 281–291. [Google Scholar]
- World Health Organization. Oral Health Surveys: Basic Methods, 5th ed.; WHO: Geneva, Switzerland, 2013; Available online: https://www.who.int/publications/i/item/9789241548649 (accessed on 28 January 2025).
- Kosaka, T.; Ono, T.; Yoshimuta, Y.; Kida, M.; Kikui, M.; Nokubi, T.; Maeda, Y.; Kokubo, Y.; Watanabe, M.; Miyamoto, Y. The effect of periodontal status and occlusal support on masticatory performance: The Suita study. J. Clin. Periodontol. 2014, 41, 497–503. [Google Scholar] [CrossRef]
- Podzimek, S.; Vondrackova, L.; Duskova, J.; Janatova, T.; Broukai, Z. Salivary Markers for Periodontal and General Disease. Dis. Markers 2016, 2016, 9179632. [Google Scholar] [CrossRef]
- Corana, M.; Baima, G.; Iaderosa, G.; Franco, F.; Zhang, J.; Berta, G.N.; Romano, F.; Aimetti, M. Salivary Proteomics for Detecting Novel Biomarkers of Periodontitis: A Systematic Review. J. Periodontal. Res. 2024. published online. [Google Scholar] [CrossRef] [PubMed]
- Blanco-Pintos, T.; Requeira-Iglesias, A.; Seijo-Porto, I.; Balsa-Castro, C.; Castelo-Baz, P.; Nibali, L.; Tomás, I. Accuracy of periodontitis diagnosis obtained using multiple molecular biomarkers in oral fluids: A systematic review and meta-analysis. J. Clin. Periodontol. 2023, 50, 1420–1443. [Google Scholar] [CrossRef] [PubMed]
- Silva, M.L.V.; Viana, K.S.S.; de Arruda, J.A.A.; de Miranda, R.D.; Soares, M.C.F.; Calado, H.D.R.; Amorim, M.C.L.; Costa, F.O.; Cota, L.O.M.; Abreu, L.G.; et al. Volatile sulfur compounds, biofilm, and salivary parameters in patients with periodontal disease: A cross-sectional study. Odontology 2025, 113, 809–817. [Google Scholar] [CrossRef] [PubMed]
- Kosaka, T.; Kokubo, Y.; Ono, T.; Sekine, S.; Kida, M.; Kikui, M.; Yamamoto, M.; Watanabe, M.; Amano, A.; Maeda, Y.; et al. Salivary inflammatory cytokines may be novel markers of carotid atherosclerosis in a Japanese general population: The Suita study. Atherosclerosis 2014, 237, 123–128. [Google Scholar] [CrossRef]
- Kim, H.D.; Kim, S.; Jeon, S.; Kim, S.J.; Cho, H.J.; Choi, Y.N. Diagnostic and prognostic ability of salivary MMP-9 and S100A8 for periodontitis. J. Clin. Periodontol. 2020, 47, 1191–1200. [Google Scholar] [CrossRef]
- Relvas, M.; Mendes-Frias, A.; Goncalves, M.; Salazar, F.; López-Jarana, P.; Silvestre, R.; de Costa, A.V. Salivary IL-1β, IL-6, and IL-10 are key biomarkers of periodontitis severity. Int. J. Mol. Sci. 2024, 25, 8401. [Google Scholar] [CrossRef]
- Heiz-Mayfield, L.J.A. Conventional diagnostic criteria for periodontal diseases (plaque-induced gingivitis and periodontitis). Periodontology 2000 2024, 95, 10–19. [Google Scholar] [CrossRef]
- Swets, J.A. Measuring the accuracy of diagnostic systems. Science 1988, 240, 1285–1293. [Google Scholar] [CrossRef]
- Teles, F.R.F.; Chandrasekaran, G.; Martin, L.; Patel, M.; Kallan, M.J.; Furquim, C.; Hamza, T.; Cucchiara, A.J.; Kantarci, A.; Urquhart, O.; et al. Salivary and serum inflammatory biomarkers during periodontitis progression and after treatment. J. Clin. Periodontol. 2024, 51, 1619–1631. [Google Scholar] [CrossRef]
- Relvas, M.; Tomás, I.; Salazar, F.; Velazco, C.; Blanco, J.; Diz, P. Reliability of partial-mouth recording systems to determine periodontal status: A pilot study in an adult Portuguese population. J. Periodontol. 2014, 85, e188–e197. [Google Scholar] [CrossRef]
- Shirone, K.; Ogawa, H.; Hirotomi, T.; Takano, N.; Yamaga, T.; Kaneko, N.; Sakuma, S.; Yoshihara, A.; Miyazaki, H. Evaluation of CPI and loss of attachment scoring methods (WHO) and longitudinal study on periodontal conditions in Japanese elderly cohort. J. Dent. Health 2007, 57, 28–35. [Google Scholar] [CrossRef]
- Noh, J.W.; Jang, J.H.; Yoon, H.S.; Kim, K.B.; Heo, M.H.; Jang, H.E.; Kim, Y.J.; Lee, Y. Evaluation of Salivary Biomarkers of Periodontal Disease Based on Smoking Status: A Systematic Review. Int. J. Environ. Res. Public Health 2022, 19, 14619. [Google Scholar] [CrossRef] [PubMed]
- Altıngöz, S.M.; Kurgan, Ş.; Önder, C.; Serdar, M.A.; Ünlütürk, U.; Uyanık, M.; Başkal, N.; Tatakis, D.N.; Günhan, M. Salivary and serum oxidative stress biomarkers and advanced glycation end products in periodontitis patients with or without diabetes: A cross-sectional study. J. Periodontol. 2021, 92, 1274–1285. [Google Scholar] [CrossRef] [PubMed]
SMT Items | Periodontal Pocket | p-Value | Gingival Inflammation | p-Value | |||
---|---|---|---|---|---|---|---|
Without | With | Without | With | ||||
n | 307 | 65 | 279 | 93 | |||
Occult blood | 44.0 (28.0–60.0) | 57.0 (43.0–70.0) | <0.001 | 44.0 (30.0–60.0) | 54.0 (35.0–66.0) | 0.019 | |
Normal | 170 (89.9) | 19 (10.1) | <0.001 | 155 (82.0) | 34 (18.0) | 0.002 | |
Higher | 137 (74.9) | 46 (25.1) | 124 (67.8) | 59 (32.2) | |||
Leukocyte | 76.0 (62.0–88.0) | 81.0 (68.5–89.0) | 0.132 | 76.0 (62.0–88.0) | 80.0 (68.5–87.5) | 0.127 | |
Normal | 166 (86.9) | 25 (13.1) | 0.028 | 150 (78.5) | 41 (21.5) | 0.120 | |
Higher | 141 (77.9) | 40 (22.1) | 129 (71.3) | 52 (28.7) | |||
Protein | 73.0 (60.0–85.0) | 81.0 (69.5–95.5) | 0.002 | 73.0 (60.0–87.0) | 79.0 (64.0–88.5) | 0.131 | |
Normal | 169 (88.0) | 23 (12.0) | 0.004 | 153 (79.7) | 39 (20.3) | 0.041 | |
Higher | 138 (76.7) | 42 (23.3) | 126 (70.0) | 54 (30.0) |
SMT Items | Periodontal Status | Sensitivity | Specificity | PPV | NPV | AUC |
---|---|---|---|---|---|---|
Occult blood | Periodontal pocket | 71% (60–82) | 55% (49–61) | 25% (15–36) | 90% (87–93) | 0.672 (0.605–0.738) |
Gingival inflammation | 57% (45–69) | 56% (50–61) | 32% (21–43) | 82% (78–86) | 0.588 (0.520–0.656) | |
Leukocyte | Periodontal pocket | 62% (50–74) | 54% (48–60) | 22% (12–32) | 87% (83–91) | 0.606 (0.533–0.680) |
Gingival inflammation | 56% (44–68) | 54% (48–60) | 29% (18–40) | 79% (74–84) | 0.555 (0.488–0.621) | |
Protein | Periodontal pocket | 65% (53–77) | 55% (49–61) | 23% (13–33) | 88% (84–92) | 0.638 (0.562–0.714) |
Gingival inflammation | 58% (46–70) | 55% (49–61) | 30% (19–41) | 80% (76–84) | 0.557 (0.489–0.625) |
Combinations of SMT Items | Periodontal Pocket | p-Value | Gingival Inflammation | p-Value | ||
---|---|---|---|---|---|---|
Without | With | Without | With | |||
n | 307 | 65 | 279 | 93 | ||
Occult blood and leukocyte | ||||||
Occult blood (−) and leukocyte (−) | 115 (92.7) | 9 (7.3) | 0.001 | 103 (83.1) | 21 (16.9) | 0.014 |
Occult blood (−) and leukocyte (+) | 55 (84.6) | 10 (15.4) | 52 (80.0) | 13 (20.0) | ||
Occult blood (+) and leukocyte (−) | 51 (76.1) | 16 (23.9) | 47 (70.1) | 20 (29.9) | ||
Occult blood (+) and leukocyte (+) | 86 (74.1) | 30 (25.9) | 77 (66.4) | 39 (33.6) | ||
Leukocyte and protein | ||||||
Leukocyte (−) and protein (−) | 115 (89.8) | 13 (10.2) | 0.015 | 104 (81.3) | 24 (18.8) | 0.132 |
Leukocyte (−) and protein (+) | 51 (81.0) | 12 (19.0) | 46 (73.0) | 17 (27.0) | ||
Leukocyte (+) and protein (−) | 54 (84.4) | 10 (15.6) | 49 (76.6) | 15 (23.4) | ||
Leukocyte (+) and protein (+) | 87 (74.4) | 30 (25.6) | 80 (68.4) | 37 (31.6) | ||
Occult blood and protein | ||||||
Occult blood (−) and protein (−) | 123 (89.1) | 15 (10.9) | <0.001 | 113 (81.9) | 25 (18.1) | 0.008 |
Occult blood (−) and protein (+) | 47 (92.2) | 4 (7.8) | 42 (82.4) | 9 (17.6) | ||
Occult blood (+) and protein (−) | 46 (85.2) | 8 (14.8) | 40 (74.1) | 14 (25.9) | ||
Occult blood (+) and protein (+) | 91 (70.5) | 38 (29.5) | 84 (65.1) | 45 (34.9) |
Combinations of SMT Items | All, n | Cases, n | ORs | 95% CI | p-Value |
---|---|---|---|---|---|
Occult blood and leukocyte | |||||
Occult blood (−) and leukocyte (−) | 124 | 9 | ref | ||
Occult blood (−) and leukocyte (+) | 65 | 10 | 2.36 | 0.90–6.16 | 0.081 |
Occult blood (+) and leukocyte (−) | 67 | 16 | 3.92 | 1.61–9.54 | 0.003 |
Occult blood (+) and leukocyte (+) | 116 | 30 | 4.55 | 2.04–10.12 | <0.001 |
Leukocyte and protein | |||||
Leukocyte (−) and protein (−) | 128 | 13 | ref | ||
Leukocyte (−) and protein (+) | 63 | 12 | 2.16 | 0.91–5.11 | 0.081 |
Leukocyte (+) and protein (−) | 64 | 10 | 1.85 | 0.75–4.53 | 0.181 |
Leukocyte (+) and protein (+) | 117 | 30 | 3.04 | 1.49–6.19 | 0.002 |
Occult blood and protein | |||||
Occult blood (−) and Protein (−) | 138 | 15 | ref | ||
Occult blood (−) and Protein (+) | 51 | 4 | 0.68 | 0.21–2.17 | 0.515 |
Occult blood (+) and Protein (−) | 54 | 8 | 1.45 | 0.58–3.67 | 0.430 |
Occult blood (+) and Protein (+) | 129 | 38 | 3.38 | 1.74–6.55 | <0.001 |
Combinations of SMT Items | All, n | Cases, n | ORs | 95% CI | p-Value |
---|---|---|---|---|---|
Occult blood and leukocyte | |||||
Occult blood (−) and leukocyte (−) | 124 | 68 | ref | ||
Occult blood (−) and leukocyte (+) | 65 | 30 | 1.23 | 0.57–2.65 | 0.603 |
Occult blood (+) and leukocyte (−) | 67 | 47 | 2.13 | 1.05–4.33 | 0.036 |
Occult blood (+) and leukocyte (+) | 116 | 83 | 2.50 | 1.36–4.59 | 0.003 |
Leukocyte and protein | |||||
Leukocyte (−) and protein (−) | 128 | 70 | ref | ||
Leukocyte (−) and protein (+) | 63 | 37 | 1.65 | 0.81–3.37 | 0.172 |
Leukocyte (+) and protein (−) | 64 | 45 | 1.35 | 0.65–2.81 | 0.426 |
Leukocyte (+) and protein (+) | 117 | 76 | 2.01 | 1.11–3.63 | 0.021 |
Occult blood and protein | |||||
Occult blood (−) and Protein (−) | 138 | 72 | ref | ||
Occult blood (−) and Protein (+) | 51 | 26 | 0.96 | 0.42–2.23 | 0.929 |
Occult blood (+) and Protein (−) | 54 | 35 | 1.59 | 0.75–3.35 | 0.228 |
Occult blood (+) and Protein (+) | 129 | 95 | 2.47 | 1.40–4.35 | 0.002 |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2025 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Kosaka, T.; Fushida, S.; Wada, M.; Gonda, T.; Hatta, K.; Kuboniwa, M.; Wada, A.; Hashimoto, S.; Hatanaka, H.; Higashi, M.; et al. Effectiveness of a Salivary Testing System to Screen for Periodontal Disease: A Cross-Sectional Study from the NOSE Study. J. Clin. Med. 2025, 14, 4965. https://doi.org/10.3390/jcm14144965
Kosaka T, Fushida S, Wada M, Gonda T, Hatta K, Kuboniwa M, Wada A, Hashimoto S, Hatanaka H, Higashi M, et al. Effectiveness of a Salivary Testing System to Screen for Periodontal Disease: A Cross-Sectional Study from the NOSE Study. Journal of Clinical Medicine. 2025; 14(14):4965. https://doi.org/10.3390/jcm14144965
Chicago/Turabian StyleKosaka, Takayuki, Shuri Fushida, Masahiro Wada, Tomoya Gonda, Kodai Hatta, Masae Kuboniwa, Arisa Wada, Sumiyo Hashimoto, Hiromi Hatanaka, Makiko Higashi, and et al. 2025. "Effectiveness of a Salivary Testing System to Screen for Periodontal Disease: A Cross-Sectional Study from the NOSE Study" Journal of Clinical Medicine 14, no. 14: 4965. https://doi.org/10.3390/jcm14144965
APA StyleKosaka, T., Fushida, S., Wada, M., Gonda, T., Hatta, K., Kuboniwa, M., Wada, A., Hashimoto, S., Hatanaka, H., Higashi, M., Kikuchi, T., Terauchi, K., Kido, M., Akagi, Y., Kamide, K., Kabayama, M., & Ikebe, K. (2025). Effectiveness of a Salivary Testing System to Screen for Periodontal Disease: A Cross-Sectional Study from the NOSE Study. Journal of Clinical Medicine, 14(14), 4965. https://doi.org/10.3390/jcm14144965