Effects of smoking on salivary C-telopeptide pyridinoline cross-links of type I collagen and osteocalcin levels
Abstract
Aim This study was planned to investigate whether smoker patients with inflammatory periodontal disease exhibit different salivary concentrations of C-telopeptide pyridinoline cross-links of type I collagen (ICTP) and osteocalcin (OC) compared to the non-smoker and/or ex-smoker counterparts.Methods Whole saliva samples, full-mouth clinical periodontal recordings were obtained from 67 otherwise healthy patients with inflammatory periodontal disease. According to self-reports there were 34 smokers, 22 non-smokers and 11 ex-smokers. Salivary cotinine, ICTP and OC levels were determined by enzyme-linked immunoassays.Results Salivary cotinine measurements confirmed self-reports about smoking. Smoker patients revealed significantly higher plaque index values than non-smokers (p<0.05). Bleeding on probing values were significantly lower in smoker group than ex-smoker group (p<0.05). There was no significant difference between the study groups in salivary ICTP levels (p>0.05). OC levels in smoker group was significantly lower than the other groups (p<0.001). Salivary ICTP levels correlated negatively with number of teeth present (p<0.05), positively with bleeding on probing (p<0.01). Salivary OC levels correlated negatively with years smoked (p<0.01).Conclusions Within the limits of this study, smoking seems to suppress salivary osteocalcin level but ICTP levels seem not to be affected by smoking status. This suppression in OC levels may be one mechanism of deteriorating effects of smoking on periodontal health.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Smoking significantly decreased salivary levels of osteocalcin.
“Gürlek et al. reported that smoking significantly decreased salivary levels of osteocalcin (OC, later stage of osteogenic differentiation) [81].”
From An Overlooked Bone Metabolic Disorder: Cigarette Smoking-Induced Osteoporosis (2022) · cites this paper as [81]
Cites
A Simple Sequentially Rejective Multiple Test Procedure
(1979) · Scandinavian Journal of Statistics · doi:10.2307/4615733 · Cited by 21,526 · see citing works
Navazesh, M. (1993) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1993.tb18343.x · Cited by 1,449 · see citing works
Assessment of Risk for Periodontal Disease. I. Risk Indicators for Attachment Loss
Grossi, S. G., Zambon, J. J., Ho, A. W., Koch, G. G., Dunford, R. G., Machtei, E. E., Norderyd, O. M., & Genco, R. J. (1994) · Journal of Periodontology · doi:10.1902/jop.1994.65.3.260 · Cited by 1,127 · see citing works
Assessment of Risk for Periodontal Disease. II. Risk Indicators for Alveolar Bone Loss
Grossi, S. G., Genco, R. J., Machtet, E. E., Ho, A. W., Koch, G. G., Dunford, R. G., Zambon, J. J., & Hausmann, E. (1995) · Journal of Periodontology · doi:10.1902/jop.1995.66.1.23 · Cited by 735 · see citing works
Evidence for Cigarette Smoking as a Major Risk Factor for Periodontitis
Haber, J., Wattles, J., Crowley, M., Mandell, R. L., JOSHIPURA, K. J., & Kent, R. (1993) · Journal of Periodontology · doi:10.1902/jop.1993.64.1.16 · Cited by 602 · see citing works
Saliva: its secretion, composition and functions
Edgar, W. M. (1992) · BDJ · doi:10.1038/sj.bdj.4807861 · Cited by 573 · see citing works
Biochemical Markers of Bone Metabolism: An Overview
Christenson, R. H. (1997) · Clinical Biochemistry · doi:10.1016/s0009-9120(97)00113-6 · Cited by 544 · see citing works
Mechanisms of action of environmental factors – tobacco smoking
Palmer, R. M. J., Wilson, R. F., Hasan, A., & Scott, D. A. (2005) · Journal Of Clinical Periodontology · doi:10.1111/j.1600-051x.2005.00786.x · Cited by 525 · see citing works
Cigarette Smoking and the Periodontal Patient
Johnson, G. K., & HILL, M. A. (2004) · Journal of Periodontology · doi:10.1902/jop.2004.75.2.196 · Cited by 402 · see citing works
Analysis of saliva for periodontal diagnosis
Kaufman, E., & Lamster, I. B. (2000) · Journal Of Clinical Periodontology · doi:10.1034/j.1600-051x.2000.027007453.x · Cited by 393 · see citing works
Smoking and Periodontal Disease
Kinane, D. F., & Chestnutt, I. G. (2000) · Critical Reviews in Oral Biology & Medicine · doi:10.1177/10454411000110030501 · Cited by 355 · see citing works
Effects of smoking on periodontal tissues
Calsina, G., Ramon, J. M., & Echeverría, J. J. (2002) · Journal Of Clinical Periodontology · doi:10.1034/j.1600-051x.2002.290815.x · Cited by 349 · see citing works
Dental Plaque‐Induced Gingival Diseases
Mariotti, A. J. (1999) · Annals of Periodontology · doi:10.1902/annals.1999.4.1.7 · Cited by 334 · see citing works
Osteocalcin. Biochemical considerations and clinical applications
道脇幸博 (1988) · Clinical Orthopaedics and Related Research · Cited by 328 · see citing works
The effect of smoking on the response to periodontal therapy
Ah, M. K. B., Johnson, G. K., Kaldahl, W. B., Patil, K. D., & Kalkwart, K. L. (1994) · Journal Of Clinical Periodontology · doi:10.1111/j.1600-051x.1994.tb00285.x · Cited by 325 · see citing works
Barbour, S. E., Nakashima, K., Zhang, J.-B., Tangada, S. D., Hahn, C., Schenkein, H. A., & Tew, J. G. (1997) · Critical Reviews in Oral Biology & Medicine · doi:10.1177/10454411970080040501 · Cited by 253 · see citing works
Chapple, I., Mason, G. I., Garner, I., Matthews, J. B., Thorpe, G. H. G., Maxwell, S. R. J., & Whitehead, T. P. (1997) · Annals of Clinical Biochemistry International Journal of Laboratory Medicine · doi:10.1177/000456329703400413 · Cited by 171 · see citing works
The response of human bone marrow to chronic cigarette smoking
van Eeden, S. F., & Hogg, J. C. (2000) · European Respiratory Journal · doi:10.1034/j.1399-3003.2000.15e18.x · Cited by 161 · see citing works
Connective tissues of the periodontium: a summary of current work.
Narayanan, A. S., & Page, R. C. (1983) · PubMed · Cited by 149 · see citing works
Osteocalcin. Biochemical considerations and clinical applications
LIAN, J. B., & GUNDBERG, C. M. (1988) · Clinical Orthopaedics and Related Research · doi:10.1097/00003086-198801000-00036 · Cited by 149 · see citing works
Renvert, S., Dahlén, G., & Wikström, M. B. (1998) · Journal Of Clinical Periodontology · doi:10.1111/j.1600-051x.1998.tb02421.x · Cited by 148 · see citing works
Connective Tissues of the Periodontium: A Summary of Current Work
Narayanan, A. S., & Page Roy, C. (1983) · Collagen and Related Research · doi:10.1016/s0174-173x(83)80047-8 · Cited by 148 · see citing works
Occurrence of periopathogens in smoker and non‐smoker patients
Preber, H., Bergström, J., & Linder, L. E. (1992) · Journal Of Clinical Periodontology · doi:10.1111/j.1600-051x.1992.tb01716.x · Cited by 144 · see citing works
Smoking and crevicular fluid levels of IL‐6 and TNF‐a in periodontal disease
Boström, L., Linder, L. E., & Bergström, J. (1999) · Journal Of Clinical Periodontology · doi:10.1034/j.1600-051x.1999.260604.x · Cited by 139 · see citing works
Nakashima, K., Roehrich, N., & Cimasoni, G. (1994) · Journal Of Clinical Periodontology · doi:10.1111/j.1600-051x.1994.tb00721.x · Cited by 126 · see citing works
Validation of smoking status in clinical research into inflammatory periodontal disease
Scott, D. A., Palmer, R. M. J., & Stapleton, J. (2001) · Journal Of Clinical Periodontology · doi:10.1034/j.1600-051x.2001.280801.x · Cited by 104 · see citing works
Murata, M., Tatsumi, J., Kato, Y., Suda, S., Nunokawa, Y., Kobayashi, Y., Takeda, H., Araki, H., Shin, K., Okuda, K., et al. (2002) · Clinical Oral Implants Research · doi:10.1034/j.1600-0501.2002.130610.x · Cited by 102 · see citing works
Effects of smoking and gingival inflammation on salivary antioxidant capacity
Buduneli, N., Kardeşler, L., Isşık, H., Willis, C. S., Hawkins, S. I., Kinane, D. F., & Scott, D. A. (2006) · Journal Of Clinical Periodontology · doi:10.1111/j.1600-051x.2006.00892.x · Cited by 97 · see citing works
Self-citationRezavandi, K., Palmer, R. M. J., Odell, E. W., Scott, D. A., & Wilson, R. F. (2002) · Journal of Oral Pathology and Medicine · doi:10.1046/j.0904-2512.2001.joptest.doc.x · Cited by 89 · see citing works
Effect of Locally Delivered Minocycline Microspheres on Markers of Bone Resorption
Oringer, R. J., Al‐Shammari, K. F., Aldredge, W. A., Iacono, V. J., Eber, R., Wang, H., Berwald, B., Nejat, R., & Giannobile, W. V. (2002) · Journal of Periodontology · doi:10.1902/jop.2002.73.8.835 · Cited by 79 · see citing works
Buduneli, N., Bıyıkoğlu, B., Sherrabeh, S., & Lappin, D. F. (2008) · Journal Of Clinical Periodontology · doi:10.1111/j.1600-051x.2008.01310.x · Cited by 75 · see citing works
Self-citationNicotine-induced release of elastase and eicosanoids by human neutrophils
Seow, W. K., Thong, Y. H., Nelson, R. D., MacFarlane, G. D., & Herzberg, M. C. (1994) · Inflammation · doi:10.1007/bf01534553 · Cited by 73 · see citing works
Markers of bone destruction and formation and periodontitis in type 1 diabetes mellitus
Lappin, D. F., Eapen, B., Robertson, D. P., Young, J., & Hodge, P. J. (2009) · Journal Of Clinical Periodontology · doi:10.1111/j.1600-051x.2009.01440.x · Cited by 71 · see citing works
Self-citationGingival crevicular fluid osteocalcin in adult periodontitis
Lee, A. J., Walsh, T. F., Hodges, S. J., & Rawlinson, Ā. (1999) · Journal Of Clinical Periodontology · doi:10.1034/j.1600-051x.1999.260409.x · Cited by 67 · see citing works
A Cross‐Sectional Study on Osteocalcin Levels in Gingival Crevicular Fluid From Periodontal Patients
Kunimatsu, K., Mataki, S., Tanaka, H., Mine, N., Kiyoki, M., Hosoda, K., Kato, Y., & Kato, I. (1993) · Journal of Periodontology · doi:10.1902/jop.1993.64.9.865 · Cited by 54 · see citing works
C‐Telopeptide Pyridinoline Cross‐Links: Sensitive Indicators of Periodontal Tissue Destruction
Giannobile, W. V. (1999) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1999.tb07698.x · Cited by 54 · see citing works
The influence of tobacco smoking on adhesion molecule profiles
Scott, D. A., & Palmer, R. (2003) · Tobacco Induced Diseases · doi:10.1186/1617-9625-1-1-7 · Cited by 49 · see citing works
Oringer, R. J., Palys, M. D., Iranmanesh, A., Fiorellini, J. P., Haffajee, A. D., Socransky, S. S., & Giannobile, W. V. (1998) · Clinical Oral Implants Research · doi:10.1034/j.1600-0501.1996.090602.x · Cited by 48 · see citing works
A one step sandwich enzyme immunoassay for γ-carboxylated osteocalcin using monoclonal antibodies
Koyama, N., Ohara, K., Yokota, H., Kurome, T., Katayama, M., Hino, F., Kato, I., & Akai, T. (1991) · Journal of Immunological Methods · doi:10.1016/0022-1759(91)90346-h · Cited by 46 · see citing works
Plasminogen activator system in smokers and non‐smokers with and without periodontal disease
Buduneli, N., Buduneli, E., Kardeşler, L., Lappin, D. F., & Kinane, D. F. (2005) · Journal Of Clinical Periodontology · doi:10.1111/j.1600-051x.2005.00694.x · Cited by 35 · see citing works
Self-citationBiochemical markers of bone metabolism in the assessment of osteoporosis: Useful or not?
Seibel, M. J. (2003) · Journal of Endocrinological Investigation · doi:10.1007/bf03345204 · Cited by 29 · see citing works
Yoshihara, A., Deguchi, T., Hanada, N., & Miyazaki, H. (2009) · Oral Diseases · doi:10.1111/j.1601-0825.2008.01511.x · Cited by 25 · see citing works
Buduneli, E., Buduneli, N., Vardar‐Şengül, S., Kardeşler, L., Atilla, G., Lappin, D. F., & Kinane, D. F. (2005) · Journal of Periodontology · doi:10.1902/jop.2005.76.11.1927 · Cited by 24 · see citing works
Self-citationEvaluation of the relationship between smoking during pregnancy and subgingival microbiota
Buduneli, N., Baylas, H., Buduneli, E., Türkoğlu, O., & Dahlén, G. (2005) · Journal Of Clinical Periodontology · doi:10.1111/j.1600-051x.2004.00633.x · Cited by 22 · see citing works
Self-citationTümer, C., Aksoy, Y., Güncü, G. N., Nohutçu, R. M., KILINC, K., & Tözüm, T. F. (2008) · Journal of Oral Rehabilitation · doi:10.1111/j.1365-2842.2008.01879.x · Cited by 18 · see citing works
The influence of tobacco smoking on adhesion molecule profiles
Scott, D., & Palmer, R. (2003) · Tobacco Induced Diseases · doi:10.1186/1617-9625-1-3 · Cited by 16 · see citing works
[Analysis of serum osteocalcin of patients with periodontitis].
Shi, F., Yu, S., & Xu, L. (1996) · PubMed · Cited by 11 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Buduneli, N., & Kinane, D. F. (2011) · Journal Of Clinical Periodontology · doi:10.1111/j.1600-051x.2010.01670.x · Cited by 348 · see citing works
Self-citationGürsoy, U. K., Könönen, E., Huumonen, S., Tervahartiala, T. I., Pussinen, P. J., Suominen, A. L., & Sorsa, T. A. (2012) · Journal Of Clinical Periodontology · doi:10.1111/jcpe.12020 · Cited by 158 · see citing works
The Effect of Tobacco Smoking on Musculoskeletal Health: A Systematic Review
AL-Bashaireh, A. M., Haddad, L. G., Weaver, M., Kelly, D. L., Chengguo, X., & Yoon, S. (2018) · Journal of Environmental and Public Health · doi:10.1155/2018/4184190 · Cited by 128 · see citing works
Bone remodeling‐associated salivary biomarker MIP‐1α distinguishes periodontal disease from health
Al‐Sabbagh, M., Alladah, A., Lin, Y., Kryscio, R. J., Thomas, M. V., Ebersole, J. L., & Miller, C. S. (2011) · Journal of Periodontal Research · doi:10.1111/j.1600-0765.2011.01445.x · Cited by 94 · see citing works
An Overlooked Bone Metabolic Disorder: Cigarette Smoking-Induced Osteoporosis
Weng, W., Li, H., & Zhu, S. (2022) · Genes · doi:10.3390/genes13050806 · Cited by 65 · see citing works
Bone turnover in passive smoking female rat: relationships to change in bone mineral density
Gao, S.-G., Li, K.-H., Xu, M., Jiang, W., Shen, H., Luo, W., Xu, W.-S., Tian, J., & Lei, G.-H. (2011) · BMC Musculoskeletal Disorders · doi:10.1186/1471-2474-12-131 · Cited by 37 · see citing works
Negri, B. M., Pimentel, S. P., Casati, M. Z., Cirano, F. R., Casarin, R. C. V., & Ribeiro, F. V. (2016) · Archives of Oral Biology · doi:10.1016/j.archoralbio.2016.05.014 · Cited by 32 · see citing works
Secondhand Smoke and Periodontal Disease: Atherosclerosis Risk in Communities Study
Sanders, A. E., Slade, G. D., Beck, J. D., & Ágústsdóttir, H. (2011) · American Journal of Public Health · doi:10.2105/ajph.2010.300069 · Cited by 28 · see citing works
Salivary osteocalcin levels are decreased in smoker chronic periodontitis patients
Özçaka, Ö., Nalbantsoy, A., & Buduneli, N. (2010) · Oral Diseases · doi:10.1111/j.1601-0825.2010.01721.x · Cited by 24 · see citing works
Self-citationSalivary Osteocalcin as Potential Diagnostic Marker of Periodontal Bone Destruction among Smokers
Joseph, B., Javali, M. A., Khader, M. A., AlQahtani, S. M., & Amanullah, M. R. (2020) · Biomolecules · doi:10.3390/biom10030380 · Cited by 18 · see citing works
Smoking influences salivary histamine levels in periodontal disease
Bertl, K., Haririan, H., Laky, M., Matĕjka, M., Andrukhov, O., & Rausch‐Fan, X. (2011) · Oral Diseases · doi:10.1111/j.1601-0825.2011.01891.x · Cited by 14 · see citing works
Ameer, L. A. A., & Ali, B. G. (2015) · Journal of Baghdad College of Dentistry · doi:10.12816/0015305 · Cited by 12 · see citing works
Comparison of Bone Turnover Markers between Young Adult Male Smokers and Nonsmokers
Al-Bashaireh, A. M., & Alqudah, O. M. (2020) · Cureus · doi:10.7759/cureus.6782 · Cited by 11 · see citing works
Özçaka, Ö., Nalbantsoy, A., Bıçakçı, N., Köse, T., & Buduneli, N. (2010) · Inflammation · doi:10.1007/s10753-010-9225-0 · Cited by 9 · see citing works
Self-citationEffects of Tobacco Smoking on Chronic Periodontitis and Periodontal Treatment
Buduneli, N. (2012) · InTech eBooks · doi:10.5772/39169 · Cited by 6 · see citing works
Self-citationAgrawal, P., Pandit, A., Malagi, S. K., Abraham, D. V., Vasant, B., & Tembhurne, S. (2024) · Cureus · doi:10.7759/cureus.66236 · Cited by 4 · see citing works
Ketabi, M., Manoochehr, M., & Rafiei, E. (2015) · Res Dent Sci · Cited by 2 · see citing works
SecondhandSmokeandPeriodontalDisease:Atherosclerosis RiskinCommunitiesStudy
Sanders, A. E., Slade, G. D., & Beck, J. D. (2011)
Clinical Diagnostics and Patient Stratification for Use in the Dental Office
Plonka, A. B., & Giannobile, W. V. (2015) · Springer eBooks · doi:10.1007/978-3-319-23297-3_5
Kouvelis, G., Davidopoulou, S., Kolokitha, O., Papadopoulos, M., & Chatzigianni, A. (2023) · Applied Sciences · doi:10.3390/app132413012 · Cited by 1 · see citing works
- Authors
- Gürlek, Ö., Lappin, D. F., & Buduneli, N.
- Affiliations
- Ege University (TR)
- University of Glasgow (GB)
- Venue
- Archives of Oral Biology
- Publisher
- Elsevier BV
- Published
- 2009-12
- Volume
- 54
- Issue
- 12
- Pages
- 1099-1104
- ISSN
- 0003-9969 (ISSN-L)
- OpenAlex
- W2034640304
- Cited by
- 20
- References
- 47
- Citations by year
- 2024: 1 · 2023: 1 · 2022: 1 · 2020: 2 · 2018: 1 · 2016: 1 · 2015: 3 · 2012: 2
- FWCI
- 3.51
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Archives of Oral Biology (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Dentistry › Periodontics › Oral microbiology and periodontitis research
- Health Sciences › Medicine › Physiology › Smoking Behavior and Cessation
- Health Sciences › Dentistry › Periodontics › Oral Health Pathology and Treatment
- Keywords
- smoking, salivary biomarkers, type I collagen, osteocalcin, inflammatory periodontal diseases, cotinine, former smokers, plaque index, bleeding on probing, periodontal health
- MeSH terms
- Adult, Analysis of Variance, Cotinine, Female, Humans, Indicators and Reagents, Male, Middle Aged, Peptides, Periodontal Index, Periodontitis, Salivary Proteins and Peptides, Smoking, Osteocalcin, Collagen Type I
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
