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Originally published as JCO Early Release 10.1200/JCO.2003.11.069 on September 2 2003

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Journal of Clinical Oncology, Vol 21, Issue 20 (October), 2003: 3798-3807
© 2003 American Society for Clinical Oncology

Epidermal Growth Factor Receptor in Non–Small-Cell Lung Carcinomas: Correlation Between Gene Copy Number and Protein Expression and Impact on Prognosis

Fred R. Hirsch, Marileila Varella-Garcia, Paul A. Bunn, Jr, Michael V. Di Maria, Robert Veve, Roy M. Bremnes, Anna E. Barón, Chan Zeng, Wilbur A. Franklin

From the Departments of Pathology, Medicine, and Preventive Medicine and Biometrics, University of Colorado Health Sciences Center; and the Tobacco Related Malignancy Program, University of Colorado Comprehensive Cancer Center, Denver, CO.

Address reprint requests to Fred R. Hirsch, MD, PhD, Departments of Medicine and Pathology, Campus Box B188, University of Colorado Health Sciences Center, Denver, CO 80262; e-mail: Fred.Hirsch{at}uchsc.edu.

Purpose: The epidermal growth factor receptor (EGFR) is frequently overexpressed in non–small-cell lung carcinoma (NSCLC), and EGFR inhibitors are promising new therapeutic agents. The molecular mechanisms responsible for EGFR overexpression are poorly understood.

Materials and Methods: Gene copy number and protein status of EGFR were investigated in microarrayed tumors from 183 NSCLC patients, including squamous cell carcinoma (SCC; 89 patients) and non-SCC (94 patients) histologies. Protein expression was assessed by immunohistochemistry on a scale from 0 to 400 (percentage of positive cells x staining intensity). Gene and chromosome 7 copy numbers were identified by fluorescent in situ hybridization (FISH).

Results: EGFR protein overexpression was observed in 62% of the NSCLC (25% scored 201 to 300; 37% scored 301 to 400), more frequently in SCC than non-SCC (82% v 44%; P < .001), and in 80% of the bronchioloalveolar carcinomas. The prevalent FISH patterns were balanced disomy (40%) and trisomy (38%) for EGFR gene and chromosome 7 (40%), whereas balanced polysomy was seen in 13% and gene amplification was seen in 9% of the patients. Gene copy number correlated with protein expression (r = 0.4; P < .001). EGFR overexpression or high gene copy numbers had no significant influence on prognosis.

Conclusion: EGFR overexpression is frequent in NSCLC, is most prominent in SCC, and correlates with increased gene copy number per cell. High gene copy numbers per cell showed a trend toward poor prognosis. It will be important to evaluate EGFR gene and EGFR protein status and signal protein expression to properly interpret future clinical trials using EGFR inhibitors.

Supported in part by the National Cancer Institute grants Cancer Center Core Grant 2P30-CA46934, Specialized Program of Research Excellence P01-CA58187, and Early Detection Research Network U01-CA85070. A career development grant was awarded to F.R.H. from the International Association for the Study of Lung Cancer/Cancer Research Foundation of America.


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F. R. Hirsch, M. Varella-Garcia, P. A. Bunn Jr, W. A. Franklin, R. Dziadziuszko, N. Thatcher, A. Chang, P. Parikh, J. R. Pereira, T. Ciuleanu, et al.
Molecular Predictors of Outcome With Gefitinib in a Phase III Placebo-Controlled Study in Advanced Non-Small-Cell Lung Cancer
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C. H. Chung, K. Ely, L. McGavran, M. Varella-Garcia, J. Parker, N. Parker, C. Jarrett, J. Carter, B. A. Murphy, J. Netterville, et al.
Increased Epidermal Growth Factor Receptor Gene Copy Number Is Associated With Poor Prognosis in Head and Neck Squamous Cell Carcinomas
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C-Q Zhu, W Shih, C-H Ling, and M-S Tsao
Immunohistochemical markers of prognosis in non-small cell lung cancer: a review and proposal for a multiphase approach to marker evaluation.
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C. D. Coldren, B. A. Helfrich, S. E. Witta, M. Sugita, R. Lapadat, C. Zeng, A. Baron, W. A. Franklin, F. R. Hirsch, M. W. Geraci, et al.
Baseline Gene Expression Predicts Sensitivity to Gefitinib in Non-Small Cell Lung Cancer Cell Lines
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G. R. Simon, C. R. Garrett, S. C. Olson, M. Langevin, I. A. Eiseman, J. J. Mahany, C. C. Williams, R. Lush, A. Daud, P. Munster, et al.
Increased Bioavailability of Intravenous Versus Oral CI-1033, a Pan erbB Tyrosine Kinase Inhibitor: Results of a Phase I Pharmacokinetic Study
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R. Dziadziuszko, F. R. Hirsch, M. Varella-Garcia, and P. A. Bunn Jr.
Selecting Lung Cancer Patients for Treatment with Epidermal Growth Factor Receptor Tyrosine Kinase Inhibitors by Immunohistochemistry and Fluorescence In situ Hybridization--Why, When, and How?
Clin. Cancer Res., July 15, 2006; 12(14): 4409s - 4415s.
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F. Cappuzzo, L. Toschi, G. Tallini, G. L. Ceresoli, I. Domenichini, S. Bartolini, G. Finocchiaro, E. Magrini, G. Metro, A. Cancellieri, et al.
Insulin-like growth factor receptor 1 (IGFR-1) is significantly associated with longer survival in non-small-cell lung cancer patients treated with gefitinib
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Biological Markers for Non-Small Cell Lung Cancer Patient Selection for Epidermal Growth Factor Receptor Tyrosine Kinase Inhibitor Therapy.
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A. Italiano, F. B. Vandenbos, J. Otto, J. Mouroux, D. Fontaine, P.-Y. Marcy, N. Cardot, A. Thyss, and F. Pedeutour
Comparison of the epidermal growth factor receptor gene and protein in primary non-small-cell-lung cancer and metastatic sites: implications for treatment with EGFR-inhibitors
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Lung adenocarcinomas induced in mice by mutant EGF receptors found in human lung cancers respond to a tyrosine kinase inhibitor or to down-regulation of the receptors
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E. Calvo and J. Baselga
Ethnic Differences in Response to Epidermal Growth Factor Receptor Tyrosine Kinase Inhibitors
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D. T. Merrick, J. Kittelson, R. Winterhalder, G. Kotantoulas, S. Ingeberg, R. L. Keith, T. C. Kennedy, Y. E. Miller, W. A. Franklin, and F. R. Hirsch
Analysis of c-ErbB1/epidermal growth factor receptor and c-ErbB2/HER-2 expression in bronchial dysplasia: evaluation of potential targets for chemoprevention of lung cancer.
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F. R. Hirsch, M. Varella-Garcia, W. A. Franklin, and P. A. Bunn Jr
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Restoring E-Cadherin Expression Increases Sensitivity to Epidermal Growth Factor Receptor Inhibitors in Lung Cancer Cell Lines
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Modern Treatment of Lung Cancer: CASE 1. Amplification and Mutation of the Epidermal Growth Factor Receptor in Metastatic Lung Cancer With Remission From Gefitinib
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F. R. Hirsch, M. Varella-Garcia, J. McCoy, H. West, A. C. Xavier, P. Gumerlock, P. A. Bunn Jr, W. A. Franklin, J. Crowley, and D. R. Gandara
Increased Epidermal Growth Factor Receptor Gene Copy Number Detected by Fluorescence In Situ Hybridization Associates With Increased Sensitivity to Gefitinib in Patients With Bronchioloalveolar Carcinoma Subtypes: A Southwest Oncology Group Study
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Epidermal Growth Factor Receptor Gene Mutations and Increased Copy Numbers Predict Gefitinib Sensitivity in Patients With Recurrent Non-Small-Cell Lung Cancer
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Selecting Patients for Epidermal Growth Factor Receptor Inhibitor Treatment: A FISH Story or a Tale of Mutations?
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Erlotinib in Lung Cancer -- Molecular and Clinical Predictors of Outcome
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Z. Zheng, G. Bepler, A. Cantor, and E. B. Haura
Small Tumor Size and Limited Smoking History Predicts Activated Epidermal Growth Factor Receptor in Early-Stage Non-small Cell Lung Cancer
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Association Between Epidermal Growth Factor Receptor Mutation and Improved Survival in Never-Smokers With Primary Adenocarcinoma of the Lung
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V. A. Miller, F. R. Hirsch, and D. H. Johnson
Systemic Therapy of Advanced Bronchioloalveolar Cell Carcinoma: Challenges and Opportunities
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A Curious Link Between Epidermal Growth Factor Receptor Amplification and Survival: Effect of "Allele Dilution" on Gefitinib Sensitivity?
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G. W. Cole Jr, A. M. Alleva, R. M. Reddy, J. B. Maxhimer, J. Zuo, D. S. Schrump, and D. M. Nguyen
The selective epidermal growth factor receptor tyrosine kinase inhibitor PD153035 suppresses expression of prometastasis phenotypes in malignant pleural mesothelioma cells in vitro
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Changes in Angiogenic Growth Factor Levels After Gefitinib Treatment in Non-small Cell Lung Cancer
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Skin rash and good performance status predict improved survival with gefitinib in patients with advanced non-small cell lung cancer
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J. Baselga and C. L. Arteaga
Critical Update and Emerging Trends in Epidermal Growth Factor Receptor Targeting in Cancer
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R. S. Herbst, D. H. Johnson, E. Mininberg, D. P. Carbone, T. Henderson, E. S. Kim, G. Blumenschein Jr, J. J. Lee, D. D. Liu, M. T. Truong, et al.
Phase I/II Trial Evaluating the Anti-Vascular Endothelial Growth Factor Monoclonal Antibody Bevacizumab in Combination With the HER-1/Epidermal Growth Factor Receptor Tyrosine Kinase Inhibitor Erlotinib for Patients With Recurrent Non-Small-Cell Lung Cancer
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W. Pao and V. A. Miller
Epidermal Growth Factor Receptor Mutations, Small-Molecule Kinase Inhibitors, and Non-Small-Cell Lung Cancer: Current Knowledge and Future Directions
J. Clin. Oncol., April 10, 2005; 23(11): 2556 - 2568.
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K. J. Reichenberger, R. D. Coletta, A. P. Schulte, M. Varella-Garcia, and H. L. Ford
Gene Amplification Is a Mechanism of Six1 Overexpression in Breast Cancer
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S. Dubey and J. H. Schiller
Three Emerging New Drugs for NSCLC: Pemetrexed, Bortezomib, and Cetuximab
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A. J. Dannenberg, S. M. Lippman, J. R. Mann, K. Subbaramaiah, and R. N. DuBois
Cyclooxygenase-2 and Epidermal Growth Factor Receptor: Pharmacologic Targets for Chemoprevention
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