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Evaluation of bone texture imaging parameters on panoramic radiographs of patients with Sheehan’s syndrome: a STROBE-compliant case-control study

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Abstract

Summary

Sheehan’s syndrome (SHS) is a rare condition related to the risk of osteoporosis and evaluation of bone texture imaging features on panoramic radiographs would be suitable for this condition, which was the aim of the present study. Fractal dimension, lacunarity, and trabecular morphologic aspects were significantly altered in these patients.

Introduction

SHS is an important public health problem particularly in developing countries. It is characterized as postpartum hypopituitarism secondary to obstetric complications-related ischemic pituitary necrosis that shows significant systemic metabolic repercussions. Thus, this study aimed to evaluate bone texture parameters in digital panoramic radiographs of patients with SHS.

Methods

A case-control study was conducted with 30 SHS patients from an Endocrinology and Diabetology Service of reference in Brazil, and 30 age- and sex-matched healthy controls. A custom computer program measured fractal dimension, lacunarity, and some morphologic features in the following mandibular regions of interest (50 × 50 pixels): below the mental foramen (F1), between the first and second molars (M1), and at the center of the mandibular ramus (R1).

Results

The fractal analysis showed a statistically significant difference between the studied groups in all regions of interest. The fractal dimension in F1 (p = 0.016), M1 (p = 0.043), and R1 (p = 0.028) was significantly lower in SHS group, as well as lacunarity in R1 (p = 0.008). Additionally, several morphologic features were statistically significant in the SHS group (p < 0.05).

Conclusion

Therefore, individuals with SHS showed altered imaging texture parameters on panoramic radiographs, which reflect a smaller spatial organization of the bone trabeculae and, possibly, a state of reduced mineral bone density.

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References

  1. Imam A, Iqbal J, Blair HC, Davies TF, Huang CL, Zallone A, Zaidi M, Sun L (2009) Role of the pituitary-bone axis in skeletal pathophysiology. Curr Opin Endocrinol Diabetes Obes 16:423–429

    Article  CAS  PubMed  Google Scholar 

  2. Colaianni G, Cuscito C, Colucci S (2013) FSH and TSH in the regulation of bone mass: the pituitary/immune/bone axis. Clin Dev Immunol 2013:382698

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Zaidi M, Sun L, Liu P, Davies TF, New M, Zallone A, Yuen T (2016) Pituitary-bone connection in skeletal regulation. Horm Mol Biol Clin Investig 28:85–94

    CAS  PubMed  Google Scholar 

  4. Sheehan HL (1937) Postpartum necrosis of the anterior pituitary. J Pathol Bacteriol 45:189–214

    Article  CAS  Google Scholar 

  5. Gokalp D, Tuzcu A, Bahceci M, Arikan S, Ozmen CA, Cil T (2009) Sheehan’s syndrome and its impact on bone mineral density. Gynecol Endocrinol 25:344–349

    Article  CAS  PubMed  Google Scholar 

  6. Karaca Z, Laway BA, Dokmetas HS, Atmaca H, Kelestimur F (2016) Sheehan syndrome. Nat Rev Dis Primers 22:16092

    Article  Google Scholar 

  7. Haddock L, Vega LA, Aguiló F, Rodríguez O (1972) Adrenocortical, thyroidal and human growth hormone reserve in Sheehan’s syndrome. Johns Hopkins Med J 131:80–99

    CAS  PubMed  Google Scholar 

  8. Keleştimur F (2003) Sheehan's syndrome. Pituitary 6:181–188

    Article  PubMed  Google Scholar 

  9. Bolanowski M, Halupczok J, Jawiarczyk-Przybyłowska A (2015) Pituitary disorders and osteoporosis. Int J Endocrinol 2015:206853

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Sert M, Tetiker T, Kirim S, Kocak M (2003) Clinical report of 28 patients with Sheehan's syndrome. Endocr J 50:297–301

    Article  PubMed  Google Scholar 

  11. Dökmetaş HS, Kilicli F, Korkmaz S. Yonem O (2006) Characteristic features of 20 patients with Sheehan's syndrome. Gynecol Endocrinol 22:279–283

  12. Diri H, Tanriverdi F, Karaca Z, Senol S, Unluhizarci K, Durak AC, Atmaca H, Kelestimur F (2014) Extensive investigation of 114 patients with Sheehan’s syndrome: a continuing disorder. Eur J Endocrinol 171:311–318

    Article  CAS  PubMed  Google Scholar 

  13. Agarwal P, Gomez R, Bhatia E, Yadav S (2019) Decreased bone mineral density in women with Sheehan’s syndrome and improvement following oestrogen replacement and nutritional supplementation. J Bone Miner Metab 37:171–178

    Article  CAS  PubMed  Google Scholar 

  14. Shevroja E, Lamy O, Kohlmeier L, Koromani F, Rivadeneira F, Hans D (2017) Use of trabecular bone score (TBS) as a complementary approach to dual-energy X-ray absorptiometry (DXA) for fracture risk assessment in clinical practice. J Clin Densitom 20:334–345

    Article  PubMed  Google Scholar 

  15. Arsan B, Köse TE, Çene E, Özcan İ (2017) Assessment of the trabecular structure of mandibular condyles in patients with temporomandibular disorders using fractal analysis. Oral Surg Oral Med Oral Pathol Oral Radiol 123:382–391

    Article  PubMed  Google Scholar 

  16. Servais JA, Gaalaas L, Lunos S, Beiraghi S, Larson BE, Leon-Salazar V (2018) Alternative cone-beam computed tomography method for the analysis of bone density around impacted maxillary canines. Am J Orthod Dentofac Orthop 154:442–449

    Article  Google Scholar 

  17. Alman AC, Johnson LR, Calverley DC, Grunwald GK, Lezotte DC, Hokanson JE (2012) Diagnostic capabilities of fractal dimension and mandibular cortical width to identify men and women with decreased bone mineral density. Osteoporos Int 23:1631–1636

    Article  CAS  PubMed  Google Scholar 

  18. Yasar F, Akgünlü F (2005) Fractal dimension and lacunarity analysis of dental radiographs. Dentomaxillofac Radiol 34:261–267

    Article  CAS  PubMed  Google Scholar 

  19. Gumussoy I, Miloglu O, Cankaya E, Bayrakdar IS (2016) Fractal properties of the trabecular pattern of the mandible in chronic renal failure. Dentomaxillofac Radiol 45:20150389

    Article  PubMed  PubMed Central  Google Scholar 

  20. Apolinário AC, Sindeaux R, de Souza Figueiredo PT, Guimarães AT, Acevedo AC, Castro LC, de Paula AP, de Paula LM, de Melo NS, Leite AF (2016) Dental panoramic indices and fractal dimension measurements in osteogenesis imperfecta children under pamidronate treatment. Dentomaxillofac Radiol 45:20150400

    Article  PubMed  PubMed Central  Google Scholar 

  21. Shrout MK, Potter BJ, Hildebolt CF (1997) The effect of image variations on fractal dimension calculations. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 84:96–100

    Article  CAS  PubMed  Google Scholar 

  22. Sindeaux R, Figueiredo PT, de Melo NS, Guimarães AT, Lazarte L, Pereira FB, de Paula AP, Leite AF (2014) Fractal dimension and mandibular cortical width in normal and osteoporotic men and women. Maturitas 77:142–148

    Article  PubMed  Google Scholar 

  23. Hwang JJ, Lee JH, Han SS, Kim YH, Jeong HG, Choi YJ, Park W (2017) Strut analysis for osteoporosis detection model using dental panoramic radiography. Dentomaxillofac Radiol 46:20170006

    Article  PubMed  PubMed Central  Google Scholar 

  24. Ergün S, Saraçoglu A, Güneri P, Ozpinar B (2009) Application of fractal analysis in hyperparathyroidism. Dentomaxillofac Radiol 38:281–288

    Article  PubMed  Google Scholar 

  25. Demirbaş AK, Ergün S, Güneri P, Aktener BO, Boyacioğlu H (2008) Mandibular bone changes in sickle cell anemia: fractal analysis. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 106:e41–e48

    Article  PubMed  Google Scholar 

  26. Kurşun-Çakmak EŞ, Bayrak S (2018) Comparison of fractal dimension analysis and panoramic-based radiomorphometric indices in the assessment of mandibular bone changes in patients with type 1 and type 2 diabetes mellitus. Oral Surg Oral Med Oral Pathol Oral Radiol 126:184–191

    Article  PubMed  Google Scholar 

  27. Rondon RH, Pereira YC, do Nascimento GC (2014) Common positioning errors in panoramic radiography: a review. Imaging Sci Dent 44:1–6

  28. White SC, Rudolph DJ (1999) Alterations of the trabecular pattern of the jaws in patients with osteoporosis. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 88:628–635

    Article  CAS  PubMed  Google Scholar 

  29. Bradley D, Roth G (2007) Adaptative thresholding using the integral image. Journal of Graphics Tools 12:13–21

    Article  Google Scholar 

  30. Hammer GP, du Prel JB, Blettner M (2009) Avoiding bias in observational studies: part 8 in a series of articles on evaluation of scientific publications. Dtsch Arztebl Int 106:664–668

    PubMed  PubMed Central  Google Scholar 

  31. Yasar F, Apaydin B, Yilmaz HH (2012) The effects of image compression on quantitative measurements of digital panoramic radiographs. Med Oral Patol Oral Cir Bucal 17:1074–1081

    Article  Google Scholar 

  32. Kovacs K (2003) Sheehan syndrome. Lancet 361:520–522

    Article  PubMed  Google Scholar 

  33. Harris EF, Smith RN (2009) Accounting for measurement error: a critical but often overlooked process. Arch Oral Biol 54:S107–S117

    Article  PubMed  Google Scholar 

  34. Glüer CC, Blake G, Lu Y, Blunt BA, Jergas M, Genant HK (1195) Accurate assessment of precision errors: how to measure the reproducibility of bone densitometry techniques. Osteoporos Int 5:262–270

  35. Chihaoui M, Yazidi M, Chaker F, Belouidhnine M, Kanoun F, Lamine F, Ftouhi B, Sahli H, Slimane H (2016) Bone mineral density in Sheehan's syndrome; prevalence of low bone mass and associated factors. J Clin Densitom 19:413–418

    Article  PubMed  Google Scholar 

  36. Acibucu F, Kilicli F, Dokmetas HS (2014) Assessment of bone mineral density in patients with Sheehan’s syndrome. Gynecol Endocrinol 30:532–535

    Article  CAS  PubMed  Google Scholar 

  37. Lespessailles E, Gadois C, Lemineur G, Do-Huu JP, Benhamou L (2007) Bone texture analysis on direct digital radiographic images: precision study and relationship with bone mineral density at the os calcis. Calcif Tissue Int 80:97–102

    Article  CAS  PubMed  Google Scholar 

  38. Pothuaud L, Lespessailles E, Harba R, Jennane R, Royant V, Eynard E, Benhamou CL (1998) Fractal analysis of trabecular bone texture on radiographs: discriminant value in postmenopausal osteoporosis. Osteoporos Int 8:618–625

    Article  CAS  PubMed  Google Scholar 

  39. Liang Z, Feng Z, Guangxiang X (2012) Comparison of fractal dimension calculation methods for channel bed profiles. Procedia Eng 28:252–257

    Article  Google Scholar 

  40. Updike SX, Nowzari H (2008) Fractal analysis of dental radiographs to detect periodontitis-induced trabecular changes. J Periodontal Res 43:658–664

    Article  PubMed  Google Scholar 

  41. Lee BD, White SC (2005) Age and trabecular features of alveolar bone associated with osteoporosis. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 100:92–98

    Article  PubMed  Google Scholar 

  42. Licks R, Licks V, Ourique F, Radke Bittencourt H, Fontanella V (2010) Development of a prediction tool for low bone mass based on clinical data and periapical radiography. Dentomaxillofac Radiol 39:224–230

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Ramiandrasoa C, Castinetti F, Raingeard I, Fenichel P, Chabre O, Brue T, Courbière B (2013) Delayed diagnosis of Sheehan's syndrome in a developed country: a retrospective cohort study. Eur J Endocrinol 169:431–438

    Article  CAS  PubMed  Google Scholar 

  44. Stochholm K, Gravholt CH, Laursen T, Laurberg P, Andersen M, Kristensen LØ, Feldt-Rasmussen U, Christiansen JS, Frydenberg M, Green A (2007) Mortality and GH deficiency: a nationwide study. Eur J Endocrinol 157:9–18

    Article  CAS  PubMed  Google Scholar 

  45. Zargar AH, Singh B, Laway BA, Masoodi SR, Wani AI, Bashir MI (2005) Epidemiologic aspects of postpartum pituitary hypofunction (Sheehan’s syndrome). Fertil Steril 84:523–528

    Article  PubMed  Google Scholar 

  46. Shatrugna V, Kulkarni B, Kumar PA, Rani KU, Balakrishna N (2005) Bone status of Indian women from a low-income group and its relationship to the nutritional status. Osteoporos Int 16:1827–1835

    Article  PubMed  Google Scholar 

  47. Cavalcante DD, Pinto-Quidute AR, Alves-Martins MR, Walter-de-Aguiar AS, Lima-Cid AM, Silva PG, Cavalcante RF, Costa FW (2018) Dental status, salivary flow, and sociodemographic aspects in Sheehan Syndrome patients. Med Oral Patol Oral Cir Bucal 23:e436–e442

    PubMed  PubMed Central  Google Scholar 

  48. Lewiecki EM, Binkley N, Morgan SL, Shuhart CR, Camargos BM, Carey JJ, Gordon CM, Jankowski LG, Lee JK, Leslie WD; International Society for Clinical Densitometry (2016) Best practices for dual-energy X-ray absorptiometry measurement and reporting: International Society for Clinical Densitometry Guidance. J Clin Densitom 2016 19:127–140

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Funding

This study was supported by the Institutional Program for Scientific Initiation Scholarships – National Council for Scientific and Technological Development (PIBIC-CNPq), Brazil.

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Authors and Affiliations

  1. Department of Clinical Dentistry, Postgraduate Program in Dentistry, Federal University of Ceará, Alexandre Baraúna St 949, Rodolfo Teofilo, Fortaleza, Ceará, 60430-160, Brazil

    D. de Sá Cavalcante, A.M.P.L. Cid, P.G. de Barros Silva, T.R. Ribeiro & F.W.G. Costa

  2. Realistic Simulation Center, Univeristy Center UNICHRISTUS, R. João Adolfo Gurgel St 133, Cocó, Fortaleza, Ceará, 60190-060, Brazil

    M.G. da Silva Castro

  3. Division of Endocrinology and Diabetology, Walter Cantídio University Hospital, Alexandre Baraúna St 949, Rodolfo Teofilo, Fortaleza, Ceará, 60430-160, Brazil

    A.R.P. Quidute & M.R.A. Martins

  4. Department of Anatomy and Cell Biology, Indiana School of Medicine, 635 Barnhill Dr, Indianapolis, IN, 46202, USA

    J. Cadwell Williams Jr

  5. Division of Oral Radiology, School of Dentistry, Federal University of Bahia, Araújo Pinho ave 62, Canela, Salvador, Bahia, 40110-040, Brazil

    F.S. Neves

Authors
  1. D. de Sá Cavalcante
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  2. M.G. da Silva Castro
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  3. A.R.P. Quidute
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  4. M.R.A. Martins
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  5. A.M.P.L. Cid
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  6. P.G. de Barros Silva
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  7. J. Cadwell Williams Jr
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  8. F.S. Neves
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  9. T.R. Ribeiro
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  10. F.W.G. Costa
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Corresponding author

Correspondence to F.W.G. Costa.

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This study was approved by the Ethics Committee of the Federal University of Ceará (research protocol # 983 022).

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de Sá Cavalcante, D., da Silva Castro, M., Quidute, A. et al. Evaluation of bone texture imaging parameters on panoramic radiographs of patients with Sheehan’s syndrome: a STROBE-compliant case-control study. Osteoporos Int 30, 2257–2269 (2019). https://doi.org/10.1007/s00198-019-05086-4

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