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VOLUME 9 , ISSUE 4 ( July-August, 2018 ) > List of Articles

ORIGINAL RESEARCH

Differential Expression of Toll-like Receptor 4 and Nuclear Factor κB of Primary Rat Oral Keratinocytes in Response to Stimulation with Fusobacterium nucleatum

Ali A Abdulkareem, Hayder R Abdulbaqi, Ahmed K Nayyef, Saif S Saliem

Keywords : Fusobacterium nucleatum, Gingival epithelium, Nuclear factor êB, Toll-like receptor 4

Citation Information : Abdulkareem AA, Abdulbaqi HR, Nayyef AK, Saliem SS. Differential Expression of Toll-like Receptor 4 and Nuclear Factor κB of Primary Rat Oral Keratinocytes in Response to Stimulation with Fusobacterium nucleatum. World J Dent 2018; 9 (4):270-274.

DOI: 10.5005/jp-journals-10015-1547

License: CC BY-SA 4.0

Published Online: 01-06-2009

Copyright Statement:  Copyright © 2018; The Author(s).


Abstract

Aim: Gram-negative anaerobic periodontal pathogens are well known for their ability to stimulate innate immune response once being recognized by special receptors of epithelial pocket lining. The aim of this study was to investigate the expression of toll-like receptor 4 (TLR4) and nuclear factor kappa-lightchain-enhancer of activated B cells (NF-êB) following exposure to Fusobacterium nucleatum. Materials and methods: Primary oral keratinocytes were collected from gingiva of Wistar Han rat and cultured to confluency. Then, the epithelial cells were stimulated with heat-killed F. nucleatum and 20 μg/mL Escherichia coli lipopolysaccharide (E. coli LPS). Expression of NF-êB was assayed by immunocytochemistry in addition to semi-quantitative reverse transcriptase (RT)-polymerase chain reaction (PCR), which was also used to determine transcription of TLR4 in comparison with unstimulated control. Results: Immunocytochemical analysis indicated that nuclear translocation of NF-êB was significantly increased (p < 0.05) in cultures stimulated with bacteria as compared with control. In addition, the expression of TLR4 and NF-êB in stimulated keratinocytes was also significantly increased (p < 0.05) 3- and 2.5-fold respectively, in comparison with unstimulated cultures. Conclusion: Fusobacterium nucleatum potentially triggers NF-êB signaling pathway through activation of TLR4 in oral epithelial cells. Clinical significance: Recognition of early immune response against pathogenic periodontal bacteria would highlight new aspects in pathogenesis of periodontal diseases that could provide potential therapeutic opportunity for these conditions.


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  1. Armitage GC, Robertson PB. The biology, prevention, diagnosis and treatment of periodontal diseases: scientific advances in the United States. J Am Dent Assoc 2009 Sep;140(Suppl 1): 36S-43S.
  2. Socransky SS, Haffajee AD, Cugini MA, Smith C, Kent RL Jr. Microbial complexes in subgingival plaque. J Clin Periodontol 1998 Feb;25(2):134-144.
  3. Kornman KS, Page RC, Tonetti MS. The host response to the microbial challenge in periodontitis: assembling the players. Periodontol 2000 1997 Jun;14(1):33-53.
  4. Liotta LA, Tryggvason K, Garbisa S, Hart I, Foltz CM, Shafie S. Metastatic potential correlates with enzymatic degradation of basement membrane collagen. Nature 1980 Mar;284(5751): 67-68.
  5. Janeway CAJr. Approaching the asymptote? Evolution and revolution in immunology. Cold Spring Harb Symp Quant Biol 1989;54(Pt 1):1-13.
  6. Mahla RS, Reddy CM, Prasad D, Kumar H. Sweeten PAMPs: role of sugar complexed PAMPs in innate immunity and vaccine biology. Front Immunol 2013 Sep;4:248.
  7. Poltorak A, He X, Smirnova I, Liu M-Y, Van Huffel C, Du X, Birdwell D, Alejos E, Silva M, Galanos C, et al. Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science 1998 Dec;282(5396):2085-2088.
  8. Ilango P, Mahalingam A, Parthasarathy H, Katamreddy V, Subbareddy V. Evaluation of TLR2 and 4 in chronic periodontitis. J Clin Diagn Res 2016 Jun;10(6):ZC86-ZC89.
  9. Kawai T, Akira S. Signaling to NF-kB by Toll-like receptors. Trends Mol Med 2007 Nov;13(11):460-469.
  10. Kuper C, Beck FX, Neuhofer W. Toll-like receptor 4 activates NF-ƒÈB and MAP kinase pathways to regulate expression of proinflammatory COX-2 in renal medullary collecting duct cells. Am J Physiol Renal Physiol 2012 Jan;302(1):F38-F46.
  11. Sun Y, Shu R, Zhang M-Z, Wu AP. Toll-like receptor 4 signaling plays a role in triggering periodontal infection. FEMS Immunol Med Microbiol 2008 Apr;52(3):362-369.
  12. Arabaci T, Cicek Y, Canakci V, Canakci CF, Ozgoz M, Albayrak M, Keles ON. Immunohistochemical and stereologic analysis of NF-ƒÈB activation in chronic periodontitis. Eur J Dent 2010 Oct;4(4):454-461.
  13. Milward MR, Chapple IL, Wright HJ, Millard JL, Matthews JB, Cooper PR. Differential activation of NF-ƒÈB and gene expression in oral epithelial cells by periodontal pathogens. Clin Exp Immunol 2007 May;148(2):307-324.
  14. Zhang G, Chen R, Rudney JD. Streptococcus cristatus modulates the Fusobacterium nucleatum-induced epithelial interleukin-8 response through the nuclear factor-kappa B pathway. J Periodontal Res 2011 Oct;46(5):558-567.
  15. Roberts A, Matthews JB, Socransky SS, Freestone PP, Williams PH, Chapple IL. Stress and the periodontal diseases: effects of catecholamines on the growth of periodontal bacteria in vitro. Oral Microbiol Immunol 2002 Oct;17(5): 296-303.
  16. Kedjarune U, Pongprerachok S, Arpornmaeklong P, Ungkusonmongkhon K. Culturing primary human gingival epithelial cells: comparison of two isolation techniques. J Craniomaxillofac Surg 2001 Aug;29(4):224-231.
  17. Dierickx K, Pauwels M, Van Eldere J, Cassiman JJ, Van Steenberghe D, Quirynen M. Viability of cultured periodontal pocket epithelium cells and Porphyromonas gingivalis association. J Clin Periodontol 2002 Nov;29(11):987-996.
  18. Medzhitov R, Janeway CJ. Innate immunity. N Engl J Med 2000 Aug;343(5):338-344.
  19. Lu YC, Yeh WC, Ohashi PS. LPS/TLR4 signal transduction pathway. Cytokine 2008 May;42(2):145-151.
  20. Steimle A, Autenrieth IB, Frick JS. Structure and function: lipid A modifications in commensals and pathogens. Int J Med Microbiol 2016 Aug;306(5):290-301.
  21. Sen R, Baltimore D. Multiple nuclear factors interact with the immunoglobulin enhancer sequences. Cell 1986 Aug;46(5):705-716.
  22. Signat B, Roques C, Poulet P, Duffaut D. Fusobacterium nucleatum in periodontal health and disease. Curr Issues Mol Biol 2011 Jan;13(2):25-36.
  23. Yin L, Dale BA. Activation of protective responses in oral epithelial cells by Fusobacterium nucleatum and human ƒÀ-defensin-2. J Med Microbiol 2007 Jul;56(Pt 7):976-987.
  24. Rakoff-Nahoum S, Medzhitov R. Toll-like receptors and cancer. Nat Rev Cancer 2008 Jan;9(1):57-63.
  25. Gonzalez OA, Li M, Ebersole JL, Huang CB. HIV-1 reactivation induced by the periodontal pathogens fusobacterium nucleatum and porphyromonas gingivalis involves toll-like receptor 4 and 9 activation in monocytes/macrophages. Clin Vaccine Immunol 2010 Sep;17(9):1417-1427.
  26. Liu H, Redline RW, Han YW. Fusobacterium nucleatum Induces fetal death in mice via stimulation of TLR4-mediated placental inflammatory response. J Immunol 2007 Aug;179(4):2501-2508.
  27. Mizuno E, Sakuma H. Wadaiko performance enhances synchronized motion of mentally disabled persons. Percept Mot Skills 2013 Feb;116(1):187-196.
  28. Virji-Babul N, Moiseev A, Sun W, Feng T, Moiseeva N, Watt KJ, Huotilainen M. Neural correlates of music recognition in Down syndrome. Brain Cogn 2013 Mar;81(2):256-262.
  29. Zyada MM, El-Said Elewa M, El-Meadawy S, El Sharkawy H. Effectiveness of topical mucoadhesive gel containing propolis in management of patients with atrophic and erosive oral lichen planus: clinical and immunohistochemical study. Egypt Dent Assoc 2012;58:1-3.
  30. Kainz J, Braun H, Genser P. Haller's cells: morphologic evaluation and clinico-surgical relevance. Laryngorhinootologie 1993 Dec;72(12):599-604.
  31. Ahmad M, Khurana N, Jaberi J, Sampair C, Kuba RK. Prevalence of infraorbital ethmoid (Haller's) cells on panoramic radiographs. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2006 May;101(5):658-661.
  32. Khojastepour L, Mirhadi S, Mesbahi SA. Anatomical variations of ostiomeatal complex in CBCT of patients seeking rhinoplasty. J Dent 2015 Mar;16(1):42-48.
  33. Raina A, Guledgud MV, Patil K. Infraorbital ethmoid (Haller's) cells: a panoramic radiographic study. Dentomaxillofac Radiol 2012 May;41(4):305-308.
  34. Kamdi P, Nimma V, Gogri A. Role of CBCT in Haller cells identification and its clinical significance. Int J Curr Res 2017 Jun;9(06):52630-52635.
  35. Fadda G, Rosso S, Aversa S, Ondolo C, Succo G. Multiparametric statistical correlations between paranasal sinus anatomic variations and chronic rhinosinusitis. Acta Otorhinolaryngol Ital 2012 Aug;32(4):244-251.
  36. Khayam E, Mahabadi AM, Ezoddini F, Mohamad AG, Zeinab H, Malihe M, Razavi SH. The prevalence of ethmoidal infraorbital cells in panoramic radiography. Am J Res Commun 2013;1(2):109-118.
  37. Göçmen G, Borahan MO, Aktop S, Dumlu A, Pekiner FN, Göker K. Effect of septal deviation, concha bullosa and Haller's cell on maxillary sinus's inferior pneumatization: a retrospective study. Open Dent J 2015 Jul 31;9:282-286.
  38. Pekiner FN, Borahan MO, Dumlu A, Ozbayrak S. Infraorbital ethmoid (Haller) cells: a cone-beam computed tomographic study. Oral Radiol 2014;30(3):219-225.
  39. Sebrechts H, Vlaminck S, Casselman J. Orbital edema resulting from Haller cell pathology: 3 case reports and review of literature. Acta Otorhinolaryngol Belg 2000;54(1):39-43.
  40. Cook PR, Nishioka GJ, Davis WE, McKinsey JP. Functional endoscopic sinus surgery in patients with normal computed tomography scans. Otolaryngol Neck Surg 1994 Jun; 110(6):505-509.
  41. Choi JH. Hypoesthesia of midface by isolated Haller's cell mucocele. Braz J Otorhinolaryngol 2016 Jul 22. pii:S1808- 8694(16)30138-0.
  42. Salonen MA, Oikarinen K, Virtanen K, Pernu H. Failures in the osseointegration of endosseous implants. Int J Oral Maxillofac Implants 1993;8(1):92-97.
  43. Zhang X, Sun Z, Yang Q. Application of Denaturing gradient gel electrophoresis to the analysis of bacterial communities associated with asymptomatic and symptomatic pericoronitis. J Oral Maxillofac Surg 2018 Mar;76(3):483-489.
  44. Suárez-López Del Amo F, Yu SH, Wang HL. Non-surgical therapy for peri-implant diseases: a systematic review. J Oral Maxillofac Res 2016 Sep;7(3):e13.
  45. Aberg CH, Kelk P, Johansson A. Aggregatibacter actinomycetemcomitans: virulence of its leukotoxin and association with aggressive periodontitis. Virulence 2015 Apr;6(3):188-195.
  46. Larsen OI, Enersen M, Kristoffersen AK, Wennerberg A, Bunæs DF, Lie SA, Leknes KN. Antimicrobial effects of three different treatment modalities on dental implant surfaces. J Oral Implantol 2017 Dec;43(6):429-436.
  47. Prathapachandran J, Suresh N. Management of periimplantitis. Dent Res J (Isfahan) 2012 Sep-Oct;9(5):516-521.
  48. Bhattacharyya M, Kumar AN, Kapuria S. Synthesis and characterization of Al/SiC and Ni/Al2O3 functionally graded materials. Mater Sci Eng A 2008 Jul;487(1-2):524-535.
  49. Chenglin C, Jingchuan Z, Zhongda Y, Shidong W. Hydroxyapatite-Ti functionally graded biomaterial fabricated by powder metallurgy. Mater Sci Eng A 1999 Nov;271(1):95-100.
  50. Oleiwi JK, Anaee RA, Muhsin SA. Fabrication, characterization and physical properties of functionally graded Ti/HAP bioimplants. Wulfenia J 2015 Jul;22(7):336-348.
  51. Ogawa T, Watanabe Y, Sato H, Kim IS, Fukui Y. Theoretical study on fabrication of functionally graded material with density gradient by a centrifugal solid-particle method. Compos Part A Appl S 2006 Dec;37(12):2194-2200.
  52. Yang ZM, Tian F, Zhang LM. Theoretical study on two sedimentation processes used to form functionally graded materials. J Mater Sci Lett 2003 May;22(10):739-741.
  53. Yang ZM, Gong DR, Zhang LM. Design of co-sedimentation experiments used to fabricate functionally graded materials with a continuous change of composition. J Wuhan Univ Technol Mater Sci Ed 2004 Jan;19(2):11-13.
  54. Jin G, Takeuchi M, Honda S, Nishikawa T, Awaji H. Properties of multilayered mullite/Mo functionally graded materials fabricated by powder metallurgy processing. Mater Chem Physics 2005 Feb;89(2):238-243.
  55. Jamaludin SN, Basri S, Hussain A, Al-Othmany DS, Mustapha F, Nuruzzaman DM. Three-dimensional finite element modeling of thermomechanical problems in functionally graded hydroxyapatite/titanium plate. Math Probl Eng 2014 Apr;2014:371462.
  56. Halpern LR, Dodson TB. Does prophylactic administration of systemic antibiotics prevent postoperative inflammatory complications after third molar surgery? J Oral Maxillofac Surg 2007 Feb;65(2):177-185.
  57. Lopez-Cedrun JL, Pijoan JI, Fernandez S, Santamaria J, Hernandez G. Efficacy of amoxycillin treatment in preventing postoperative complications in patients undergoing third molar surgery: a prospective, randomized, double-blind controlled study. J Oral Maxillofac Surg 2011 Jun;69(6):e5-e14.
  58. Arteagoitia MI, Barbier L, Santamaria J, Santamaria G, Ramos E. Efficacy of amoxicillin and amoxicillin/clavulanic acid in the prevention of infection and dry socket after third molar extraction. A systematic review and meta-analysis. Med Oral Patol Oral Cir Bucal 2016 Jul;21(4):e494-e504.
  59. Piltz JR, Starita RJ. The use of subconjunctivally administered tissue plasminogen activator after trabeculectomy. Ophthalmic Surg 1994 Jan;25(1):51-53.
  60. Por YM, Tan YL, Mehta JS, Tan DT. Intracameral fibrin tissue sealant as an adjunct in tectonic lamellar keratoplasty for large corneal perforations. Cornea 2009 May;28(4):451-455.
  61. Sakarya Y, Sakarya R, Yildirim A. Sutureless amniotic membrane fixation with fibrin glue in symptomatic bullous keratopathy with poor visual potential. Eur J Ophthalmol 2010 Jan-Feb;20(1):249; author reply 249-250.
  62. Lee GA, Holcombe DJ. Surgical revision of dysfunctional filtration blebs with bleb preservation sliding conjunctival flap and fibrin glue. Eye (Lond) 2010 Jun;24(6):947-953.
  63. Kahook MY, Noecker RJ. Fibrin glue-assisted glaucoma drainage device surgery. Br J Ophthalmol 2006 Dec;90(12):1486-1489.
  64. Valimaki J. Fibrin glue for preventing immediate postoperative hypotony following glaucoma drainage implant surgery. Acta Ophthalmol Scand 2006 Jun;84(3):372-374.
  65. Malhotra C, Jain AK. Human amniotic membrane transplantation: different modalities of its use in ophthalmology. World J Transplant 2014 Jun;4(2):111-121.
  66. Dua HS, Gomes JA, King AJ, Maharajan VS. The amniotic membrane in ophthalmology. Surv Ophthalmol 2004 Jan-Feb;49(1):51-77.
  67. Shimmura S, Shimazaki J, Ohashi Y, Tsubota K. Antiinflammatory effects of amniotic membrane transplantation in ocular surface disorders. Cornea 2001 May;20(4):408-413.
  68. Yazdani S, Mahboobipour H, Pakravan M, Doozandeh A, Ghahari E. Adjunctive mitomycin c or amniotic membrane transplantation for Ahmed glaucoma valve implantation: a randomized clinical trial. J Glaucoma 2016 May;25(5):415-421.
  69. Sheha H, Kheirkhah A, Taha H. Amniotic membrane transplantation in trabeculectomy with mitomycin C for refractory glaucoma. J Glaucoma 2008 Jun-Jul;17(4):303-307.
  70. Khairy HA, Elsawy MF. Trabeculectomy with mitomycin-C versus trabeculectomy with amniotic membrane transplant: a medium-term randomized controlled trial. J Glaucoma 2015 Sep;24(7):556-559.
  71. Rauscher FM, Barton K, Budenz DL, Feuer WJ, Tseng SC. Long-term outcomes of amniotic membrane transplantation for repair of leaking glaucoma filtering blebs. Am J Ophthalmol 2007 Jun;143(6):1052-1054.
  72. Sethi P, Patel RN, Goldhardt R, Ayyala RS. Conjunctival advancement with subconjunctival amniotic membrane draping technique for leaking cystic blebs. J Glaucoma 2016 Feb;25(2):188-192.
  73. Kitagawa K, Yanagisawa S, Watanabe K, Yunoki T, Hayashi A, Okabe M, Nikaido T. A hyperdry amniotic membrane patch using a tissue adhesive for corneal perforations and bleb leaks. Am J Ophthalmol 2009 Sep;148(3):383-389.
  74. Nagai-Kusuhara A, Nakamura M, Fujioka M, Negi A. Longterm results of amniotic membrane transplantation-assisted bleb revision for leaking blebs. Graefes Arch Clin Exp Ophthalmol 2008 Apr;246(4):567-571.
  75. Rai P, Lauande-Pimentel R, Barton K. Amniotic membrane as an adjunct to donor sclera in the repair of exposed glaucoma drainage devices. Am J Ophthalmol 2005 Dec;140(6): 1148-1152.
  76. Ainsworth G, Rotchford A, Dua HS, King AJ. A novel use of amniotic membrane in the management of tube exposure following glaucoma tube shunt surgery. Br J Ophthalmol 2006 Apr;90(4):417-419.
  77. Papadaki TG, Siganos CS, Zacharopoulos IP, Panteleontidis V, Charissis SK. Human amniotic membrane transplantation for tube exposure after glaucoma drainage device implantation. J Glaucoma 2007 Jan;16(1):171-172.
  78. Mulder EJ, Leiblum DM, Visser GH. Fetal breathing movements in late diabetic pregnancy: relationship to fetal heart rate patterns and Braxton Hicks’ contractions. Early Hum Dev 1995 Nov;43(3):225-232.
  79. Schulte FJ, Michaelis R, Nolte R, Albert G, Parl U, Lasson U. Brain and behavioral maturation in newborn infants of diabetic mothers. I. Nerve conduction and EEG patterns. Neuropadiatrie 1969 Jan-Jul;1(1):24-35.
  80. Devoe LD, Youssef AA, Castillo RA, Croom CS. Fetal biophysical activities in third-trimester pregnancies complicated by diabetes mellitus. Am J Obstet Gynecol 1994 Aug;171(2):298-303.
  81. Dierker LJ Jr, Pillay S, Sorokin Y, Rosen MG. The change in fetal activity periods in diabetic and nondiabetic pregnancies. Am J Obstet Gynecol 1982 May;143(2):181-185.
  82. Doherty NN, Hepper PG. Habituation in fetuses of diabetic mothers. Early Hum Dev 2000 Aug;59(2):85-93.
  83. Kainer F, Prechtl HF, Engele H, Einspieler C. Assessment of the quality of general movements in fetuses and infants of women with type-1 diabetes mellitus. Early Hum Dev 1997 Nov;50(1):13-25.
  84. Mulder EJ, O'Brien MJ, Lems YL, Visser GH, Prechtl HF. Body and breathing movements in near-term fetuses and newborn infants of type-1 diabetic women. Early Hum Dev 1990 Nov;24(2):131-152.
  85. Mulder EJ, Visser GH. Growth and motor development in fetuses of women with type-1 diabetes. I. Early growth patterns. Early Hum Dev 1991 May;25(2):91-106.
  86. Mulder EJ, Visser GH. Growth and motor development in fetuses of women with type-1 diabetes. II. Emergence of specific movement patterns. Early Hum Dev 1991 May;25(2):107-115.
  87. Mulder EJ, Visser GH. Impact of early growth delay on subsequent fetal growth and functional development: a study on diabetic pregnancy. Early Hum Dev 1992 Dec;31(2):91-95.
  88. Mulder EJ, Visser GH, Bekedam DJ, Prechtl HF. Emergence of behavioral states in fetuses of type-1 diabetic women. Early Hum Dev 1987 Jul;15(4):231-251.
  89. Mulder EJ, Visser GH, Morssink LP, de Vries JI. Growth and motor development in fetuses of women with type-1 diabetes. III. First trimester quantity of fetal movement patterns. Early Hum Dev 1991 May;25(2):117-133.
  90. Aberg A, Westbom L, Kallen B. Congenital malformations among infants whose mothers had gestational diabetes or preexisting diabetes. Early Hum Dev 2001 Mar;61(2):85-95.
  91. Deregnier RA, Nelson CA, Thomas KM, Wewerka S, Georgieff MK. Neurophysiologic evaluation of auditory recognition memory in healthy newborn infants and infants of diabetic mothers. J Pediatr 2000 Dec;137(6):777-784.
  92. Nelson CA, Wewerka S, Thomas KM, Tribby-Walbridge S, deRegnier R, Georgieff M. Neurocognitive sequelae of infants of diabetic mothers. Behav Neurosci 2000 Oct;114(5):950-956.
  93. Reece EA, Homko CJ. Infant of the diabetic mother. Semin Perinatol 1994 Oct;18(5):459-469.
  94. Reece EA, Homko CJ. Why do diabetic women deliver malformed infants? Clin Obstet Gynecol 2000 Mar;43(1):32-45.
  95. Rizzo T, Metzger BE, Burns WJ, Burns K. Correlations between antepartum maternal metabolism and intelligence of offspring. N Engl J Med 1991 Sep;325(13):911-916.
  96. Rizzo TA, Metzger BE, Dooley SL, Cho NH. Early malnutrition and child neurobehavioral development: insights from the study of children of diabetic mothers. Child Dev 1997 Feb;68(1):26-38.
  97. Schwartz R, Teramo KA. Effects of diabetic pregnancy on the fetus and newborn. Semin Perinatol 2000 Apr;24(2):120-135.
  98. Vaarasmaki MS, Hartikainen A, Anttila M, Pramila S, Koivisto M. Factors predicting peri- and neonatal outcome in diabetic pregnancy. Early Hum Dev 2000 Jul;59(1):61-70.
  99. Robertson SS, Dierker LJ. Fetal cyclic motor activity in diabetic pregnancies: sensitivity to maternal blood glucose. Dev Psychobiol 2003 Jan;42(1):9-16.
  100. Accardo PJ, Blondis TA, Whitman BY. Disorders of attention and activity level in a referral population. Pediatrics 1990 Mar;85(3 Pt 2):426-431.
  101. Ornoy A, Uriel L, Tennenbaum A. Inattention, hyperactivity and speech delay at 2-4 years of age as a predictor for ADDADHD syndrome. Isr J Psychiatry Relat Sci 1993;30(3):155-163.
  102. Smyth TR. Impaired motor skill (clumsiness) in otherwise normal children: a review. Child Care Health Dev 1992 Sep-Oct;18(5):283-300.
  103. Petersen MB, Pedersen SA, Greisen G, Pedersen JF, Mølsted- Pedersen L. Early growth delay in diabetic pregnancy: relation to psychomotor development at age 4. Br Med J (Clin Res Ed) 1988 Feb;296(6622):598-600.
  104. Sells CJ, Robinson NM, Brown Z, Knopp RH. Long-term developmental follow-up of infants of diabetic mothers. J Pediatr 1994 Jul;125(1):S9-S17.
  105. Vladareanu R, Lebit D, Constantinescu S. Ultrasound assessment of fetal neurobehaviour in high risk pregnancies. DSJUOG 2012 Apr-Jun;6(2):132-147.
  106. Talic A, Kurjak A, Ahmed B, Stanojevic M, Predojevic M, Kadic AS, Di Renzo GC. The potential of 4D sonography in the assessment of fetal behavior in high-risk pregnancies. J Matern Fetal Neonatal Med 2011 Jul;24(7):948-954.
  107. Bekedam DJ, Visser GH, de Vries JJ, Prechtl HF. Motor behaviour in the growth retarded fetus. Early Hum Dev 1985 Nov;12(2):155-165.
  108. Cioni G, Prechtl HF. Preterm and early postterm motor behaviour in low-risk premature infants. Early Hum Dev 1990 Sep;23(3):159-191.
  109. Seme-Ciglenecki P. Predictive value of assessment of general movements for neurological development of highrisk preterm infants: comparative study. Croat Med J 2003 Dec;44(6):721-727.
  110. Abo-Yaqoub S, Kurjak A, Mohammed AB, Shadad A, Abdel-Maaboud M. The role of 4-D ultrasonography in prenatal assessment of fetal neurobehaviour and prediction of neurological outcome. J Matern Fetal Neonatal Med 2012 Mar;25(3):231-236.
  111. Athanasiadis AP, Mikos T, Tambakoudis GP, Theodoridis TD, Papastergiou M, Assimakopoulos E, Tarlatzis BC. Neurodevelopmental fetal assessment using KANET scoring system in low and high-risk pregnancies. J Matern Fetal Neonatal Med 2013 Mar;26(4):363-368.
  112. Fauser BC, Tarlatzis BC, Rebar RW, Legro RS, Balen AH, Lobo R, Carmina E, Chang J, Yildiz BO, Laven JS, et al. Consensus on women's health aspects of polycystic ovary syndrome (PCOS): the Amsterdam ESHRE/ASRM-Sponsored 3rd PCOS Consensus Workshop Group. Fertil Steril 2012 Jan;97(1):28-38.e25
  113. Sirmans SM, Pate KA. Epidemiology, diagnosis and management of polycystic ovary syndrome. Clin Epidemiol 2014; 6:1-13.
  114. Fauser BC, Diedrich K, Bouchard P, Domínguez F, Matzuk M, Franks S, Hamamah S, Simón C, Devroey P, Ezcurra D, et al. Contemporary genetic technologies and female reproduction. Human Reproduction Update 2011 Nov;17(6):829-847.
  115. Balen A, Conway G, Kaltsas G. Polycystic ovary syndrome: the spectrum of the disorder in 1741 patients. Hum Reprod 1995 Aug;10(8):2107-2111.
  116. Azziz R, Sanchez L, Knochenhauer ES, Moran C, Lazenby J, Stephens KC, Taylor K, Boots LR. Androgen excess in women: experience with over 1000 consecutive patients. J Clin Endocrinol Metab 2004 Feb;89(2):453-462.
  117. Wild S, Pierpoint T, McKeigue P, Jacobs H. Cardiovascular disease in women with polycystic ovary syndrome at longterm follow-up: a retrospective cohort study. Clin Endocrinol (Oxf) 2000 May;52(5):595-600.
  118. Hollinrake E, Abreu A, Maifeld M, Van Voorhis BJ, Dokras A. Increased risk of depressive disorders in women with polycystic ovary syndrome. Fertil Steril 2007 Jun;87(6): 1369-1376.
  119. Zawadski JK, Dunaif A. Diagnostic criteria for polycystic ovary syndrome. In: Givens JHF, Merriman G, editors. The polycystic ovary syndrome. Cambridge, MA: Blackwell Scientific; 1992. p. 377-384.
  120. Rotterdam ESHRE/ASRM-Sponsored PCOS Consensus Workshop Group. Revised 2003 consensus on diagnostic criteria and long-term health risks related to polycystic ovary syndrome. Fertil Steril 2004 Jan;81(1):19-25.
  121. Azziz R, Carmina E, DeWailly D, Diamanti-Kandarakis E, Escobar-Morreale HF, Futterweit W, Janssen OE, Legro RS, Norman RJ, Taylor AE, et al. Position statement: criteria for defining polycystic ovary syndrome as a predominantly hyperandrogenic syndrome: an Androgen Excess Society guideline. J Clin Endocrinol Metab 2006 Nov;91(11):4237-4245.
  122. Lujan ME, Jarrett BY, Brooks ED, Reines JK, Peppin AK, Muhn N, Haider E, Pierson RA, Chizen DR. Updated ultrasound criteria for polycystic ovary syndrome: reliable thresholds for elevated follicle population and ovarian volume. Hum Reprod 2013 May;28(5):1361-1368.
  123. Badawy A, Elnashar A. Treatment options for polycystic ovary syndrome. Int J Womens Health 2011 Feb;3:25-35.
  124. ACOG Committee on Practice Bulletins—Gynecology. ACOG Practice Bulletin No 108: Polycystic ovary syndrome. Obstet Gynecol 2009 Oct;114(4):936-949.
  125. Thessaloniki ESHRE/ASRM-Sponsored PCOS Consensus Workshop Group Consensus on infertility treatment related to polycystic ovary syndrome. Fertil Steril 2008 Mar;89(3): 505-522.
  126. Balen AH. Ovulation induction in the management of anovulatory polycystic ovary syndrome. Mol Cell Endocrinol 2013 Jul;373(1-2):77-82.
  127. Berridge DL, Winter TC. Saline infusion sonohysterography: technique, indications, and imaging findings. J Ultrasound Med 2004 Jan;23(1):97-112.
  128. Allison SJ, Horrow MM, Kim HY, Lev-Toaff AS. Salineinfused sonohysterography: tips for achieving greater success. Radiographics 2011 Nov-Dec;31(7):1991-2004.
  129. O'Neill MJ. Sonohysterography. Radiol Clin North Am 2003 Jul;41(4):781-797.
  130. Bonnamy L, Marret H, Perrotin F, Body G, Berger C, Lansac J. Sonohysterography: a prospective survey of results and complications in 81 patients. Eur J Obstet Gynecol Reprod Biol 2002 Apr;102(1):42-47.
  131. Lindheim SR, Adsuar N, Kushner DM, Pritts EA, Olive DL. Sonohysterography: a valuable tool in evaluating the female pelvis. Obstet Gynecol Surv 2003 Nov;58(11):770-784.
  132. Lindheim SR, Sprague C, Winter TC. Hysterosalpingography and sonohysterography: lessons in technique. AJR Am J Roentgenol 2006 Jan;186(1):24-29.
  133. Jeanty P, Besnard S, Arnold A, Turner C, Crum P. Air-contrast sonohysterography as a first step assessment of tubal patency. J Ultrasound Med 2000 Aug;19(8):519-527.
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