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Morphologic features of adenocarcinoma of the lung predictive of response to the epidermal growth factor receptor kinase inhibitors erlotinib and gefitinib

Morphologic features of adenocarcinoma of the lung predictive of response to the epidermal growth factor receptor kinase inhibitors erlotinib and gefitinib

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Morphologic features of adenocarcinoma of the lung predictive of response to the epidermal growth factor receptor kinase inhibitors erlotinib and gefitinib

Maureen F Zakowski et al. Arch Pathol Lab Med. 2009 Mar.

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Abstract

Context: A subset of lung adenocarcinomas appears preferentially sensitive to epidermal growth factor receptor (EGFR) tyrosine kinase inhibitors (TKIs). EGFR-activating mutations and never smoking are associated with response to TKIs.

Objectives: To describe the morphology of adenocarcinomas responsive to TKIs, compare it to tumors in nonresponding patients, and correlate findings with EGFR mutations, gene copy number, and protein expression.

Design: Material from 52 EGFR TKI-treated patients was studied: 29 responders and 23 nonresponders. Adenocarcinoma subtypes and morphologic features were defined in histologic and cytologic material. EGFR mutations were detected by sequencing, copy number by chromogenic in situ hybridization, and expression by immunohistochemistry.

Results: Tumors from TKI responders tended to be better-differentiated adenocarcinomas with bronchioloalveolar carcinoma components. Nonresponders showed more heterogeneous morphology, higher grade, and more subtypes, and were more likely to show solid growth. In nonresponders, the only pure bronchioloalveolar carcinoma was mucinous, a subtype known to be negative for EGFR mutations. Using World Health Organization criteria, all tumors in both groups other than pure bronchioloalveolar carcinomas would be classified as adenocarcinomas, mixed subtype, thereby obscuring some of these distinctions. EGFR mutations were significantly more common in responders (22/29 vs 0/23; P < .001). Immunohistochemistry and chromogenic in situ hybridization results were not significantly correlated with EGFR mutations or response to TKIs in this study.

Conclusions: Overall, histologic differences exist between tumors that respond to TKIs and those that do not, although sampling affects classification, and there is significant histologic overlap between the 2 groups. Response is strongly associated with EGFR mutations.

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Figures

Figure 1

A, An area of bronchioloalveolar…

Figure 1

A, An area of bronchioloalveolar carcinoma (BAC) in a responder. This tumor was…

Figure 1

A, An area of bronchioloalveolar carcinoma (BAC) in a responder. This tumor was from a lobectomy specimen (hematoxylin-eosin, original magnification ×40). B, A focus of adenocarcinoma interpreted as BAC in a small biopsy specimen from a responder. The inset shows the intranuclear inclusions frequently found in BAC (hematoxylin-eosin, original magnifications ×4 and ×100 [inset]).

Figure 2

A focus of micropapillary carcinoma…

Figure 2

A focus of micropapillary carcinoma seen in a nonresponder. This morphology was not…

Figure 2

A focus of micropapillary carcinoma seen in a nonresponder. This morphology was not seen in responders (hematoxylin-eosin, original magnification ×100).

Figure 3

Mixed subtype adenocarcinoma can be…

Figure 3

Mixed subtype adenocarcinoma can be found in both responders and nonresponders. This is…

Figure 3

Mixed subtype adenocarcinoma can be found in both responders and nonresponders. This is from a nonresponder who underwent a wedge resection (hematoxylin-eosin, original magnification ×40).

Figure 4

Increased epidermal growth factor receptor…

Figure 4

Increased epidermal growth factor receptor (EGFR) copy number by chromogenic in situ hybridization…

Figure 4

Increased epidermal growth factor receptor (EGFR) copy number by chromogenic in situ hybridization in a responder. EGFR copy number was high (more than 6), and the specimen was from a wedge resection (original magnification ×40).

Figure 5

Epidermal growth factor receptor immunohistochemical…

Figure 5

Epidermal growth factor receptor immunohistochemical stain scored as 3+ in a responder. The…

Figure 5

Epidermal growth factor receptor immunohistochemical stain scored as 3+ in a responder. The specimen was from a lobectomy (original magnification ×40).

Figure 6

Chromogenic in situ hybridization showing…

Figure 6

Chromogenic in situ hybridization showing epidermal growth factor receptor amplification in case 3,…

Figure 6

Chromogenic in situ hybridization showing epidermal growth factor receptor amplification in case 3, a gefitinib nonresponder. The copy number in this case was 6 (original magnification ×100).

Figure 7

Mucinous bronchioloalveolar carcinoma (BAC) (case…

Figure 7

Mucinous bronchioloalveolar carcinoma (BAC) (case 22) from an erlotinib nonresponder. This tumor was…

Figure 7

Mucinous bronchioloalveolar carcinoma (BAC) (case 22) from an erlotinib nonresponder. This tumor was homogeneous in appearance. Areas of nonmucinous BAC were not identified (hematoxylin-eosin, original magnification ×40).

Figure 8

Papillary component in adenocarcinoma from…

Figure 8

Papillary component in adenocarcinoma from patient 13, an erlotinib nonresponder (hematoxylin-eosin, original magnification…

Figure 8

Papillary component in adenocarcinoma from patient 13, an erlotinib nonresponder (hematoxylin-eosin, original magnification ×40).

Figure 9

Necrosis seen in patient 1,…

Figure 9

Necrosis seen in patient 1, a gefitinib nonresponder. Necrosis was seen in 3…

Figure 9

Necrosis seen in patient 1, a gefitinib nonresponder. Necrosis was seen in 3 nonresponders (hematoxylin-eosin, original magnification ×40).

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    1. Jemal A, Murray T, Ward E, et al. Cancer statistics, 2005. CA Cancer J Clin. 2005;55:10–30. - PubMed
    1. Miller VA, Kris MG, Shah N, et al. Bronchioloalveolar pathologic subtype and smoking history predict sensitivity to gefitinib in advanced non-small-cell lung cancer. J Clin Oncol. 2004;22:1103–1109. - PubMed
    1. Scagliotti GV, Selvaggi G, Novello S, Hirsch FR. The biology of epidermal growth factor receptor in lung cancer. Clin Cancer Res. 2004;10:4227S–4232S. - PubMed
    1. Thatcher N, Chang A, Parikh P, et al. Gefitinib plus best supportive care in previously treated patients with refractory advanced non-small-cell lung cancer: results from a randomised, placebo-controlled, multicentre study (Iressa Survival Evaluation in Lung Cancer) Lancet. 2005;366:1527–1537. - PubMed
    1. Pao W, Miller V, Zakowski M, et al. EGF receptor gene mutations are common in lung cancers from “never smokers” and are associated with sensitivity of tumors to gefitinib and erlotinib. Proc Natl Acad Sci U S A. 2004;101:13306–13311. - PMC - PubMed

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