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Different approaches for interpretation and reporting of immunohistochemistry analysis results in the bone tissue – a review

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Fedchenko, Nickolay, Reifenrath, Janin·2014·Diagnostic Pathology
DOI 10.1186/s13000-014-0221-9
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Abstract

BACKGROUND: Immunohistochemistry (IHC) is a well-established, widely accepted method in both clinical and experimental parts of medical science. It allows receiving valuable information about any process in any tissue, and especially in bone. Each year the amount of data, received by IHC, grows in geometric progression. But the lack of standardization, especially on the post-analytical stage (interpreting and reporting of results), makes the comparison of the results of different studies impossible. METHODS: Comprehensive PubMED literature search with a combination of search words "immunohistochemistry" and "scoring system" was performed and 773 articles describing IHC results were identified. After further manual analysis 120 articles were selected for detailed evaluation of used approaches. RESULTS: Six major approaches to the interpretation and presentation of IHC analysis results were identified, analyzed and described. CONCLUSIONS: The overview of the existing approaches in evaluation and interpretation of IHC data, which are provided in the article, can be used in bone tissue research and for either better understanding of existing scoring systems or developing a new one. Standard multiparametric, semiquantitative IHC scoring systems should simplify and clarify the process of interpretation and reporting of received data. VIRTUAL SLIDES: The virtual slide(s) for this article can be found here: http://www.diagnosticpathology.diagnomx.eu/vs/13000_2014_221.

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Research works printed but not linked: 136

  1. An YH, Martin KL: Handbook of Histology Methods for Bone and Cartilage. Softcover reprint of hardcover 1st ed. 2003 edition. 2010, Humana Press, Totowa, NJ
  2. Wittenburg G, Volkel C, Mai R, Lauer G: Immunohistochemical comparison of differentiation markers on paraffin and plastic embedded human bone samples. J Physiol Pharmacol Off J Pol Physiol Soc. 2009, 60 (Suppl 8): 43-49.
  3. Bancroft JD, Gamble M: Theory and Practice of Histological Techniques, 6e. 2007, Churchill Livingstone, Edinburgh, 6
  4. Dettmeyer R: Forensic Histopathology: Fundamentals and Perspectives. 1st ed. 2011. Corr. 5th printing 2013 edition. 2011, Springer, Berlin · DOI
  5. Mills SE: Histology for Pathologists. 2012, LWW, Philadelphia, 4
  6. Recker RR, Kimmel DB, Dempster D, Weinstein RS, Wronski TJ, Burr DB: Issues in modern bone histomorphometry. Bone. 2011, 49: 955-964. · DOI
  7. Klopfleisch R: Multiparametric and semiquantitative scoring systems for the evaluation of mouse model histopathology–a systematic review. BMC Vet Res. 2013, 9: 123- · DOI · Paper page
  8. Jambhekar N, Chaturvedi A, Madur B: Immunohistochemistry in surgical pathology practice: a current perspective of a simple, powerful, yet complex, tool. Indian J Pathol Microbiol. 2008, 51: 2- · doi:10.4103/0377-4929.40382
  9. Dabbs DJ: Diagnostic Immunohistochemistry. Elsevier Health Sciences; 2013. ISBN 978-1-4160-5766-6.
  10. Parfitt AM, Drezner MK, Glorieux FH, Kanis JA, Malluche H, Meunier PJ, Ott SM, Recker RR: Bone histomorphometry: standardization of nomenclature, symbols, and units. report of the ASBMR Histomorphometry Nomenclature Committee. J Bone Miner Res Off J Am Soc Bone Miner Res. 1987, 2: 595-610. · DOI · Paper page
  11. Shi S-R, Liu C, Taylor CR: Standardization of immunohistochemistry for formalin-fixed, paraffin-embedded tissue sections based on the antigen-retrieval technique: from experiments to hypothesis. J Histochem Cytochem. 2007, 55: 105-109. · DOI
  12. Dunstan RW, Wharton KA, Quigley C, Lowe A: The use of immunohistochemistry for biomarker assessment—can it compete with other technologies?. Toxicol Pathol. 2011, 39: 988-1002. · doi:10.1177/0192623311419163
  13. Shi S-R, Shi Y, Taylor CR: Antigen retrieval immunohistochemistry review and future prospects in research and diagnosis over two decades. J Histochem Cytochem. 2011, 59: 13-32. · DOI
  14. Kaczorowski S, Kaczorowska M: Is standardization possible in immunohistochemical examination?. Patol Pol. 1992, 43: 10-15.
  15. Walker RA: Quantification of immunohistochemistry–issues concerning methods, utility and semiquantitative assessment I. Histopathology. 2006, 49: 406-410. · DOI · Paper page
  16. Fritz P, Hönes J, Lutz D, Multhaupt H, Mischlinski A, Dörrer A, Schwarzmann P, Tuczek HV, Müller W: Quantitative immunohistochemistry: standardization and possible application in research and surgical pathology. Acta Histochem Suppl. 1989, 37: 213-219.
  17. Taylor CR: An exaltation of experts: concerted efforts in the standardization of immunohistochemistry. Hum Pathol. 1994, 25: 2-11. · doi:10.1016/0046-8177(94)90164-3
  18. Seidal T, Balaton AJ, Battifora H: Interpretation and quantification of immunostains. Am J Surg Pathol. 2001, 25: 1204-1207. · DOI
  19. Taylor CR, Levenson RM: Quantification of immunohistochemistry–issues concerning methods, utility and semiquantitative assessment II. Histopathology. 2006, 49: 411-424. · DOI · Paper page
  20. O’Leary TJ: Standardization in immunohistochemistry. Appl Immunohistochem Mol Morphol AIMM Off Publ Soc Appl Immunohistochem. 2001, 9: 3-8. · doi:10.1097/00022744-200103000-00002
  21. Torlakovic EE, Riddell R, Banerjee D, El-Zimaity H, Pilavdzic D, Dawe P, Magliocco A, Barnes P, Berendt R, Cook D, Gilks B, Williams G, Perez-Ordonez B, Wehrli B, Swanson PE, Otis CN, Nielsen S, Vyberg M, Butany J: Canadian Association of Pathologists-Association canadienne des pathologistes National Standards Committee/Immunohistochemistry: best practice recommendations for standardization of immunohistochemistry tests. Am J Clin Pathol. 2010, 133: 354-365. · doi:10.1309/ajcpdyz1xmf4hjwk
  22. Goldstein NS, Hewitt SM, Taylor CR, Yaziji H, Hicks DG: Recommendations for improved standardization of immunohistochemistry. Appl Immunohistochem Mol Morphol AIMM Off Publ Soc Appl Immunohistochem. 2007, 15: 124-133. · DOI · Paper page
  23. Lin F, Prichard J: Handbook of Practical Immunohistochemistry: Frequently Asked Questions. 2011, Springer, New York, 2011 · doi:10.1007/978-1-4419-8062-5
  24. Van Diest PJ, van Dam P, Henzen-Logmans SC, Berns E, van der Burg ME, Green J, Vergote I: A scoring system for immunohistochemical staining: consensus report of the task force for basic research of the EORTC-GCCG. European Organization for Research and Treatment of Cancer-Gynaecological Cancer Cooperative Group. J Clin Pathol. 1997, 50: 801-804. · DOI · Paper page
  25. Ramos-Vara JA: Technical aspects of immunohistochemistry. Vet Pathol Online. 2005, 42: 405-426. · DOI · Paper page
  26. Warford A, Akbar H, Riberio D: Antigen retrieval, blocking, detection and visualisation systems in immunohistochemistry: a review and practical evaluation of tyramide and rolling circle amplification systems. Methods San Diego Calif. 2014
  27. Shi S-R, Cote RJ, Taylor CR: Antigen retrieval immunohistochemistry: past, present, and future. J Histochem Cytochem. 1997, 45: 327-343. · DOI · Paper page
  28. Taylor CR: Immunohistochemistry in surgical pathology: principles and practice. Methods Mol Biol Clifton NJ. 2014, 1180: 81-109. · doi:10.1007/978-1-4939-1050-2_5
  29. Yamashita S: Heat-induced antigen retrieval: mechanisms and application to histochemistry. Prog Histochem Cytochem. 2007, 41: 141-200. · DOI · Paper page
  30. Chu P, Weiss L: Modern Immunohistochemistry with DVD-ROM. Cambridge University Press; 2014. ISBN 9781107040151. · doi:10.1017/cbo9781316167366
  31. Crissman JW, Goodman DG, Hildebrandt PK, Maronpot RR, Prater DA, Riley JH, Seaman WJ, Thake DC: Best practices guideline: toxicologic histopathology. Toxicol Pathol. 2004, 32: 126-131. · DOI · Paper page
  32. Gibson-Corley KN, Olivier AK, Meyerholz DK: Principles for valid histopathologic scoring in research. Vet Pathol. 2013, 50: 1007-1015. · DOI · Paper page
  33. Sojo K, Sawaki Y, Hattori H, Mizutani H, Ueda M: Immunohistochemical study of vascular endothelial growth factor (VEGF) and bone morphogenetic protein-2, −4 (BMP-2, −4) on lengthened rat femurs. J Cranio-Maxillo-fac Surg Off Publ Eur Assoc Cranio-Maxillo-fac Surg. 2005, 33: 238-245. · DOI
  34. Obuchowski NA: How many observers are needed in clinical studies of medical imaging?. Am J Roentgenol. 2004, 182: 867-869. · doi:10.2214/ajr.182.4.1820867
  35. Fitzgibbons PL, Dillon DA, Alsabeh R, Berman MA, Hayes DF, Hicks DG, Hughes KS, Nofech-Mozes S: Template for reporting results of biomarker testing of specimens from patients with carcinoma of the breast. Arch Pathol Lab Med. 2014, 138: 595-601. · DOI · Paper page
  36. Adams EJ, Green JA, Clark AH, Youngson JH: Comparison of different scoring systems for immunohistochemical staining. J Clin Pathol. 1999, 52: 75-77. · DOI
  37. Rhodes A, Jasani B, Balaton AJ, Miller KD: Immunohistochemical demonstration of oestrogen and progesterone receptors: correlation of standards achieved on in house tumours with that achieved on external quality assessment material in over 150 laboratories from 26 countries. J Clin Pathol. 2000, 53: 292-301. · doi:10.1136/jcp.53.4.292
  38. Campisi P, Hamdy RC, Lauzier D, Amako M, Rauch F, Lessard M-L: Expression of bone morphogenetic proteins during mandibular distraction osteogenesis. Plast Reconstr Surg. 2003, 111: 201-208. discussion 209–210 · DOI
  39. Yazawa M, Kishi K, Nakajima H, Nakajima T: Expression of bone morphogenetic proteins during mandibular distraction osteogenesis in rabbits. J Oral Maxillofac Surg Off J Am Assoc Oral Maxillofac Surg. 2003, 61: 587-592. · doi:10.1053/joms.2003.50116
  40. Long GV, Wilmott JS, Capper D, Preusser M, Zhang YE, Thompson JF, Kefford RF, von Deimling A, Scolyer RA: Immunohistochemistry is highly sensitive and specific for the detection of V600E BRAF mutation in melanoma. Am J Surg Pathol. 2013, 37: 61-65. · DOI · Paper page
  41. Hussein KA, Choksi K, Akeel S, Ahmad S, Megyerdi S, El-Sherbiny M, Nawaz M, Abu El-Asrar A, Al-Shabrawey M: Bone morphogenetic protein 2: a potential new player in the pathogenesis of diabetic retinopathy. Exp Eye Res. 2014, 125: 79-88. · DOI
  42. Campisi P, Hamdy RC, Lauzier D, Amako M, Schloss MD, Lessard ML: Overview of the radiology, histology, and bone morphogenetic protein expression during distraction osteogenesis of the mandible. J Otolaryngol. 2002, 31: 281-286. · doi:10.2310/7070.2002.34305
  43. Cao L, Wang J, Hou J, Xing W, Liu C: Vascularization and bone regeneration in a critical sized defect using 2-N,6-O-sulfated chitosan nanoparticles incorporating BMP-2. Biomaterials. 2014, 35: 684-698. · DOI · Paper page
  44. Adeyemo WL, Reuther T, Bloch W, Korkmaz Y, Fischer JH, Zöller JE, Kuebler AC: Influence of host periosteum and recipient bed perforation on the healing of onlay mandibular bone graft: an experimental pilot study in the sheep. Oral Maxillofac Surg. 2008, 12: 19-28. · DOI
  45. Alberius P, Gordh M: Osteopontin and bone sialoprotein distribution at the bone graft recipient site. Arch Otolaryngol Head Neck Surg. 1998, 124: 1382-1386. · doi:10.1001/archotol.124.12.1382
  46. Zhu W-Q, Wang X, Wang X-X, Wang Z-Y: Temporal and spatial expression of osteoprotegerin and receptor activator of nuclear factor -kappaB ligand during mandibular distraction in rats. J Cranio-Maxillo-fac Surg Off Publ Eur Assoc Cranio-Maxillo-fac Surg. 2007, 35: 103-111. · DOI
  47. Tanaka H, Mine T, Ogasa H, Taguchi T, Liang CT: Expression of RANKL/OPG during bone remodeling in vivo. Biochem Biophys Res Commun. 2011, 411: 690-694. · DOI
  48. Knabe C, Kraska B, Koch C, Gross U, Zreiqat H, Stiller M: A method for immunohistochemical detection of osteogenic markers in undecalcified bone sections. Biotech Histochem. 2006, 81: 31-39. · doi:10.1080/10520290600725474
  49. Cross SS: Grading and scoring in histopathology. Histopathology. 1998, 33: 99-106. · doi:10.1046/j.1365-2559.1998.00495.x
  50. Yan Y, Gong P, Jin W, Xu J, Wu X, Xu T, Hang Q, Fu H, Kei K, Gao Y: The cell-specific upregulation of bone morphogenetic protein-10 (BMP-10) in a model of rat cortical brain injury. J Mol Histol. 2012, 43: 543-552. · DOI
  51. Ishihara Y, Ueki K, Sotobori M, Marukawa K, Moroi A: Bone regeneration by statin and low-intensity pulsed ultrasound (LIPUS) in rabbit nasal bone. J Cranio-Maxillo-fac Surg Off Publ Eur Assoc Cranio-Maxillo-fac Surg. 2014, 42: 185-193. · doi:10.1016/j.jcms.2013.05.002
  52. Shi W, Gong P, Fan J, Yan YH, Ni L, Wu X, Cui G, Wu X, Gu X, Chen J: The expression pattern of ADP-ribosyltransferase 3 in rat traumatic brain injury. J Mol Histol. 2012, 43: 37-47. · doi:10.1007/s10735-011-9366-y
  53. Anannamcharoen S, Nimmanon T: Study of the vascular endothelial growth factor (VEGF) expression and microvascular density (MVD) in primary colorectal cancer specimens. J Med Assoc Thail Chotmaihet Thangphaet. 2012, 95: 1041-1047.
  54. Kumagai Y, Sobajima J, Higashi M, Ishiguro T, Fukuchi M, Ishibashi K, Baba H, Mochiki E, Yakabi K, Kawano T, Tamaru J, Ishida H: Angiogenesis in superficial esophageal squamous cell carcinoma: assessment of microvessel density based on immunostaining for CD34 and CD105. Jpn J Clin Oncol. 2014, 44: 526-533. · doi:10.1093/jjco/hyu039
  55. Łuczyńska E, Gasińska A, Wilk W: Microvessel density and expression of vascular endothelial growth factor in clinically localized prostate cancer. Pol J Pathol Off J Pol Soc Pathol. 2013, 64: 33-38. · doi:10.5114/pjp.2013.34601
  56. Elezoğlu B, Tolunay S: The relationship between the stromal mast cell number, microvessel density, c-erbB-2 staining and survival and prognostic factors in colorectal carcinoma. Türk Patoloji Derg. 2012, 28: 110-118.
  57. Wobser M, Siedel C, Kneitz H, Bröcker E-B, Goebeler M, Houben R, Geissinger E: Microvessel density and expression of vascular endothelial growth factor and its receptors in different subtypes of primary cutaneous B-cell lymphoma. Acta Derm Venereol. 2013, 93: 656-662. · DOI
  58. Wang H-L, Zhang Z-L: Analysis of the relationship between ultrasound of breast cancer DOT-SDI and the expression of MVD, VEGF and HIF-1α. Cell Biochem Biophys. 2014, 70 (1): 205-208. · DOI
  59. Bădescu A, Georgescu CV, Vere CC, Crăiţoiu S, Grigore D: Correlations between Her2 oncoprotein, VEGF expression, MVD and clinicopathological parameters in gastric cancer. Romanian J Morphol Embryol Rev Roum Morphol Embryol. 2012, 53: 997-1005.
  60. Cai Y, Zhang J: Expression of fascin and correlation with MVD in sinonasal inverted papilloma. Lin Chuang Er Bi Yan Hou Tou Jing Wai Ke Za Zhi J Clin Otorhinolaryngol Head Neck Surg. 2012, 26: 629-632.
  61. Bodnar M, Szylberg Ł, Kaźmierczak W, Marszałek A: Evaluation of microvessel density (MVD) in laryngeal squamous cell carcinoma. Przegļd Lek. 2012, 69: 726-730.
  62. Boëck-Neto RJ, Artese L, Piattelli A, Shibli JA, Perrotti V, Piccirilli M, Marcantonio E: VEGF and MVD expression in sinus augmentation with autologous bone and several graft materials. Oral Dis. 2009, 15: 148-154. · DOI
  63. Geiger F, Beverungen M, Lorenz H, Wieland J, Fehr M, Kasten P: Bone substitute effect on vascularization and bone remodeling after application of phVEGF165 transfected BMSC. J Funct Biomater. 2012, 3: 313-326. · doi:10.3390/jfb3020313
  64. Weidner N, Semple JP, Welch WR, Folkman J: Tumor angiogenesis and metastasis — correlation in invasive breast carcinoma. N Engl J Med. 1991, 324: 1-8. · DOI · Paper page
  65. Chen J, Wu X, Shao B, Zhao W, Shi W, Zhang S, Ni L, Shen A: Increased expression of TNF receptor-associated factor 6 after rat traumatic brain injury. Cell Mol Neurobiol. 2011, 31: 269-275. · doi:10.1007/s10571-010-9617-6
  66. Ramazanoglu M, Lutz R, Rusche P, Trabzon L, Kose GT, Prechtl C, Schlegel KA: Bone response to biomimetic implants delivering BMP-2 and VEGF: an immunohistochemical study. J Cranio-Maxillofac Surg. 2013, 41: 826-835. · DOI
  67. Bondarenko A, Angrisani N, Meyer-Lindenberg A, Seitz JM, Waizy H, Reifenrath J: Magnesium-based bone implants: immunohistochemical analysis of peri-implant osteogenesis by evaluation of osteopontin and osteocalcin expression. J Biomed Mater Res A. 2014, 102: 1449-1457. · DOI
  68. Bologna-Molina R, Damián-Matsumura P, Molina-Frechero N: An easy cell counting method for immunohistochemistry that does not use an image analysis program. Histopathology. 2011, 59: 801-803. · DOI
  69. Wang C-J, Huang K-E, Sun Y-C, Yang Y-J, Ko J-Y, Weng L-H, Wang F-S: VEGF modulates angiogenesis and osteogenesis in shockwave-promoted fracture healing in rabbits. J Surg Res. 2011, 171: 114-119. · DOI
  70. Wehrhan F, Amann K, Molenberg A, Lutz R, Neukam FW, Schlegel KA: Critical size defect regeneration using PEG-mediated BMP-2 gene delivery and the use of cell occlusive barrier membranes - the osteopromotive principle revisited. Clin Oral Implants Res. 2013, 24: 910-920. · doi:10.1111/j.1600-0501.2012.02489.x
  71. Wehrhan F, Amann K, Molenberg A, Lutz R, Neukam FW, Schlegel KA: PEG matrix enables cell-mediated local BMP-2 gene delivery and increased bone formation in a porcine critical size defect model of craniofacial bone regeneration. Clin Oral Implants Res. 2012, 23: 805-813. · DOI
  72. Yoshikawa H, Rettig WJ, Takaoka K, Alderman E, Rup B, Rosen V, Wozney JM, Lane JM, Huvos AG, Garin-Chesa P: Expression of bone morphogenetic proteins in human osteosarcoma. immunohistochemical detection with monoclonal antibody. Cancer. 1994, 73: 85-91. · doi:10.1002/1097-0142(19940101)73:1<85::aid-cncr2820730116>3.0.co;2-8
  73. Cheung LK, Zheng LW, Ma L: Effect of distraction rates on expression of bone morphogenetic proteins in rabbit mandibular distraction osteogenesis. J Cranio-Maxillo-fac Surg Off Publ Eur Assoc Cranio-Maxillo-fac Surg. 2006, 34: 263-269. · DOI
  74. Sulzbacher I, Birner P, Trieb K, Pichlbauer E, Lang S: The expression of bone morphogenetic proteins in osteosarcoma and its relevance as a prognostic parameter. J Clin Pathol. 2002, 55: 381-385. · doi:10.1136/jcp.55.5.381
  75. DeRycke MS, Andersen JD, Harrington KM, Pambuccian SE, Kalloger SE, Boylan KLM, Argenta PA, Skubitz APN: S100A1 expression in ovarian and endometrial endometrioid carcinomas is a prognostic indicator of relapse-free survival. Am J Clin Pathol. 2009, 132: 846-856. · DOI
  76. Rizzardi AE, Johnson AT, Vogel RI, Pambuccian SE, Henriksen J, Skubitz AP, Metzger GJ, Schmechel SC: Quantitative comparison of immunohistochemical staining measured by digital image analysis versus pathologist visual scoring. Diagn Pathol. 2012, 7: 42- · DOI · Paper page
  77. Soares AF, Xavier RL de F, da Costa Miguel MC, de Souza LB, Pinto LP: Bone morphogenetic protein-2/4 and bone morphogenetic protein receptor type IA expression in metastatic and nonmetastatic oral squamous cell carcinoma. Am J Otolaryngol. 2010, 31: 266-271. · doi:10.1016/j.amjoto.2009.03.002
  78. Laboux O, Ste-Marie L-G, Glorieux FH, Nanci A: Quantitative immunogold labeling of bone sialoprotein and osteopontin in methylmethacrylate-embedded rat bone. J Histochem Cytochem Off J Histochem Soc. 2003, 51: 61-67. · doi:10.1177/002215540305100108
  79. Ida CM, Vrana JA, Rodriguez FJ, Jentoft ME, Caron AA, Jenkins SM, Giannini C: Immunohistochemistry is highly sensitive and specific for detection of BRAF V600E mutation in pleomorphic xanthoastrocytoma. Acta Neuropathol Commun. 2013, 1: 20- · doi:10.1186/2051-5960-1-20
  80. Sand JP, Kokorina NA, Zakharkin SO, Lewis JS, Nussenbaum B: BMP-2 expression correlates with local failure in head and neck squamous cell carcinoma. Otolaryngol-Head Neck Surg Off J Am Acad Otolaryngol-Head Neck Surg. 2014, 150: 245-250. · doi:10.1177/0194599813513003
  81. De Oliveira Neto PJ, Cricchio G, Hawthorne AC, Okamoto R, Sennerby L, Lungren S, Salata LA: Tomographic, histological, and immunohistochemical evidences on the use of N-butyl-2-cyanoacrilate for onlay graft fixation in rabbits. Clin Implant Dent Relat Res. 2012, 14: 861-871. · doi:10.1111/j.1708-8208.2010.00321.x
  82. Yang R, Davies CM, Archer CW, Richards RG: Immunohistochemistry of matrix markers in Technovit 9100 New-embedded undecalcified bone sections. Eur Cell Mater. 2003, 6: 57-71. discussion 71 · DOI
  83. Zimmermann A-K, Camenisch U, Rechsteiner MP, Bode-Lesniewska B, Rössle M: Value of immunohistochemistry in the detection of BRAFV600E mutations in fine-needle aspiration biopsies of papillary thyroid carcinoma. Cancer Cytopathol. 2014, 122: 48-58. · DOI
  84. Kapoor P, Deshmukh R: VEGF: a critical driver for angiogenesis and subsequent tumor growth: An IHC study. J Oral Maxillofac Pathol JOMFP. 2012, 16: 330-337. · doi:10.4103/0973-029x.102478
  85. Kukreja I, Kapoor P, Deshmukh R, Kulkarni V: VEGF and CD 34: a correlation between tumor angiogenesis and microvessel density-an immunohistochemical study. J Oral Maxillofac Pathol JOMFP. 2013, 17: 367-373. · doi:10.4103/0973-029x.125200
  86. Bösmüller H, Fischer A, Pham DL, Fehm T, Capper D, von Deimling A, Bonzheim I, Staebler A, Fend F: Detection of the BRAF V600E mutation in serous ovarian tumors: a comparative analysis of immunohistochemistry with a mutation-specific monoclonal antibody and allele-specific PCR. Hum Pathol. 2013, 44: 329-335. · doi:10.1016/j.humpath.2012.07.010
  87. Raica M, Cimpean AM, Anghel A: Immunohistochemical expression of vascular endothelial growth factor (VEGF) does not correlate with microvessel density in renal cell carcinoma. Neoplasma. 2007, 54: 278-284.
  88. Li Y, Wei Q, Feng J, Xu M, Huang R, Shi F: Expression of bone morphogenetic protein 2, 4, and related components of the BMP signaling pathway in the mouse uterus during the estrous cycle. J Zhejiang Univ Sci B. 2014, 15: 601-610. · doi:10.1631/jzus.b1300288
  89. Shi F, Stewart RL, Perez E, Chen JY-H, LaPolt PS: Cell-specific expression and regulation of soluble guanylyl cyclase alpha 1 and beta 1 subunits in the rat ovary. Biol Reprod. 2004, 70: 1552-1561. · doi:10.1095/biolreprod.103.025510
  90. Hawthorne AC, Xavier SP, Okamoto R, Salvador SL, Antunes AA, Salata LA: Immunohistochemical, tomographic, and histological study on onlay bone graft remodeling. part III: allografts. Clin Oral Implants Res. 2013, 24: 1164-1172. · doi:10.1111/j.1600-0501.2012.02528.x
  91. Guskuma MH, Hochuli-Vieira E, Pereira FP, Rangel-Garcia I, Okamoto R, Okamoto T, Filho OM: Evaluation of the presence of VEGF, BMP2 and CBFA1 proteins in autogenous bone graft: histometric and immunohistochemical analysis. J Cranio-Maxillofac Surg. 2014, 42: 333-339. · doi:10.1016/j.jcms.2013.05.022
  92. Yu YY, Lieu S, Lu C, Miclau T, Marcucio RS, Colnot C: Immunolocalization of BMPs, BMP antagonists, receptors, and effectors during fracture repair. Bone. 2010, 46: 841-851. · DOI
  93. Li Y, Zhou X, Wei Q, Huang R, Shi F: Cell-specific expression and immunolocalization of nitric oxide synthase isoforms and soluble guanylyl cyclase α and β subunits in postnatal porcine uteri. Acta Histochem. 2014, 116: 466-473. · DOI
  94. Koerdt S, Siebers J, Bloch W, Ristow O, Kuebler AC, Reuther T: Role of oxidative and nitrosative stress in autogenous bone grafts to the mandible using guided bone regeneration and a deproteinized bovine bone material. J Cranio-Maxillo-fac Surg Off Publ Eur Assoc Cranio-Maxillo-fac Surg. 2014, 42: 560-567. · DOI
  95. Ding W, Zhang W, Hui F, Zhang Y, Zhang F, Li X, Shi F: Cell-specific expression and immunolocalization of nitric oxide synthase isoforms and soluble guanylyl cyclase α1 and β1 subunits in the ovary of fetal, neonatal and immature pigs. Anim Reprod Sci. 2012, 131: 172-180. · DOI
  96. Suter WN: Introduction to Educational Research: A Critical Thinking Approach. Second Edition edition. 2011, SAGE Publications, Inc, Thousand Oaks, Calif
  97. Shang ZJ, Li JR: Expression of endothelial nitric oxide synthase and vascular endothelial growth factor in oral squamous cell carcinoma: its correlation with angiogenesis and disease progression. J Oral Pathol Med Off Publ Int Assoc Oral Pathol Am Acad Oral Pathol. 2005, 34: 134-139.
  98. Shackelford C, Long G, Wolf J, Okerberg C, Herbert R: Qualitative and quantitative analysis of nonneoplastic lesions in toxicology studies. Toxicol Pathol. 2002, 30: 93-96. · DOI · Paper page
  99. Thoolen B, Maronpot RR, Harada T, Nyska A, Rousseaux C, Nolte T, Malarkey DE, Kaufmann W, Küttler K, Deschl U, Nakae D, Gregson R, Vinlove MP, Brix AE, Singh B, Belpoggi F, Ward JM: Proliferative and nonproliferative lesions of the rat and mouse hepatobiliary system. Toxicol Pathol. 2010, 38 (7 Suppl): 5S-81S. · DOI · Paper page
  100. De la Torre NG, Buley I, Wass JAH, Turner HE: Angiogenesis and lymphangiogenesis in thyroid proliferative lesions: relationship to type and tumour behaviour. Endocr Relat Cancer. 2006, 13: 931-944. · DOI
  101. Jin Y, Tipoe GL, Liong EC, Lau TYH, Fung PCW, Leung KM: Overexpression of BMP-2/4, −5 and BMPR-IA associated with malignancy of oral epithelium. Oral Oncol. 2001, 37: 225-233. · DOI
  102. Sappayatosok K, Maneerat Y, Swasdison S, Viriyavejakul P, Dhanuthai K, Zwang J, Chaisri U: Expression of pro-inflammatory protein, iNOS, VEGF and COX-2 in oral squamous cell carcinoma (OSCC), relationship with angiogenesis and their clinico-pathological correlation. Med Oral Patol Oral Cir Bucal. 2009, 14: E319-E324.
  103. Megumi K, Ishigami S, Uchikado Y, Kita Y, Okumura H, Matsumoto M, Uenosono Y, Arigami T, Kijima Y, Kitazono M, Shinchi H, Ueno S, Natsugoe S: Clinicopathological significance of BMP7 expression in esophageal squamous cell carcinoma. Ann Surg Oncol. 2012, 19: 2066-2071. · doi:10.1245/s10434-011-2024-5
  104. Hübner R-H, Gitter W, El Mokhtari NE, Mathiak M, Both M, Bolte H, Freitag-Wolf S, Bewig B: Standardized quantification of pulmonary fibrosis in histological samples. Biotechniques. 2008, 44: 507-511. 514–517 · DOI · Paper page
  105. Cheek E, Rajkumar C: How to present statistics in medical journals. Age Ageing. 2014, 43: 306-308. · DOI
  106. Klein M, Picard E, Vignaud JM, Marie B, Bresler L, Toussaint B, Weryha G, Duprez A, Leclère J: Vascular endothelial growth factor gene and protein: strong expression in thyroiditis and thyroid carcinoma. J Endocrinol. 1999, 161: 41-49. · DOI
  107. Klein M, Vignaud JM, Hennequin V, Toussaint B, Bresler L, Plénat F, Leclère J, Duprez A, Weryha G: Increased expression of the vascular endothelial growth factor is a pejorative prognosis marker in papillary thyroid carcinoma. J Clin Endocrinol Metab. 2001, 86: 656-658. · doi:10.1210/jcem.86.2.7226
  108. Nakagawa S, Cuthill IC: Effect size, confidence interval and statistical significance: a practical guide for biologists. Biol Rev. 2007, 82: 591-605. · DOI · Paper page
  109. Remmele W, Stegner HE: Recommendation for uniform definition of an immunoreactive score (IRS) for immunohistochemical estrogen receptor detection (ER-ICA) in breast cancer tissue. Pathol. 1987, 8: 138-140.
  110. McCarty KS, Miller LS, Cox EB, Konrath J, McCarty KS: Estrogen receptor analyses. correlation of biochemical and immunohistochemical methods using monoclonal antireceptor antibodies. Arch Pathol Lab Med. 1985, 109: 716-721.
  111. Cagle PT, Sholl LM, Lindeman NI, Alsabeh R, Divaris DXG, Foulis P, Lee G, Neal JW, Nowak JA, Yu PP: Template for reporting results of biomarker testing of specimens from patients with non-small cell carcinoma of the lung. Arch Pathol Lab Med. 2014, 138: 171-174. · DOI
  112. Bartley AN, Hamilton SR, Alsabeh R, Ambinder EP, Berman M, Collins E, Fitzgibbons PL, Gress DM, Nowak JA, Samowitz WS, Zafar SY: Template for reporting results of biomarker testing of specimens from patients with carcinoma of the colon and rectum. Arch Pathol Lab Med. 2014, 138: 166-170. · DOI
  113. Allred DC, Harvey JM, Berardo M, Clark GM: Prognostic and predictive factors in breast cancer by immunohistochemical analysis. Mod Pathol Off J U S Can Acad Pathol Inc. 1998, 11: 155-168.
  114. Harvey JM, Clark GM, Osborne CK, Allred DC: Estrogen receptor status by immunohistochemistry is superior to the ligand-binding assay for predicting response to adjuvant endocrine therapy in breast cancer. J Clin Oncol Off J Am Soc Clin Oncol. 1999, 17: 1474-1481. · DOI · Paper page
  115. Detre S, Saclani Jotti G, Dowsett M: A “quickscore” method for immunohistochemical semiquantitation: validation for oestrogen receptor in breast carcinomas. J Clin Pathol. 1995, 48: 876-878. · DOI · Paper page
  116. Sangplod P, Sangkhathat S, Boonpipattanapong T, Kanngurn S: Association of BMP6 methylation and expression with clinicopathological features in colorectal cancer. Int J Biosci Biochem Bioinforma. 2013, 3 (5): 452-455.
  117. Kejner AE, Burch MB, Sweeny L, Rosenthal EL: Bone morphogenetic protein 6 expression in oral cavity squamous cell cancer is associated with bone invasion. Laryngoscope. 2013, 123: 3061-3065. · doi:10.1002/lary.24267
  118. Bramwell VH, Tuck AB, Chapman J-AW, Anborgh PH, Postenka CO, Al-Katib W, Shepherd LE, Han L, Wilson CF, Pritchard KI, Pollak MN, Chambers AF: Assessment of osteopontin in early breast cancer: correlative study in a randomised clinical trial. Breast Cancer Res BC. 2014, 16: R8- · doi:10.1186/bcr3600
  119. Parris TZ, Aziz L, Kovacs A, Hajizadeh S, Nemes S, Semaan M, Chen CY, Karlsson P, Helou K: Clinical relevance of breast cancer-related genes as potential biomarkers for oral squamous cell carcinoma. BMC Cancer. 2014, 14: 324- · DOI
  120. Koerdt S, Siebers J, Bloch W, Ristow O, Kuebler AC, Reuther T: Immunohistochemial study on the expression of von Willebrand factor (vWF) after onlay autogenous iliac grafts for lateral alveolar ridge augmentation. Head Face Med. 2013, 9: 40- · doi:10.1186/1746-160x-9-40
  121. Koerdt S, Ristow O, Wannhoff A, Kübler AC, Reuther T: Expression of growth factors during the healing process of alveolar ridge augmentation procedures using autogenous bone grafts in combination with GTR and an anorganic bovine bone substitute: an immunohistochemical study in the sheep. Clin Oral Investig. 2014, 18: 179-188. · doi:10.1007/s00784-013-0938-y
  122. Raida M, Sarbia M, Clement JH, Adam S, Gabbert HE, Höffken K: Expression, regulation and clinical significance of bone morphogenetic protein 6 in esophageal squamous-cell carcinoma. Int J Cancer. 1999, 83: 38-44. · doi:10.1002/(sici)1097-0215(19990924)83:1<38::aid-ijc8>3.0.co;2-b
  123. De Carvalho CHP, Nonaka CFW, de Araújo CRF, de Souza LB, Pinto LP: Immunoexpression of bone morphogenetic protein-2 (BMP-2), BMP receptor type IA, and BMP receptor type II in metastatic and non-metastatic lower lip squamous cell carcinoma. J Oral Pathol Med Off Publ Int Assoc Oral Pathol Am Acad Oral Pathol. 2011, 40: 181-186.
  124. Krajewska M, Krajewski S, Epstein JI, Shabaik A, Sauvageot J, Song K, Kitada S, Reed JC: Immunohistochemical analysis of bcl-2, bax, bcl-X, and mcl-1 expression in prostate cancers. Am J Pathol. 1996, 148: 1567-1576.
  125. Choudhury KR, Yagle KJ, Swanson PE, Krohn KA, Rajendran JG: A robust automated measure of average antibody staining in immunohistochemistry images. J Histochem Cytochem. 2010, 58: 95-107. · DOI
  126. Fu D, Yang S, Li K, Yuan Y: Expression of vascular endothelial growth factor in bone morphogenic protein-2 induced osteogenesis. J Wuhan Univ Technol-Mater Sci Ed. 2005, 20: 118-122.
  127. Zhu C, Wang J, Cheng T, Li Q, Shen H, Qin H, Cheng M, Zhang X: The potential role of increasing the release of mouse ?- defensin-14 in the treatment of osteomyelitis in mice: a primary study. PLoS One. 2014, 9 (1): e86874- · DOI
  128. Zhang H, Zhao X, Zhang Z, Chen W, Zhang X: An Immunohistochemistry study of Sox9, Runx2, and osterix expression in the mandibular cartilages of newborn mouse. BioMed Res Int. 2013, 2013: e265380-
  129. Prichard J, Bitting A, Myers J: Overview of Automated Immunohistochemistry. Handb Pract Immunohistochem. Edited by: Lin F, Prichard J. 2011, Springer, New York, 23-30. · doi:10.1007/978-1-4419-8062-5_3
  130. Brey EM, Lalani Z, Johnston C, Wong M, McIntire LV, Duke PJ, Patrick CW: Automated selection of DAB-labeled tissue for immunohistochemical quantification. J Histochem Cytochem. 2003, 51: 575-584. · DOI
  131. Alvarenga AW, Coutinho-Camillo CM, Rodrigues BR, Rocha RM, Torres LFB, Martins VR, da Cunha IW, Hajj GNM: A comparison between manual and automated evaluations of tissue microarray patterns of protein expression. J Histochem Cytochem. 2013, 61: 272-282. · DOI
  132. Schlederer M, Mueller KM, Haybaeck J, Heider S, Huttary N, Rosner M, Hengstschläger M, Moriggl R, Dolznig H, Kenner L: Reliable quantification of protein expression and cellular localization in histological sections. PLoS One. 2014, 9: e100822- · DOI
  133. Mohammed ZMA, Orange C, McMillan DC, Mallon E, Doughty JC, Edwards J, Going JJ: Comparison of visual and automated assessment of microvessel density and their impact on outcome in primary operable invasive ductal breast cancer. Hum Pathol. 2013, 44: 1688-1695. · doi:10.1016/j.humpath.2012.11.023
  134. Strömberg S, Björklund MG, Asplund C, Sköllermo A, Persson A, Wester K, Kampf C, Nilsson P, Andersson A-C, Uhlen M, Kononen J, Ponten F, Asplund A: A high-throughput strategy for protein profiling in cell microarrays using automated image analysis. Proteomics. 2007, 7: 2142-2150. · DOI
  135. Kraan MC, Haringman JJ, Ahern MJ, Breedveld FC, Smith MD, Tak PP: Quantification of the cell infiltrate in synovial tissue by digital image analysis. Rheumatology. 2000, 39: 43-49. · DOI
  136. Ali HR, Irwin M, Morris L, Dawson S-J, Blows FM, Provenzano E, Mahler-Araujo B, Pharoah PD, Walton NA, Brenton JD, Caldas C: Astronomical algorithms for automated analysis of tissue protein expression in breast cancer. Br J Cancer. 2013, 108: 602-612. · DOI

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Metadata

Authors
Fedchenko, N., & Reifenrath, J.
Venue
Diagnostic Pathology
Publisher
Springer Science and Business Media LLC
Published
2014-11-29
Volume
9
Issue
1
Pages
221-221
ISSN
1746-1596 (ISSN-L)
DOI
10.1186/s13000-014-0221-9
OpenAlex
W2112825838
Cited by
808
References
2
FWCI
6.41
Type
journal article
Language
en
Open access
gold
Licence
creativecommons.org/licenses/by/4.0 (unspecified)

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CoChat. (2026). Citation check: Different approaches for interpretation and reporting of immunohistochemistry analysis results in the bone tissue – a review. https://app.cochat.ai/papers/10.1186/s13000-014-0221-9
The paper
Fedchenko, N., & Reifenrath, J. (2014). Different approaches for interpretation and reporting of immunohistochemistry analysis results in the bone tissue – a review. Diagnostic Pathology. https://doi.org/10.1186/s13000-014-0221-9

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Contains information from the Semantic Scholar Academic Graph Datasets, made available under the ODC Attribution License (ODC-BY 1.0).

Semantic Scholar’s data is described in: Kinney, R., et al. (2023). The Semantic Scholar Open Data Platform. arXiv:2301.10140.