Skip to main content

Advertisement

SpringerLink
Log in

The tendency of reduced periodontal destruction in acromegalic patients showing similar inflammatory status with periodontitis patients

  • Original Article
  • Published:
Endocrine Aims and scope Submit manuscript

Abstract

Purpose

Evaluate periodontal status of acromegalics through clinical and biochemical variables.

Methods

Demographics, hormone and metabolic variables, periodontal variables, gingival crevicular fluid (GCF) volume, and content data were collected from 30 patients with acromegaly, 30 patients with periodontitis, and 20 healthy subjects and comparatively analyzed.

Results

GH differences between acromegaly (2.56 ± 4.86) and periodontitis (0.53 ± 0.95) (p < 0.001) were statistically significant. IGF-1 was lowest at periodontitis (113.31 ± 45.01) and lower (152.11 ± 45.56) at healthy group compared with acromegalics (220.38 ± 167.62) (p < 0.05). GH and IGF-1 had positive correlation (p < 0.05). IGF-1 and CAL had negative (p < 0.01) correlation except healthy group that showed the same correlation at the opposite direction (p < 0.05). Besides similar plaque and gingival indices with periodontitis, acromegalics showed relatively less CAL and GCF volume but except CAL, all their periodontal variables were higher than healthy subjects. GCF GH and prolactin showed higher values in acromegalics while healthy subjects showed relatively high interleukin-1, -10 and carboxyterminal telopeptide of type I collagen compared with others.

Conclusion

Acromegalics have a tendency of slowed periodontal destruction with an influence of GH and IGF-1 to the inflammation- and collage metabolism-related mechanisms rather than bone-associated ones. However, this information must be confirmed with further studies exploring the mechanisms possibly bonded to others.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. A. Lavrentaki, A. Paluzzi, J.A. Wass, N. Karavitaki, Epidemiology of acromegaly: review of population studies. Pituitary 20(1), 4–9 (2017). https://doi.org/10.1007/s11102-016-0754-x

    Article  Google Scholar 

  2. Schilbach, K., Strasburger, C. J., Bidlingmaier, M, Biochemical investigations in diagnosis and follow up of acromegaly. Pituitary 20(1), 33–45 (2017). https://doi.org/10.1007/s11102-017-0792-z

    Article  CAS  Google Scholar 

  3. R. Zahr, M. Fleseriu, Updates in diagnosis and treatment of acromegaly. Eur. Endocrinol. 14(2), 57–61 (2018). https://doi.org/10.17925/EE.2018.14.2.57

    Article  PubMed  PubMed Central  Google Scholar 

  4. A.P. Heaney, S. Melmed, Molecular targets in pituitary tumours. Nat. Rev. Cancer 4(4), 285–295 (2004). https://doi.org/10.1038/nrc1320

    Article  CAS  PubMed  Google Scholar 

  5. S. Melmed, A. Colao, A. Barkan, M. Molitch, A.B. Grossman, D. Kleinberg, D. Clemmons, P. Chanson, E. Laws, J. Schlechte, M.L. Vance, K. Ho, A. Giustina, Acromegaly Consensus Group, Guidelines for acromegaly management: an update. J. Clin. Endocrinol. Metab. 94(5), 1509–1517 (2009). https://doi.org/10.1210/jc.2008-2421

    Article  CAS  PubMed  Google Scholar 

  6. L. Vilar, C.F. Vilar, R. Lyra, R. Lyra, L.A. Naves, Acromegaly: clinical features at diagnosis. Pituitary 20(1), 22–32 (2017). https://doi.org/10.1007/s11102-016-0772-8

    Article  PubMed  Google Scholar 

  7. M. Dural, G. Kabakci, N. Cinar, T. Erbas, U. Canpolat, K.M. Gurses, L. Tokgozoglu, A. Oto, E.B. Kaya, H. Yorgun, L. Sahiner, S. Dagdelen, K. Aytemir, Assessment of cardiac autonomic functions by heart rate recovery, heart rate variability and QT dynamicity parameters in patients with acromegaly. Pituitary 17(2), 163–170 (2014). https://doi.org/10.1007/s11102-013-0482-4

    Article  CAS  PubMed  Google Scholar 

  8. I.M. Holdaway, R.C. Rajasoorya, G.D. Gamble, Factors influencing mortality in acromegaly. J. Clin. Endocrinol. Metab. 89(2), 667–674 (2004). https://doi.org/10.1210/jc.2003-031199

    Article  CAS  PubMed  Google Scholar 

  9. A. Colao, D. Ferone, P. Marzullo, G. Lombardi, Systemic complications of acromegaly: epidemiology, pathogenesis, and management. Endocr. Rev. 25(1), 102–152 (2004). https://doi.org/10.1210/er.2002-0022

    Article  CAS  PubMed  Google Scholar 

  10. S. Dogan, A. Atmaca, S. Dagdelen, B. Erbas, T. Erbas, Evaluation of thyroid diseases and differentiated thyroid cancer in acromegalic patients. Endocrine 45(1), 114–121 (2014). https://doi.org/10.1007/s12020-013-9981-3

    Article  CAS  PubMed  Google Scholar 

  11. E. Ritvonen, E. Loyttyniemi, P. Jaatinen, T. Ebeling, L. Moilanen, P. Nuutila, R. Kauppinen-Makelin, C. Schalin-Jantti, Mortality in acromegaly: a 20-year follow-up study. Endocr. Relat. Cancer 23(6), 469–480 (2016). https://doi.org/10.1530/ERC-16-0106

    Article  CAS  PubMed  Google Scholar 

  12. A. Ciresi, M.C. Amato, R. Pivonello, E. Nazzari, L.F. Grasso, F. Minuto, D. Ferone, A. Colao, C. Giordano, The metabolic profile in active acromegaly is gender-specific. J. Clin. Endocrinol. Metab. 98(1), E51–E59 (2013). https://doi.org/10.1210/jc.2012-2896

    Article  CAS  PubMed  Google Scholar 

  13. C. Giordano, A. Ciresi, M.C. Amato, R. Pivonello, R.S. Auriemma, L.F. Grasso, A. Galluzzo, A. Colao, Clinical and metabolic effects of first-line treatment with somatostatin analogues or surgery in acromegaly: a retrospective and comparative study. Pituitary 15(4), 539–551 (2012). https://doi.org/10.1007/s11102-011-0365-5

    Article  CAS  PubMed  Google Scholar 

  14. J.L. Ebersole, D. Dawson 3rd, P. Emecen-Huja, R. Nagarajan, K. Howard, M.E. Grady, K. Thompson, R. Peyyala, A. Al-Attar, K. Lethbridge, S. Kirakodu, O.A. Gonzalez, The periodontal war: microbes and immunity. Periodontol. 2000 75(1), 52–115 (2017). https://doi.org/10.1111/prd.12222

    Article  PubMed  Google Scholar 

  15. R.J. Genco, W.S. Borgnakke, Risk factors for periodontal disease. Periodontol. 2000 62(1), 59–94 (2013). https://doi.org/10.1111/j.1600-0757.2012.00457.x

    Article  PubMed  Google Scholar 

  16. P.N. Papapanou, C. Susin, Periodontitis epidemiology: is periodontitis under-recognized, over-diagnosed, or both? Periodontol. 2000 75(1), 45–51 (2017). https://doi.org/10.1111/prd.12200

    Article  PubMed  Google Scholar 

  17. American academy of periodontology task force report on the update to the 1999 classification of periodontal diseases and conditions. J Periodontol. 86(7), 835–838 (2015). https://doi.org/10.1902/jop.2015.157001

  18. I. Kreitschmann-Andermahr, J. Kohlmann, B. Kleist, U. Hirschfelder, R. Buslei, M. Buchfelder, S. Siegel, Oro-dental pathologies in acromegaly. Endocrine 60(2), 323–328 (2018). https://doi.org/10.1007/s12020-018-1571-y

    Article  CAS  PubMed  Google Scholar 

  19. A. Ben-Shlomo, S. Melmed, Acromegaly. Endocrinol. Metab. Clin. North Am. 37(1), 101–122 (2008). https://doi.org/10.1016/j.ecl.2007.10.002.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. H. Serinsoz, M.E. Ertorer, S. Bascil, O. Bakiner, E. Bozkirli, N.B. Tutuncu, Low prevalence of periodontitis in acromegaly: growth hormone may exert a protective effect. Turk. J. Endocrinol. Metab. 19(2), 42–48 (2015). https://doi.org/10.4274/tjem.2687

    Article  Google Scholar 

  21. D.L. Lima, R.M. Montenegro Jr., A.P. Vieira, M.F. Albano, D.M. Rego, Absence of periodontitis in acromegalic patients. Clin. Oral. Invest. 13(2), 165–169 (2009). https://doi.org/10.1007/s00784-008-0216-6

    Article  Google Scholar 

  22. P. Chanson, S. Salenave, Acromegaly. Orphanet J. Rare Dis. 3, 17 (2008). https://doi.org/10.1186/1750-1172-3-17

    Article  PubMed  PubMed Central  Google Scholar 

  23. A.N. Harb, B. Holtfreter, N. Friedrich, H. Wallaschofski, M. Nauck, M. Albers, P. Meisel, R. Biffar, T. Kocher, Association between the insulin-like growth factor axis in serum and periodontitis in the study of health in pomerania: an exploratory study. J. Clin. Periodontol. 39(10), 931–939 (2012). https://doi.org/10.1111/j.1600-051X.2012.01935.x

    Article  CAS  PubMed  Google Scholar 

  24. A. Juul, Serum levels of insulin-like growth factor I and its binding proteins in health and disease. Growth Horm. IGF Res. 13(4), 113–170 (2003)

    Article  CAS  Google Scholar 

  25. J.I. Jones, D.R. Clemmons, Insulin-like growth factors and their binding proteins: biological actions. Endocr. Rev. 16(1), 3–34 (1995). https://doi.org/10.1210/edrv-16-1-3

    Article  CAS  PubMed  Google Scholar 

  26. W. Gotz, D. Kunert, D. Zhang, A. Kawarizadeh, S. Lossdorfer, A. Jager, Insulin-like growth factor system components in the periodontium during tooth root resorption and early repair processes in the rat. Eur. J. Oral. Sci. 114(4), 318–327 (2006). https://doi.org/10.1111/j.1600-0722.2006.00381.x

    Article  PubMed  Google Scholar 

  27. A.C. Sant’Ana, M.M. Marques, T.E. Barroso, E. Passanezi, M.L. de Rezende, Effects of TGF-beta1, PDGF-BB, and IGF-1 on the rate of proliferation and adhesion of a periodontal ligament cell lineage in vitro. J. Periodontol. 78(10), 2007–2017 (2007). https://doi.org/10.1902/jop.2007.070119

    Article  CAS  PubMed  Google Scholar 

  28. H.L. Levin, Some dental aspects of endocrine diseases. Oral. Surg. Oral. Med. Oral. Pathol. 19, 466–477 (1965)

    Article  CAS  Google Scholar 

  29. K.S. Mine, C. Nakagawa, T. Hiramoto, K. Murata, T. Tagawa, Gingivitis in acromegaly successfully treated with a growth hormone secretion inhibitor. Endocrinologist 17(1), 20–22 (2007). https://doi.org/10.1097/01.ten.0000257447.32994.da

    Article  Google Scholar 

  30. S. Bascil, H. Serinsoz, N.B. Tutuncu, Acromegaly is protective for periodontal tissue—advanced chronic periodontitis is rare in acromegalics. Bratisl. Lek. Listy 115(9), 588–592 (2014)

    CAS  PubMed  Google Scholar 

  31. J. Meyle, I. Chapple, Molecular aspects of the pathogenesis of periodontitis. Periodontol. 2000 69(1), 7–17 (2015). https://doi.org/10.1111/prd.12104

    Article  PubMed  Google Scholar 

  32. J. Moock, C. Albrecht, N. Friedrich, H. Volzke, M. Nauck, M. Koltowska-Haggstrom, T. Kohlmann, H. Wallaschofski, Health-related quality of life and IGF-1 in GH-deficient adult patients on GH replacement therapy: analysis of the German KIMS data and the Study of Health in Pomerania. Eur. J. Endocrinol. 160(1), 17–24 (2009). https://doi.org/10.1530/EJE-08-0738

    Article  CAS  PubMed  Google Scholar 

  33. G.C. Armitage, Development of a classification system for periodontal diseases and conditions. Ann. Periodontol. 4(1), 1–6 (1999). https://doi.org/10.1902/annals.1999.4.1.1

    Article  CAS  PubMed  Google Scholar 

  34. B. Rai, J. Kaur, S.C. Anand, Possible relationship between periodontitis and dementia in a North Indian old age population: a pilot study. Gerodontology 29(2), e200–e205 (2012). https://doi.org/10.1111/j.1741-2358.2010.00441.x

    Article  PubMed  Google Scholar 

  35. J. Silness, H. Loe, Periodontal disease in pregnancy. II. correlation between oral hygiene and periodontal condtion. Acta Odontol. Scand. 22, 121–135 (1964)

    Article  CAS  Google Scholar 

  36. H. Loe, J. Silness, PeriodontAl Disease in Pregnancy. I. prevalence and severity. Acta Odontol. Scand. 21, 533–551 (1963)

    Article  CAS  Google Scholar 

  37. D. Yilmaz, F. Caglayan, E. Buber, E. Kononen, Y. Aksoy, U.K. Gursoy, G.N. Guncu, Gingival crevicular fluid levels of human beta-defensin-1 in type 2 diabetes mellitus and periodontitis. Clin. Oral. Invest. 22(5), 2135–2140 (2018). https://doi.org/10.1007/s00784-018-2469-z

    Article  Google Scholar 

  38. H. Li, P.M. Bartold, C.Z. Zhang, R.W. Clarkson, W.G. Young, M.J. Waters, Growth hormone and insulin-like growth factor I induce bone morphogenetic proteins 2 and 4: a mediator role in bone and tooth formation? Endocrinology 139(9), 3855–3862 (1998). https://doi.org/10.1210/endo.139.9.6211

    Article  CAS  PubMed  Google Scholar 

  39. H. Li, P.M. Bartold, W.G. Young, Y. Xiao, M.J. Waters, Growth hormone induces bone morphogenetic proteins and bone-related proteins in the developing rat periodontium. J. Bone Min. Res. 16(6), 1068–1076 (2001). https://doi.org/10.1359/jbmr.2001.16.6.1068

    Article  CAS  Google Scholar 

  40. A. Giustina, G. Mazziotti, E. Canalis, Growth hormone, insulin-like growth factors, and the skeleton. Endocr. Rev. 29(5), 535–559 (2008). https://doi.org/10.1210/er.2007-0036

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. H.R. Haase, S. Ivanovski, M.J. Waters, P.M. Bartold, Growth hormone regulates osteogenic marker mRNA expression in human periodontal fibroblasts and alveolar bone-derived cells. J. Periodontal Res. 38(4), 366–374 (2003)

    Article  CAS  Google Scholar 

  42. J.G. Caton, G. Armitage, T. Berglundh, I.L.C. Chapple, S. Jepsen, K.S. Kornman, B.L. Mealey, P.N. Papapanou, M. Sanz, M.S. Tonetti, A new classification scheme for periodontal and peri-implant diseases and conditions - Introduction and key changes from the 1999 classification. J. Periodontol. 89(Suppl 1), 1–8 (2018). https://doi.org/10.1002/JPER.18-0157

    Article  Google Scholar 

  43. F. Boabaid, J.E. Berry, A.J. Koh, M.J. Somerman, L.K. McCcauley, The role of parathyroid hormone-related protein in the regulation of osteoclastogenesis by cementoblasts. J. Periodontol. 75(9), 1247–1254 (2004). https://doi.org/10.1902/jop.2004.75.9.1247

    Article  CAS  PubMed  Google Scholar 

  44. S. Feitosa Dda, B. Bezerra Bde, G.M. Ambrosano, F.H. Nociti, M.Z. Casati, E.A. Sallum, S. de Toledo, Thyroid hormones may influence cortical bone healing around titanium implants: a histometric study in rats. J. Periodontol. 79(5), 881–887 (2008). https://doi.org/10.1902/jop.2008.070466

    Article  CAS  PubMed  Google Scholar 

  45. A. Ishisaka, T. Ansai, I. Soh, K. Inenaga, A. Yoshida, C. Shigeyama, S. Awano, T. Hamasaki, K. Sonoki, Y. Takata, T. Takehara, Association of salivary levels of cortisol and dehydroepiandrosterone with periodontitis in older Japanese adults. J. Periodontol. 78(9), 1767–1773 (2007). https://doi.org/10.1902/jop.2007.070044

    Article  CAS  PubMed  Google Scholar 

  46. G. Rohini, S. Kalaivani, V. Kumar, S.A. Rajasekar, J. Tuckaram, V. Pandey, Estimation and comparison of serum cortisol levels in periodontally diseased patients and periodontally healthy individuals: a clinical-biochemical study. J. Pharm. Bioallied Sci. 7(Suppl 2), S457–S460 (2015). https://doi.org/10.4103/0975-7406.163501

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. M. Morishita, M. Miyagi, Y. Iwamoto, Effects of sex hormones on production of interleukin-1 by human peripheral monocytes. J. Periodontol. 70(7), 757–760 (1999). https://doi.org/10.1902/jop.1999.70.7.757

    Article  CAS  PubMed  Google Scholar 

  48. A.M. da Silva, H.N. Newman, D.A. Oakley, Psychosocial factors in inflammatory periodontal diseases. a review. J. Clin. Periodontol. 22(7), 516–526 (1995)

    Article  Google Scholar 

  49. T. Breivik, P.K. Opstad, P. Gjermo, P.S. Thrane, Effects of hypothalamic-pituitary-adrenal axis reactivity on periodontal tissue destruction in rats. Eur. J. Oral. Sci. 108(2), 115–122 (2000)

    Article  CAS  Google Scholar 

  50. A.M. Monteiro da Silva, D.A. Oakley, H.N. Newman, F.S. Nohl, H.M. Lloyd, Psychosocial factors and adult onset rapidly progressive periodontitis. J. Clin. Periodontol. 23(8), 789–794 (1996)

    Article  CAS  Google Scholar 

  51. R. Mengel, M. Bacher, L. Flores-De-Jacoby, Interactions between stress, interleukin-1beta, interleukin-6 and cortisol in periodontally diseased patients. J. Clin. Periodontol. 29(11), 1012–1022 (2002)

    Article  CAS  Google Scholar 

  52. N.B. Tutuncu, T. Erbas, Factors associated with bone metabolism in acromegalic patients: hypogonadism and female gender. Exp. Clin. Endocrinol. Diabetes 112(6), 328–332 (2004). https://doi.org/10.1055/s-2004-820913

    Article  CAS  PubMed  Google Scholar 

  53. A. Cohen, D.W. Dempster, R. Muller, X.E. Guo, T.L. Nickolas, X.S. Liu, X.H. Zhang, A.J. Wirth, G.H. van Lenthe, T. Kohler, D.J. McMahon, H. Zhou, M.R. Rubin, J.P. Bilezikian, J.M. Lappe, R.R. Recker, E. Shane, Assessment of trabecular and cortical architecture and mechanical competence of bone by high-resolution peripheral computed tomography: comparison with transiliac bone biopsy. Osteoporos. Int. 21(2), 263–273 (2010). https://doi.org/10.1007/s00198-009-0945-7

    Article  CAS  PubMed  Google Scholar 

  54. F.F. Ozer, S. Dagdelen, T. Erbas, Relation of RANKL and OPG levels with bone resorption in patients with acromegaly and prolactinoma. Horm. Metab. Res. 50(7), 562–567 (2018). https://doi.org/10.1055/a-0630-1529

    Article  CAS  PubMed  Google Scholar 

  55. H. Hasturk, A. Kantarci, Activation and resolution of periodontal inflammation and its systemic impact. Periodontol. 2000 69(1), 255–273 (2015). https://doi.org/10.1111/prd.12105

    Article  PubMed  PubMed Central  Google Scholar 

  56. R. Pivonello, R.S. Auriemma, L.F. Grasso, C. Pivonello, C. Simeoli, R. Patalano, M. Galdiero, A. Colao, Complications of acromegaly: cardiovascular, respiratory and metabolic comorbidities. Pituitary 20(1), 46–62 (2017). https://doi.org/10.1007/s11102-017-0797-7

    Article  PubMed  Google Scholar 

  57. M. Mercado, B. Gonzalez, G. Vargas, C. Ramirez, A.L. de los Monteros, E. Sosa, P. Jervis, P. Roldan, V. Mendoza, B. Lopez-Felix, G. Guinto, Successful mortality reduction and control of comorbidities in patients with acromegaly followed at a highly specialized multidisciplinary clinic. J. Clin. Endocrinol. Metab. 99(12), 4438–4446 (2014). https://doi.org/10.1210/jc.2014-2670

    Article  CAS  PubMed  Google Scholar 

  58. K.J. Joshipura, F.J. Munoz-Torres, B.A. Dye, B.G. Leroux, M. Ramirez-Vick, C.M. Perez, Longitudinal association between periodontitis and development of diabetes. Diabetes Res. Clin. Pr. 141, 284–293 (2018). https://doi.org/10.1016/j.diabres.2018.04.028

    Article  Google Scholar 

  59. D.M. Shearer, W.M. Thomson, J.M. Broadbent, J. Mann, R. Poulton, Periodontitis is not associated with metabolic risk during the fourth decade of life. J. Clin. Periodontol. 44(1), 22–30 (2017). https://doi.org/10.1111/jcpe.12641

    Article  CAS  PubMed  Google Scholar 

  60. T. Kocher, J. Konig, W.S. Borgnakke, C. Pink, P. Meisel, Periodontal complications of hyperglycemia/diabetes mellitus: epidemiologic complexity and clinical challenge. Periodontol. 2000 78(1), 59–97 (2018). https://doi.org/10.1111/prd.12235

    Article  PubMed  Google Scholar 

  61. M. Bondanelli, M.R. Ambrosio, E.C. degli Uberti, Pathogenesis and prevalence of hypertension in acromegaly. Pituitary 4(4), 239–249 (2001)

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors express their gratitude to Cigdem Gungor from Medeniyet University for the statistical analyses and Cagman Tan for his efforts in biochemical analysis of gingival crevicular fluid samples.

Funding

The study was funded by Hacettepe University Scientific Research Committee (grant number: THD-2015-7584).

Author information

Authors and Affiliations

  1. Hacettepe University Faculty of Dentistry, Periodontology Department, Ankara, Turkey

    Yesim Ozdemir, H. Gencay Keceli & Rahime M. Nohutcu

  2. Hacettepe University Medical School, Department of Endocrinology and Metabolism, Ankara, Turkey

    Nafiye Helvaci & Tomris Erbas

Authors
  1. Yesim Ozdemir
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. H. Gencay Keceli
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Nafiye Helvaci
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Tomris Erbas
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Rahime M. Nohutcu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to H. Gencay Keceli.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional research committee (Hacettepe University Local Ethics Committee, date: Mar 04, 2015; no: GO15/173-08) and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Informed consent

Informed consent was obtained from all individual participants included in the study.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ozdemir, Y., Keceli, H.G., Helvaci, N. et al. The tendency of reduced periodontal destruction in acromegalic patients showing similar inflammatory status with periodontitis patients. Endocrine 66, 622–633 (2019). https://doi.org/10.1007/s12020-019-02060-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12020-019-02060-2

Keywords

Search

Navigation