Diagnostic and prognostic value of cancer stem cell marker CD44 and soluble CD44 in the peripheral Blood of patients with oral Squamous cell carcinoma

Aya K. Khamis, Hamed A. Fouad, Hanaa S. Raslan, Mohamed M. Fata, Amira I. Fayad

Abstract


Background

Head and neck cancer is a major health problem. Recent studies on the pathobiology of oral squamous cell carcinoma (OSCC) have led to the discovery of a small population of cancer cells with a consistent behavior with the features of cancer stem cells (CSCs).  CSCs are required and responsible for initiation, maintenance and recurrence of disease. Molecular markers are commonly used for the identification of CSCs. CD44 is the most reported CSC marker in OSCC.

The aim of the study was to evaluate and correlate the expression of CD44 in different histopathological grades of OSCC, as well as to assess the diagnostic and prognostic value of soluble CD44 (CD44sol) in peripheral blood of patients.

Materials and methods

Fifteen patients with OSCC were included; biopsies were histologically evaluated using haematoxylin and eosin. Serial sections were immunohistochemically stained by monoclonal antibody to CD44. The intensity of immunostaining of CD44 was calculated. Enzyme-linked immunosorbent assay (ELISA) method was used to determine the concentration of CD44sol in the blood serum.

Results

All grades of OSCC showed membranous immunosignaling of CD44. The well, moderately and poorly differentiated OSCC cases showed weak, moderate and intense positive membranous immunosignaling of CD44 respectively.

CD44sol levels were significantly higher in OSCC patients than they were in control groups. Soluble CD44 serum levels were significantly higher in poorly differentiated than they were in moderately and well differentiated.

Conclusion

CSCs detection in fixed human tissue and CD44sol detection in peripheral blood using ELISA seemed to be a promising method and may have a diagnostic and prognostic value in management of OSCC.

Keywords


Caner stem cell, CD44, soluble CD44, stem cells and oral squamous cell carcinoma

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References


Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA: a cancer journal for clinicians. 2011 Mar-Apr;61(2):69-90.

Moazeni-Roodi A, Allameh A, Harirchi I, Motiee-Langroudi M, Garajei A. Studies on the Contribution of Cox-2 Expression in the Progression of Oral Squamous Cell Carcinoma and H-Ras Activation. Pathology & Oncology Research. 2016:1-6.

Joseph LJ, Goodman M, Higgins K, Pilai R, Ramalingam SS, Magliocca K, et al. Racial disparities in squamous cell carcinoma of the oral tongue among women: A SEER data analysis. Oral Oncology. 2015;51(6):586-92.

NCI. Cancer Trends Progress Report2009/2010.

Sinha N, Mukhopadhyay S, Das DN, Panda PK, Bhutia SK. Relevance of cancer initiating/stem cells in carcinogenesis and therapy resistance in oral cancer. Oral Oncology. 2013;49(9):854-62.

WHO. The World Oral Health Report 2003. Geneva2003.

Rasool M, Khan SR, Malik A, Khan KM, Zahid S, Manan A, et al. Comparative Studies of Salivary and Blood Sialic Acid, Lipid Peroxidation and Antioxidative Status in Oral Squamous Cell Carcinoma (OSCC). Pak J Med Sci. 2014 2014/05//;30(3):466-71.

Silva LP, Gonzaga AKG, Serpa MS, Nascimento GJF, Sobral APV. Immunohistochemical expression of cyclooxygenase-2 and cyclin-D1 in oral squamous cell carcinoma. Journal of Oral and Maxillofacial Surgery, Medicine, and Pathology. 2017.

Prince ME, Sivanandan R, Kaczorowski A, Wolf GT, Kaplan MJ, Dalerba P, et al. Identification of a subpopulation of cells with cancer stem cell properties in head and neck squamous cell carcinoma. Proceedings of the National Academy of Sciences. 2007 January 16, 2007;104(3):973-8.

Zubair H, Azim S, Srivastava SK, Bhardwaj A, Marimuthu S, Patton MC, et al. Cancer Stem Cells. Stem Cells in Toxicology and Medicine: John Wiley & Sons, Ltd; 2016. p. 375-413.

Zhang Z, Filho MSA, Nör JE. The biology of head and neck cancer stem cells. Oral Oncology. 2012;48(1):1-9.

Somorjai IM, Lohmann JU, Holstein TW, Zhao Z. Stem cells: a view from the roots. Biotechnol J. 2012 Jun;7(6):704-22.

Grskovic M, Javaherian A, Strulovici B, Daley GQ. Induced pluripotent stem cells--opportunities for disease modelling and drug discovery. Nat Rev Drug Discov. 2011;10(12):915-29.

Diecke S, Jung SM, Lee J, Ju JH. Recent technological updates and clinical applications of induced pluripotent stem cells. Korean J Intern Med. 2014 Sep;29(5):547-57.

Murry CE, Keller G. Differentiation of embryonic stem cells to clinically relevant populations: lessons from embryonic development. Cell. 2008;132(4):661-80.

Li X, Bai J, Ji X, Li R, Xuan Y, Wang Y. Comprehensive characterization of four different populations of human mesenchymal stem cells as regards their immune properties, proliferation and differentiation. Int J Mol Med. 2014 Sep;34(3):695-704.

Miles DC, de Vries NA, Gisler S, Lieftink C, Akhtar W, Gogola E, et al. TRIM28 is an Epigenetic Barrier to Induced Pluripotent Stem Cell Reprogramming. Stem Cells. 2017;35(1):147-57.

Clarke MF, Dick JE, Dirks PB, Eaves CJ, Jamieson CH, Jones DL, et al. Cancer stem cells--perspectives on current status and future directions: AACR Workshop on cancer stem cells. Cancer Res. 2006 Oct 1;66(19):9339-44.

Virchow R. Die Cellularpathologie in ihrer Begrundung auf physiologische und

pathologische Gewebelehre. Berlin , Germany: August Hirschwald; 1858.

Allegra E, Trapasso S. Cancer stem cells in head and neck cancer. OncoTargets and therapy. 2012;5:375-83.

Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF. Prospective identification of tumorigenic breast cancer cells. Proceedings of the National Academy of Sciences of the United States of America. 2003 Apr 1;100(7):3983-8.

Singh SK, Clarke ID, Terasaki M, Bonn VE, Hawkins C, Squire J, et al. Identification of a cancer stem cell in human brain tumors. Cancer Res. 2003 Sep 15;63(18):5821-8.

Collins AT, Berry PA, Hyde C, Stower MJ, Maitland NJ. Prospective identification of tumorigenic prostate cancer stem cells. Cancer Res. 2005 Dec 1;65(23):10946-51.

Dalerba P, Dylla SJ, Park IK, Liu R, Wang X, Cho RW, et al. Phenotypic characterization of human colorectal cancer stem cells. Proceedings of the National Academy of Sciences of the United States of America. 2007 Jun 12;104(24):10158-63.

Li C, Heidt DG, Dalerba P, Burant CF, Zhang L, Adsay V, et al. Identification of pancreatic cancer stem cells. Cancer Res. 2007 Feb 1;67(3):1030-7.

Ho MM, Ng AV, Lam S, Hung JY. Side population in human lung cancer cell lines and tumors is enriched with stem-like cancer cells. Cancer Res. 2007 May 15;67(10):4827-33.

Wicha MS, Liu S, Dontu G. Cancer Stem Cells: An Old Idea—A Paradigm Shift. Cancer Res. 2006 February 15, 2006;66(4):1883-90.

Costea DE, Tsinkalovsky O, Vintermyr OK, Johannessen AC, Mackenzie IC. Cancer stem cells - new and potentially important targets for the therapy of oral squamous cell carcinoma. Oral diseases. 2006 Sep;12(5):443-54.

Sayed SI, Dwivedi RC, Katna R, Garg A, Pathak KA, Nutting CM, et al. Implications of understanding cancer stem cell (CSC) biology in head and neck squamous cell cancer. Oral Oncology. 2011 4//;47(4):237-43.

Bissell MJ, Labarge MA. Context, tissue plasticity, and cancer: are tumor stem cells also regulated by the microenvironment? Cancer cell. 2005 Jan;7(1):17-23.

Morrison SJ, Spradling AC. Stem Cells and Niches: Mechanisms That Promote Stem Cell Maintenance throughout Life. Cell.132(4):598-611.

Günthert U, Hofmann M, Rudy W, Reber S, Zöller M, Hauβmann I, et al. A new variant of glycoprotein CD44 confers metastatic potential to rat carcinoma cells. Cell.65(1):13-24.

Shakib K, Schrattenholz A, Soskic V. Stem cells in head and neck squamous cell carcinoma. British Journal of Oral and Maxillofacial Surgery. 2011 10//;49(7):503-6.

Ding X-w, Wu J-h, Jiang C-p. ABCG2: A potential marker of stem cells and novel target in stem cell and cancer therapy. Life Sciences. 2010 4/24/;86(17–18):631-7.

Szafarowski T, Szczepanski MJ. Cancer stem cells in head and neck squamous cell carcinoma. Otolaryngologia polska The Polish otolaryngology. 2014;68(3):105-11.

Atena M, Reza AM, Mehran G. A Review on the Biology of Cancer Stem Cells. Stem Cell Discovery. 2014;4(04):83.

Kalluri R, Neilson EG. Epithelial-mesenchymal transition and its implications for fibrosis. The Journal of Clinical Investigation. 2003;112(12):1776-84.

Thiery JP. Epithelial-mesenchymal transitions in tumour progression. Nature reviews Cancer. 2002 Jun;2(6):442-54.

Radisky DC, LaBarge MA. Epithelial-mesenchymal transition and the stem cell phenotype. Cell stem cell. 2008 Jun 5;2(6):511-2.

Moreno-Bueno G, Portillo F, Cano A. Transcriptional regulation of cell polarity in EMT and cancer. Oncogene. 0000 //print;27(55):6958-69.

Perl AK, Wilgenbus P, Dahl U, Semb H, Christofori G. A causal role for E-cadherin in the transition from adenoma to carcinoma. Nature. 1998 Mar 12;392(6672):190-3.

Barth P, Schenck zu Schweinsberg T, Ramaswamy A, Moll R. CD34+ fibrocytes, α-smooth muscle antigen-positive myofibroblasts, and CD117 expression in the stroma of invasive squamous cell carcinomas of the oral cavity, pharynx, and larynx. Virchows Archiv. 2004 2004/03/01;444(3):231-4.

Staibano S, Merolla F, Testa D, Iovine R, Mascolo M, Guarino V, et al. OPN//CD44v6 overexpression in laryngeal dysplasia and correlation with clinical outcome. Br J Cancer. 2007 11/06/online;97(11):1545-51.

Folkins C, Man S, Xu P, Shaked Y, Hicklin DJ, Kerbel RS. Anticancer Therapies Combining Antiangiogenic and Tumor Cell Cytotoxic Effects Reduce the Tumor Stem-Like Cell Fraction in Glioma Xenograft Tumors. Cancer Res. 2007 April 15, 2007;67(8):3560-4.

Chiou SH, Yu CC, Huang CY, Lin SC, Liu CJ, Tsai TH, et al. Positive correlations of Oct-4 and Nanog in oral cancer stem-like cells and high-grade oral squamous cell carcinoma. Clinical cancer research : an official journal of the American Association for Cancer Research. 2008 Jul 1;14(13):4085-95.

Yu CC, Chang YC. Enhancement of cancer stem-like and epithelial-mesenchymal transdifferentiation property in oral epithelial cells with long-term nicotine exposure: reversal by targeting SNAIL. Toxicology and applied pharmacology. 2013 Feb 1;266(3):459-69.

Chen YS, Wu MJ, Huang CY, Lin SC, Chuang TH, Yu CC, et al. CD133/Src axis mediates tumor initiating property and epithelial-mesenchymal transition of head and neck cancer. PLoS ONE. 2011;6(11):e28053.

Trapasso S, Allegra E. Role of CD44 as a marker of cancer stem cells in head and neck cancer. Biologics : targets & therapy. 2012;6:379-83.

Joshua B, Kaplan MJ, Doweck I, Pai R, Weissman IL, Prince ME, et al. Frequency of cells expressing CD44, a head and neck cancer stem cell marker: correlation with tumor aggressiveness. Head & neck. 2012 Jan;34(1):42-9.

Chikamatsu K, Takahashi G, Sakakura K, Ferrone S, Masuyama K. Immunoregulatory properties of CD44+ cancer stem-like cells in squamous cell carcinoma of the head and neck. Head & neck. 2011 Feb;33(2):208-15.

Picker LJ, Nakache M, Butcher EC. Monoclonal antibodies to human lymphocyte homing receptors define a novel class of adhesion molecules on diverse cell types. The Journal of cell biology. 1989 Aug;109(2):927-37.

Isacke CM, Yarwood H. The hyaluronan receptor, CD44. The international journal of biochemistry & cell biology. 2002 7//;34(7):718-21.

Huet S, Groux H, Caillou B, Valentin H, Prieur AM, Bernard A. CD44 contributes to T cell activation. Journal of immunology (Baltimore, Md : 1950). 1989 Aug 1;143(3):798-801.

David Naor SBW-D, Muayad A. Zahalka, and Ronit Vogt Sionov. Involvement of CD44, a Molecule with a Thousand Faces, in Cancer Dissemination. In: Stern R, editor. Hyaluronan in Cancer Biology: Elsevier Science; 2009. p. 127-46.

Franzmann EJ, Reategui EP, Pedroso F, Pernas FG, Karakullukcu BM, Carraway KL, et al. Soluble CD44 is a potential marker for the early detection of head and neck cancer. Cancer epidemiology, biomarkers & prevention : a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology. 2007 Jul;16(7):1348-55.

Wang SJ, Bourguignon LY. Role of hyaluronan-mediated CD44 signaling in head and neck squamous cell carcinoma progression and chemoresistance. The American journal of pathology. 2011 Mar;178(3):956-63.

Jalkanen S, Wu N, Bargatze RF, Butcher EC. Human lymphocyte and lymphoma homing receptors. Annu Rev Med. 1987;38:467-76.

Ioachim E, Assimakopoulos D, Goussia AC, Peschos D, Skevas A, Agnantis NJ. Glycoprotein CD44 expression in benign, premalignant and malignant epithelial lesions of the larynx: an immunohistochemical study including correlation with Rb, p53, Ki-67 and PCNA. Histology and histopathology. 1999 Oct;14(4):1113-8.

Hirvikoski P, Tammi R, Kumpulainen E, Virtaniemi J, Parkkinen JJ, Tammi M, et al. Irregular expression of hyaluronan and its CD44 receptor is associated with metastatic phenotype in laryngeal squamous cell carcinoma. Virchows Archiv. 1999 Jan;434(1):37-44.

Allegra E, Trapasso S, Sacco A, Aragona T, Belfiore A, Garozzo A. ELISA detection of salivary levels of Cd44sol as a diagnostic test for laryngeal carcinomas. J Cancer Sci Ther. 2012;4:330-4.

Dall P, Heider KH, Hekele A, von Minckwitz G, Kaufmann M, Ponta H, et al. Surface protein expression and messenger RNA-splicing analysis of CD44 in uterine cervical cancer and normal cervical epithelium. Cancer Res. 1994 Jul 1;54(13):3337-41.

Guo YJ, Liu G, Wang X, Jin D, Wu M, Ma J, et al. Potential use of soluble CD44 in serum as indicator of tumor burden and metastasis in patients with gastric or colon cancer. Cancer Res. 1994 Jan 15;54(2):422-6.

Naor D, Nedvetzki S, Golan I, Melnik L, Faitelson Y. CD44 in cancer. Critical reviews in clinical laboratory sciences. 2002 Nov;39(6):527-79.

Wulfkuhle JD, Liotta LA, Petricoin EF. Proteomic applications for the early detection of cancer. Nature reviews Cancer. 2003 Apr;3(4):267-75.

Kawano T, Yanoma S, Nakamura Y, Ozeki A, Kokatsu T, Kubota A, et al. Soluble CD44 standard, CD44 variant 5 and CD44 variant 6 and their relation to staging in head and neck cancer. Acta Otolaryngol. 2005 Apr;125(4):392-7.

Franzmann EJ, Reategui EP, Pereira LHM, Pedroso F, Joseph D, Allen GO, et al. Salivary protein and solCD44 levels as a potential screening tool for early detection of head and neck squamous cell carcinoma. Head & neck. 2012;34(5):687-95.

Warnakulasuriya S. Global epidemiology of oral and oropharyngeal cancer. Oral Oncology. 2009;45(4):309-16.

Ahmad AS, Ormiston-Smith N, Sasieni PD. Trends in the lifetime risk of developing cancer in Great Britain: comparison of risk for those born from 1930 to 1960. Br J Cancer. 2015;112(5):943-7.

Sharma D, Singh G. Squamous cell carcinoma of the oral cavity and oropharynx in young adults. Indian Journal of Cancer. 2016;53(3):399.

Torre LA, Bray F, Siegel RL, Ferlay J, Lortet-Tieulent J, Jemal A. Global cancer statistics, 2012. CA Cancer J Clin. 2015;65(2):87-108.

Patel SC, Carpenter WR, Tyree S, Couch ME, Weissler M, Hackman T, et al. Increasing incidence of oral tongue squamous cell carcinoma in young white women, age 18 to 44 years. J Clin Oncol. 2011 Apr 10;29(11):1488-94.

Ferlay J, Shin H-R, Bray F, Forman D, Mathers C, Parkin DM. Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. International Journal of Cancer. 2010;127(12):2893-917.

Chaturvedi AK, Engels EA, Anderson WF, Gillison ML. Incidence trends for human papillomavirus-related and -unrelated oral squamous cell carcinomas in the United States. J Clin Oncol. 2008 Feb 1;26(4):612-9.

Guimaraes EP, de Carli ML, Sperandio FF, Hanemann JA, Pereira AA. Cyclin D1 and Ki-67 expression correlates to tumor staging in tongue squamous cell carcinoma. Med Oral Patol Oral Cir Bucal. 2015 Nov 01;20(6):e657-63.

Effiom OA, Adeyemo WL, Omitola OG, Ajayi OF, Emmanuel MM, Gbotolorun OM. Oral squamous cell carcinoma: a clinicopathologic review of 233 cases in Lagos, Nigeria. J Oral Maxillofac Surg. 2008 Aug;66(8):1595-9.

Chen J, Zhou J, Lu J, Xiong H, Shi X, Gong L. Significance of CD44 expression in head and neck cancer: a systemic review and meta-analysis. BMC cancer. 2014;14:15.

Lingala S, Cui YY, Chen X, Ruebner BH, Qian XF, Zern MA, et al. Immunohistochemical staining of cancer stem cell markers in hepatocellular carcinoma. Exp Mol Pathol. 2010 Aug;89(1):27-35.

Kokko LL, Hurme S, Maula SM, Alanen K, Grenman R, Kinnunen I, et al. Significance of site-specific prognosis of cancer stem cell marker CD44 in head and neck squamous-cell carcinoma. Oral Oncol. 2011 Jun;47(6):510-6.

Lindquist D, Ahrlund-Richter A, Tarjan M, Tot T, Dalianis T. Intense CD44 expression is a negative prognostic factor in tonsillar and base of tongue cancer. Anticancer Res. 2012 Jan;32(1):153-61.

Kanke M, Fujii M, Kameyama K, Kanzaki J, Tokumaru Y, Imanishi Y, et al. Role of CD44 variant exon 6 in invasion of head and neck squamous cell carcinoma. Archives of otolaryngology--head & neck surgery. 2000 Oct;126(10):1217-23.

Maula SM, Luukkaa M, Grenman R, Jackson D, Jalkanen S, Ristamaki R. Intratumoral lymphatics are essential for the metastatic spread and prognosis in squamous cell carcinomas of the head and neck region. Cancer Res. 2003 Apr 15;63(8):1920-6.

Chen YW, Chen KH, Huang PI, Chen YC, Chiou GY, Lo WL, et al. Cucurbitacin I suppressed stem-like property and enhanced radiation-induced apoptosis in head and neck squamous carcinoma--derived CD44(+)ALDH1(+) cells. Mol Cancer Ther. 2010 Nov;9(11):2879-92.

Ghuwalewala S, Ghatak D, Das P, Dey S, Sarkar S, Alam N, et al. CD44 high CD24 low molecular signature determines the Cancer Stem Cell and EMT phenotype in Oral Squamous Cell Carcinoma. Stem Cell Research. 2016;16(2):405-17.

de Andrade NP, Rodrigues MFSD, Rodini CO, Nunes FD. Cancer stem cell, cytokeratins and epithelial to mesenchymal transition markers expression in oral squamous cell carcinoma derived from ortothopic xenoimplantation of CD44 high cells. Pathology-Research and Practice. 2016.

Ohkoshi E, Umemura N. Induced overexpression of CD44 associated with resistance to apoptosis on DNA damage response in human head and neck squamous cell carcinoma cells. International Journal of Oncology. 2017;50(2):387-95.

Baschnagel A, Tonlaar N, Wilson G, Williams L, Eskandari M. The Relationship Between CD44, EGFR, and c-MET Expression in Patients With Locally Advanced p16-Positive and p16-Negative Head and Neck Squamous Cell Carcinoma. International Journal of Radiation Oncology• Biology• Physics. 2016;94(4):938.

Dunkel J, Vaittinen S, Koivunen P, Laranne J, Mäkinen MJ, Tommola S, et al. Tumoral Expression of CD44 and HIF1α Predict Stage I Oral Cavity Squamous Cell Carcinoma Outcome. Laryngoscope Investigative Otolaryngology. 2016.

Faber A, Barth C, Hormann K, Kassner S, Schultz JD, Sommer U, et al. CD44 as a stem cell marker in head and neck squamous cell carcinoma. Oncology reports. 2011 Aug;26(2):321-6.

Han J, Kioi M, Chu WS, Kasperbauer JL, Strome SE, Puri RK. Identification of potential therapeutic targets in human head & neck squamous cell carcinoma. Head & neck oncology. 2009;1:27.

Pries R, Witrkopf N, Trenkle T, Nitsch SM, Wollenberg B. Potential stem cell marker CD44 is constitutively expressed in permanent cell lines of head and neck cancer. In vivo (Athens, Greece). 2008 Jan-Feb;22(1):89-92.

Campos MS, Neiva KG, Meyers KA, Krishnamurthy S, Nor JE. Endothelial derived factors inhibit anoikis of head and neck cancer stem cells. Oral Oncol. 2012 Jan;48(1):26-32.

Soave DF, Oliveira da Costa JP, da Silveira GG, Ianez RC, de Oliveira LR, Lourenco SV, et al. CD44/CD24 immunophenotypes on clinicopathologic features of salivary glands malignant neoplasms. Diagn Pathol. 2013;8:29.

Oh SY, Kang HJ, Kim YS, Kim H, Lim YC. CD44-negative cells in head and neck squamous carcinoma also have stem-cell like traits. European journal of cancer (Oxford, England : 1990). 2013 Jan;49(1):272-80.

Bloor BK, Rajarajan A, Jaafary-Haghighat K, Odell EW. Transcription and expression of CD44 variant exons by oro-pharyngeal squamous cell carcinomas. Int J Oncol. 2002 Oct;21(4):907-13.

Saito H, Tsujitani S, Katano K, Ikeguchi M, Maeta M, Kaibara N. Serum concentration of CD44 variant 6 and its relation to prognosis in patients with gastric carcinoma. Cancer. 1998 Sep 15;83(6):1094-101.

Van Hal NL, Van Dongen GA, Ten Brink CB, Heider KH, Rech-Weichselbraun I, Snow GB, et al. Evaluation of soluble CD44v6 as a potential serum marker for head and neck squamous cell carcinoma. Clinical cancer research : an official journal of the American Association for Cancer Research. 1999 Nov;5(11):3534-41.

Harn H-J, Ho L-I, Shyu R-Y, Yuan J-S, Lin F-G, Young T-H, et al. Soluble CD44 Isoforms in Serum as Potential Markers of Metastatic Gastric Carcinoma. Journal of Clinical Gastroenterology. 1996;22(2):107-10.

Amirghofran Z, Jalali SA, Hosseini SV, Vasei M, Sabayan B, Ghaderi A. Evaluation of CD44 and CD44v6 in colorectal carcinoma patients: soluble forms in relation to tumor tissue expression and metastasis. Journal of gastrointestinal cancer. 2008;39(1-4):73-8.

SHEEN-CHEN S-M, HUANG C-Y, CHAN Y-C, TSAI C-H, CHI S-Y, WU S-C, et al. An Evaluation of Focal Adhesion Kinase in Breast Cancer by Tissue Microarrays. Anticancer Res. 2013 March 1, 2013;33(3):1169-73.

Franzmann EJ, Lokeshwar VB. Biomarkers for detection and diagnosis of head and neck squamous cell carcinoma. Google Patents; 2016.

Patel S, Shah K, Mirza S, Shah K, Rawal R. Circulating tumor stem like cells in oral squamous cell carcinoma: An unresolved paradox. Oral Oncology. 2016;62:139-46.

Lin JT, Chang TH, Chang CS, Wang WH, Su BW, Lee KD, et al. Prognostic value of pretreatment CD44 mRNA in peripheral blood of patients with locally advanced head and neck cancer. Oral Oncol. 2010 May;46(5):e29-33.

Franzmann EJ, Reategui EP, Carraway KL, Hamilton KL, Weed DT, Goodwin WJ. Salivary soluble CD44: a potential molecular marker for head and neck cancer. Cancer epidemiology, biomarkers & prevention : a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology. 2005 Mar;14(3):735-9.

Pereira LH, Adebisi IN, Perez A, Wiebel M, Reis I, Duncan R, et al. Salivary markers and risk factor data: a multivariate modeling approach for head and neck squamous cell carcinoma detection. Cancer Biomark. 2011;10(5):241-9.

Herold-Mende C, Seiter S, Born AI, Patzelt E, Schupp M, Zoller J, et al. Expression of CD44 splice variants in squamous epithelia and squamous cell carcinomas of the head and neck. J Pathol. 1996 May;179(1):66-73.

Yuce I, Bayram A, Cagli S, Canoz O, Bayram S, Guney E. The role of CD44 and matrix metalloproteinase-9 expression in predicting neck metastasis of supraglottic laryngeal carcinoma. Am J Otolaryngol. 2011 Mar-Apr;32(2):141-6.

Lein M, Jung K, Weiss S, Schnorr D, Loening S. Soluble CD44 variants in the serum of patients with urological malignancies. Oncology. 1997;54(3):226-30.

Molica S, Vitelli G, Levato D, Giannarelli D, Gandolfo GM. Elevated serum levels of soluble CD44 can identify a subgroup of patients with early B-cell chronic lymphocytic leukemia who are at high risk of disease progression. Cancer. 2001 Aug 15;92(4):713-9.

Hoffman RM. ACP Journal Club. Periodic PSA-based screening in men 55 to 69 years of age reduced prostate cancer mortality. Ann Intern Med. 2012 Jul 17;157(2):JC2-4.

Chen H, Shu HM, Chang ZL, Wang ZF, Yao HH, Zhu HM, et al. Efficacy of Pap test in combination with ThinPrep cytological test in screening for cervical cancer. Asian Pacific journal of cancer prevention : APJCP. 2012;13(4):1651-5.




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