Spandidos Publications Logo
  • About
    • About Spandidos
    • Aims and Scopes
    • Abstracting and Indexing
    • Editorial Policies
    • Reprints and Permissions
    • Job Opportunities
    • Terms and Conditions
    • Contact
  • Journals
    • All Journals
    • Oncology Letters
      • Oncology Letters
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Oncology
      • International Journal of Oncology
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Molecular and Clinical Oncology
      • Molecular and Clinical Oncology
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Experimental and Therapeutic Medicine
      • Experimental and Therapeutic Medicine
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Molecular Medicine
      • International Journal of Molecular Medicine
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Biomedical Reports
      • Biomedical Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Oncology Reports
      • Oncology Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Molecular Medicine Reports
      • Molecular Medicine Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • World Academy of Sciences Journal
      • World Academy of Sciences Journal
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Functional Nutrition
      • International Journal of Functional Nutrition
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Epigenetics
      • International Journal of Epigenetics
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Medicine International
      • Medicine International
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
  • Articles
  • Information
    • Information for Authors
    • Information for Reviewers
    • Information for Librarians
    • Information for Advertisers
    • Conferences
  • Language Editing
Spandidos Publications Logo
  • About
    • About Spandidos
    • Aims and Scopes
    • Abstracting and Indexing
    • Editorial Policies
    • Reprints and Permissions
    • Job Opportunities
    • Terms and Conditions
    • Contact
  • Journals
    • All Journals
    • Biomedical Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Experimental and Therapeutic Medicine
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Epigenetics
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Functional Nutrition
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Molecular Medicine
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Oncology
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Medicine International
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Molecular and Clinical Oncology
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Molecular Medicine Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Oncology Letters
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Oncology Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • World Academy of Sciences Journal
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
  • Articles
  • Information
    • For Authors
    • For Reviewers
    • For Librarians
    • For Advertisers
    • Conferences
  • Language Editing
Login Register Submit
  • This site uses cookies
  • You can change your cookie settings at any time by following the instructions in our Cookie Policy. To find out more, you may read our Privacy Policy.

    I agree
Search articles by DOI, keyword, author or affiliation
Search
Advanced Search
presentation
Molecular Medicine Reports
Join Editorial Board Propose a Special Issue
Print ISSN: 1791-2997 Online ISSN: 1791-3004
Journal Cover
November 2012 Volume 6 Issue 5

Full Size Image

Sign up for eToc alerts
Recommend to Library

Journals

International Journal of Molecular Medicine

International Journal of Molecular Medicine

International Journal of Molecular Medicine is an international journal devoted to molecular mechanisms of human disease.

International Journal of Oncology

International Journal of Oncology

International Journal of Oncology is an international journal devoted to oncology research and cancer treatment.

Molecular Medicine Reports

Molecular Medicine Reports

Covers molecular medicine topics such as pharmacology, pathology, genetics, neuroscience, infectious diseases, molecular cardiology, and molecular surgery.

Oncology Reports

Oncology Reports

Oncology Reports is an international journal devoted to fundamental and applied research in Oncology.

Experimental and Therapeutic Medicine

Experimental and Therapeutic Medicine

Experimental and Therapeutic Medicine is an international journal devoted to laboratory and clinical medicine.

Oncology Letters

Oncology Letters

Oncology Letters is an international journal devoted to Experimental and Clinical Oncology.

Biomedical Reports

Biomedical Reports

Explores a wide range of biological and medical fields, including pharmacology, genetics, microbiology, neuroscience, and molecular cardiology.

Molecular and Clinical Oncology

Molecular and Clinical Oncology

International journal addressing all aspects of oncology research, from tumorigenesis and oncogenes to chemotherapy and metastasis.

World Academy of Sciences Journal

World Academy of Sciences Journal

Multidisciplinary open-access journal spanning biochemistry, genetics, neuroscience, environmental health, and synthetic biology.

International Journal of Functional Nutrition

International Journal of Functional Nutrition

Open-access journal combining biochemistry, pharmacology, immunology, and genetics to advance health through functional nutrition.

International Journal of Epigenetics

International Journal of Epigenetics

Publishes open-access research on using epigenetics to advance understanding and treatment of human disease.

Medicine International

Medicine International

An International Open Access Journal Devoted to General Medicine.

Journal Cover
November 2012 Volume 6 Issue 5

Full Size Image

Sign up for eToc alerts
Recommend to Library

  • Article
  • Citations
    • Cite This Article
    • Download Citation
    • Create Citation Alert
    • Remove Citation Alert
    • Cited By
  • Similar Articles
    • Related Articles (in Spandidos Publications)
    • Similar Articles (Google Scholar)
    • Similar Articles (PubMed)
  • Download PDF
  • Download XML
  • View XML
Article Open Access

Tumor budding is a significant indicator of a poor prognosis in lung squamous cell carcinoma patients

  • Authors:
    • Ryota Masuda
    • Hiroshi Kijima
    • Naoko Imamura
    • Naohiro Aruga
    • Yusuke  Nakamura
    • Daisuke Masuda
    • Haruka Takeichi
    • Nobusuke Kato
    • Tomoki  Nakagawa
    • Makiko Tanaka
    • Sadaki Inokuchi
    • Masayuki Iwazaki
  • View Affiliations / Copyright

    Affiliations: Department of General Thoracic Surgery, Tokai University School of Medicine, Isehara, Kanagawa 259-1193, Japan, Department of Pathology and Bioscience, Hirosaki University Graduate School of Medicine, Hirosaki, Aomori 036-8562, Japan, Department of Critical Care and Emergency Medicine, Tokai University School of Medicine, Isehara, Kanagawa 259-1193, Japan
    Copyright: © Masuda et al. This is an open access article distributed under the terms of Creative Commons Attribution License [CC BY_NC 3.0].
  • Pages: 937-943
    |
    Published online on: August 27, 2012
       https://doi.org/10.3892/mmr.2012.1048
  • Expand metrics +
Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )
Metrics: Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )
Cited By (CrossRef): 0 citations Loading Articles...

This article is mentioned in:



Abstract

Lung cancer is a leading cause of cancer mortality worldwide and patients occasionally develop local recurrence or distant metastasis soon after curative resection. Reports of new therapeutic strategies for lung squamous cell carcinoma (SqCC) are extremely rare, while selective anticancer therapy has been reported for lung adenocarcinoma. The aim of this study was to identify clinicopathological prognostic factors for SqCC. We analyzed tumor budding and infiltrative patterns (INF) in 103 cases of surgically-resected SqCC. Tumor infiltrative patterns were classified into three groups (INFa, b and c) and INFc was infiltrative growth at the tumor invasive front. The cases with an INFc component [INFc(+)]were significantly associated with venous invasion (P=0.014) and the scirrhous stromal type (P<0.001). The overall survival rate of patients with INFc(+) was significantly lower than that of patients without the INFc component [INFc(-); P=0.003]. Tumor budding was defined as a single cancer cell or a small nest of up to four cancer cells within stromal tissue. The cases with tumor budding [Bud(+)] were significantly associated with lymph node metastasis (P=0.001), lymphatic invasion (P=0.002), INFc(+) (P<0.001) and the scirrhous stromal type (P=0.014). Patients with the Bud(+) type had a lower overall survival rate than patients with the Bud(-) type (P<0.001). Multivariate analysis demonstrated that tumor budding [hazard ratio (HR), 2.766; 95% confidence interval (CI), 1.497-5.109] and lymph node metastasis (HR, 1.937; 95% CI, 1.097-3.419) were independent predictors of mortality. In conclusion, tumor budding is a significant indicator of a high malignant potential and poor prognosis in SqCC of the lung.
View Figures

Figure 1

Figure 2

Figure 3

Figure 4

View References

1 

Ferlay J, Shin HR, Bray F, Forman D, Mathers C and Parkin DM: Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int J Cancer. 127:2893–2917. 2010. View Article : Google Scholar : PubMed/NCBI

2 

Beadsmoore CJ and Screation NJ: Classification, staging and prognosis of lung cancer. Eur J Radiol. 45:8–17. 2003. View Article : Google Scholar : PubMed/NCBI

3 

Goldstraw P, Crowley J, Chansky KJ, et al: The IASLC Lung Cancer Staging Project: proposals for the revision of the TNM stage groupings in the forthcoming (seventh) edition of the TNM classification of malignant tumours. Thorac Oncol. 2:706–714. 2007. View Article : Google Scholar

4 

Marchesani W: Über den primären Bronchialkrebs. Frankf Z Path. 30:158–190. 1924.(In German).

5 

Kayser K, Bauer A, David H and Kayser G: Historical aspects of pulmonary pathology with specific emphasis on ancient reports. Electronic Journal of Pathology and Histology. 9.2:32–37. 2003.

6 

Travis WD, Brambilla E, Müller-Hermelin HK and Harris CC; World Health Organization Classification of Tumours. Pathology and Genetics. Tumours of the Lung, Pleura, Thymus and Heart. IARC Press; Lyon: 2004

7 

Hong J, Kyung SY, Lee SP, et al: Pemetrexed versus gefitinib versus erlotinib in previously treated patients with non-small cell lung cancer. Korean J Intern Med. 25:294–300. 2010. View Article : Google Scholar : PubMed/NCBI

8 

Rossi A, Ricciardi S, Maione P, de Marinis F and Gridelli C: Pemetrexed in the treatment of advanced non-squamous lung cancer. Lung Cancer. 66:141–149. 2009. View Article : Google Scholar : PubMed/NCBI

9 

Sandler A, Gray R, Perry MC, et al: Paclitaxel-carboplatin alone or with bevacizumab for non-small-cell lung cancer. N Engl J Med. 355:2542–2550. 2006. View Article : Google Scholar : PubMed/NCBI

10 

Reck M, von Pawel J, Zatloukal P, et al: Phase III trial of cisplatin plus gemcitabine with either placebo or bevacizumab as first-line therapy for nonsquamous non-small-cell lung cancer: AVAil. J Clin Oncol. 27:1227–1234. 2009. View Article : Google Scholar : PubMed/NCBI

11 

Rosell R, Perez-Roca L, Sanchez JJ, et al: Customized treatment in non-small-cell lung cancer based on EGFR mutations and BRCA1 mRNA expression. PLoS One. 4:e51332009. View Article : Google Scholar : PubMed/NCBI

12 

Okada K, Kijima H, Imaizumi T, et al: Wall-invasion pattern correlates with survival of patients with gallbladder adenocarcinoma. Anticancer Res. 29:685–691. 2009.PubMed/NCBI

13 

Song KY, Hur H, Jung CK, et al: Impact of tumor infiltration pattern into the surrounding tissue on prognosis of the subserosal gastric cancer (pT2b). Eur J Surg Oncol. 36:563–567. 2010. View Article : Google Scholar : PubMed/NCBI

14 

Kong KY, Park JY, Kim DY, et al: Prognostic significance of stromal microinvasion in the intestinal type of ovarian mucinous adenocarcinoma. Ann Surg Oncol. 18:3462–3468. 2011. View Article : Google Scholar : PubMed/NCBI

15 

Morodomi T, Isomoto H, Shirouzu K, Kakegawa K, Irie K and Morimatsu M: An index for estimating the probability of lymph node metastasis in rectal cancers. Lymph node metastasis and the histopathology of actively invasive regions of cancer. Cancer. 63:539–543. 1989. View Article : Google Scholar : PubMed/NCBI

16 

Ueno H, Murphy J, Jass JR, Mochizuki H and Talbot IC: Tumour ‘budding’ as an index to estimate the potential of aggressiveness in rectal cancer. Histopathology. 40:127–132. 2002.

17 

Nakanishi Y, Ohara M, Doumen H, Kimura N, Ishidate T and Kondo S: Correlation between tumor budding and post-resection prognosis in patients with invasive squamous cell carcinoma of the thoracic esophagus. World J Surg. 35:349–356. 2011. View Article : Google Scholar : PubMed/NCBI

18 

Ohike N, Coban I, Kim GE, et al: Tumor budding as a strong prognostic indicator in invasive ampullary adenocarcinomas. Am J Surg Pathol. 34:1417–1424. 2010. View Article : Google Scholar : PubMed/NCBI

19 

Wang C, Huang H, Huang Z, et al: Tumor budding correlates with poor prognosis and epithelial-mesenchymal transition in tongue squamous cell carcinoma. J Oral Pathol Med. 40:545–551. 2011. View Article : Google Scholar : PubMed/NCBI

20 

Sarioglu S, Acara C, Akman FC, et al: Tumor budding as a prognostic marker in laryngeal carcinoma. Pathol Res Pract. 206:88–92. 2010. View Article : Google Scholar : PubMed/NCBI

21 

Yamaguchi Y, Ishii G, Kojima M, et al: Histopathologic features of the tumor budding in adenocarcinoma of the lung: tumor budding as an index to predict the potential aggressiveness. J Thorac Oncol. 5:1361–1368. 2010. View Article : Google Scholar : PubMed/NCBI

22 

Sobin LH, Gospodarowicz MK and Wittekind C: TNM Classification of Malignant Tumors. 7th edition. Wiley; Hoboken, NJ: 2009

23 

Japanese Gastric Cancer Association. Japanese Classification of Gastric Carcinoma - 2nd English Edition. Gastric Cancer. 1:10–24. 1998. View Article : Google Scholar : PubMed/NCBI

24 

Maehara Y, Oshiro T, Adachi Y, Ohno S, Akazawa K and Sugimachi K: Growth pattern and prognosis of gastric cancer invading the subserosa. J Surg Oncol. 55:203–208. 1994. View Article : Google Scholar : PubMed/NCBI

25 

Haraguchi M, Yamamoto M, Saito A, et al: Prognostic value of depth and pattern of stomach wall invasion in patients with an advanced gastric carcinoma. Semin Surg Oncol. 10:125–129. 1994. View Article : Google Scholar : PubMed/NCBI

26 

Hase K, Shatney C, Johnson D, Trollope M and Vierra M: Prognostic value of tumor ‘budding’ in patients with colorectal cancer. Dis Colon Rectum. 36:627–635. 1993.

27 

Maeshima AM, Maeshima A, Asamura H and Matsuno Y: Histologic prognostic factors for small-sized squamous cell carcinomas of the peripheral lung. Lung Cancer. 52:53–58. 2006. View Article : Google Scholar : PubMed/NCBI

28 

Prall F: Tumour budding in colorectal carcinoma. Histopathology. 50:151–162. 2007. View Article : Google Scholar

29 

Shinto E, Tsuda H, Ueno H, et al: Prognostic implication of laminin-5 gamma 2 chain expression in the invasive front of colorectal cancers, disclosed by area-specific four-point tissue microaarays. Lab Invest. 85:257–266. 2005. View Article : Google Scholar : PubMed/NCBI

30 

Moriya Y, Niki T, Yamada T, Matsuno T, Kondo H and Hirohashi S: Increased expression of laminin-5 and its prognostic significance in lung adenocarcinomas of small size. An immunohistochemical analysis of 102 cases. Cancer. 91:1129–1141. 2001. View Article : Google Scholar : PubMed/NCBI

Related Articles

  • Abstract
  • View
  • Download
  • Twitter
Copy and paste a formatted citation
Spandidos Publications style
Masuda R, Kijima H, Imamura N, Aruga N, Nakamura Y, Masuda D, Takeichi H, Kato N, Nakagawa T, Tanaka M, Tanaka M, et al: Tumor budding is a significant indicator of a poor prognosis in lung squamous cell carcinoma patients. Mol Med Rep 6: 937-943, 2012.
APA
Masuda, R., Kijima, H., Imamura, N., Aruga, N., Nakamura, Y., Masuda, D. ... Iwazaki, M. (2012). Tumor budding is a significant indicator of a poor prognosis in lung squamous cell carcinoma patients. Molecular Medicine Reports, 6, 937-943. https://doi.org/10.3892/mmr.2012.1048
MLA
Masuda, R., Kijima, H., Imamura, N., Aruga, N., Nakamura, Y., Masuda, D., Takeichi, H., Kato, N., Nakagawa, T., Tanaka, M., Inokuchi, S., Iwazaki, M."Tumor budding is a significant indicator of a poor prognosis in lung squamous cell carcinoma patients". Molecular Medicine Reports 6.5 (2012): 937-943.
Chicago
Masuda, R., Kijima, H., Imamura, N., Aruga, N., Nakamura, Y., Masuda, D., Takeichi, H., Kato, N., Nakagawa, T., Tanaka, M., Inokuchi, S., Iwazaki, M."Tumor budding is a significant indicator of a poor prognosis in lung squamous cell carcinoma patients". Molecular Medicine Reports 6, no. 5 (2012): 937-943. https://doi.org/10.3892/mmr.2012.1048
Copy and paste a formatted citation
x
Spandidos Publications style
Masuda R, Kijima H, Imamura N, Aruga N, Nakamura Y, Masuda D, Takeichi H, Kato N, Nakagawa T, Tanaka M, Tanaka M, et al: Tumor budding is a significant indicator of a poor prognosis in lung squamous cell carcinoma patients. Mol Med Rep 6: 937-943, 2012.
APA
Masuda, R., Kijima, H., Imamura, N., Aruga, N., Nakamura, Y., Masuda, D. ... Iwazaki, M. (2012). Tumor budding is a significant indicator of a poor prognosis in lung squamous cell carcinoma patients. Molecular Medicine Reports, 6, 937-943. https://doi.org/10.3892/mmr.2012.1048
MLA
Masuda, R., Kijima, H., Imamura, N., Aruga, N., Nakamura, Y., Masuda, D., Takeichi, H., Kato, N., Nakagawa, T., Tanaka, M., Inokuchi, S., Iwazaki, M."Tumor budding is a significant indicator of a poor prognosis in lung squamous cell carcinoma patients". Molecular Medicine Reports 6.5 (2012): 937-943.
Chicago
Masuda, R., Kijima, H., Imamura, N., Aruga, N., Nakamura, Y., Masuda, D., Takeichi, H., Kato, N., Nakagawa, T., Tanaka, M., Inokuchi, S., Iwazaki, M."Tumor budding is a significant indicator of a poor prognosis in lung squamous cell carcinoma patients". Molecular Medicine Reports 6, no. 5 (2012): 937-943. https://doi.org/10.3892/mmr.2012.1048
Follow us
  • Twitter
  • LinkedIn
  • Facebook
About
  • Spandidos Publications
  • Careers
  • Cookie Policy
  • Privacy Policy
How can we help?
  • Help
  • Live Chat
  • Contact
  • Email to our Support Team