Analysis of microRNAs in pancreatic fine-needle aspirates can classify benign and malignant tissues

Anna E. Szafranska, Martina Doleshal, Hayward S. Edmunds, Stuart Gordon, Jutta Luttges, Johanna B. Munding, Richard J. Barth, Edward J. Gutmann, Arief A. Suriawinata, J. Marc Pipas, Andrea Tannapfel, Murray Korc, Stephan A. Hahn, Emmanuel Labourier, Gregory J. Tsongalis

Research output: Contribution to journalArticle

169 Citations (Scopus)

Abstract

BACKGROUND: MicroRNAs (miRNAs) are RNA molecules that are involved in the regulation of many cellular processes, including those related to human cancers. The aim of this study was to determine, as a proof of principle, whether specific candidate miRNAs could be detected in fine-needle aspirate (FNA) biopsies of pancreatic ductal adenocarcinoma (PDAC) and could accurately differentiate malignant from benign pancreatic tissues. METHODS: We used TaqMan® assays to quantify miRNA levels in FNA samples collected in RNARetain (n = 16) and compared the results with a training set consisting of frozen macrodissected pancreatic samples (n = 20). RESULTS: Quantitative reverse-transcription PCR analysis confirmed that miRNA levels are affected in PDAC FNAs and correlate well with the changes observed in the training set of frozen pancreatic samples. Analysis of the amounts produced for a few specific miRNAs enabled identification of PDAC samples. The combination of miR-196a and miR-217 biomarkers further improved the ability to distinguish between healthy tissue, PDAC, and chronic pancreatitis in the training set (P = 8.2 × 10-10), as well as segregate PDAC FNA samples from other FNA samples (P = 1.1 × 10-5). Furthermore, we showed that miR-196a production is likely specific to PDAC cells and that its incidence paralleled the progression of PDAC. CONCLUSIONS: To the best of our knowledge, this study is the first to evaluate the diagnostic potential of miRNAs in a clinical setting and has shown that miRNA analysis of pancreatic FNA biopsy samples can aid in the pathologic evaluation of suspicious cases and may provide a new strategy for improving the diagnosis of pancreatic diseases.

Original languageEnglish (US)
Pages (from-to)1716-1724
Number of pages9
JournalClinical Chemistry
Volume54
Issue number10
DOIs
StatePublished - Oct 1 2008
Externally publishedYes

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MicroRNAs
Needles
Adenocarcinoma
Tissue
Biopsy
Fine Needle Biopsy
Pancreatic Diseases
Chronic Pancreatitis
Biomarkers
Transcription
Reverse Transcription
Assays
RNA
Polymerase Chain Reaction
Molecules
Incidence
Neoplasms

ASJC Scopus subject areas

  • Clinical Biochemistry
  • Biochemistry, medical

Cite this

Szafranska, A. E., Doleshal, M., Edmunds, H. S., Gordon, S., Luttges, J., Munding, J. B., ... Tsongalis, G. J. (2008). Analysis of microRNAs in pancreatic fine-needle aspirates can classify benign and malignant tissues. Clinical Chemistry, 54(10), 1716-1724. https://doi.org/10.1373/clinchem.2008.109603

Analysis of microRNAs in pancreatic fine-needle aspirates can classify benign and malignant tissues. / Szafranska, Anna E.; Doleshal, Martina; Edmunds, Hayward S.; Gordon, Stuart; Luttges, Jutta; Munding, Johanna B.; Barth, Richard J.; Gutmann, Edward J.; Suriawinata, Arief A.; Pipas, J. Marc; Tannapfel, Andrea; Korc, Murray; Hahn, Stephan A.; Labourier, Emmanuel; Tsongalis, Gregory J.

In: Clinical Chemistry, Vol. 54, No. 10, 01.10.2008, p. 1716-1724.

Research output: Contribution to journalArticle

Szafranska, AE, Doleshal, M, Edmunds, HS, Gordon, S, Luttges, J, Munding, JB, Barth, RJ, Gutmann, EJ, Suriawinata, AA, Pipas, JM, Tannapfel, A, Korc, M, Hahn, SA, Labourier, E & Tsongalis, GJ 2008, 'Analysis of microRNAs in pancreatic fine-needle aspirates can classify benign and malignant tissues', Clinical Chemistry, vol. 54, no. 10, pp. 1716-1724. https://doi.org/10.1373/clinchem.2008.109603
Szafranska AE, Doleshal M, Edmunds HS, Gordon S, Luttges J, Munding JB et al. Analysis of microRNAs in pancreatic fine-needle aspirates can classify benign and malignant tissues. Clinical Chemistry. 2008 Oct 1;54(10):1716-1724. https://doi.org/10.1373/clinchem.2008.109603
Szafranska, Anna E. ; Doleshal, Martina ; Edmunds, Hayward S. ; Gordon, Stuart ; Luttges, Jutta ; Munding, Johanna B. ; Barth, Richard J. ; Gutmann, Edward J. ; Suriawinata, Arief A. ; Pipas, J. Marc ; Tannapfel, Andrea ; Korc, Murray ; Hahn, Stephan A. ; Labourier, Emmanuel ; Tsongalis, Gregory J. / Analysis of microRNAs in pancreatic fine-needle aspirates can classify benign and malignant tissues. In: Clinical Chemistry. 2008 ; Vol. 54, No. 10. pp. 1716-1724.
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AU - Szafranska, Anna E.

AU - Doleshal, Martina

AU - Edmunds, Hayward S.

AU - Gordon, Stuart

AU - Luttges, Jutta

AU - Munding, Johanna B.

AU - Barth, Richard J.

AU - Gutmann, Edward J.

AU - Suriawinata, Arief A.

AU - Pipas, J. Marc

AU - Tannapfel, Andrea

AU - Korc, Murray

AU - Hahn, Stephan A.

AU - Labourier, Emmanuel

AU - Tsongalis, Gregory J.

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N2 - BACKGROUND: MicroRNAs (miRNAs) are RNA molecules that are involved in the regulation of many cellular processes, including those related to human cancers. The aim of this study was to determine, as a proof of principle, whether specific candidate miRNAs could be detected in fine-needle aspirate (FNA) biopsies of pancreatic ductal adenocarcinoma (PDAC) and could accurately differentiate malignant from benign pancreatic tissues. METHODS: We used TaqMan® assays to quantify miRNA levels in FNA samples collected in RNARetain (n = 16) and compared the results with a training set consisting of frozen macrodissected pancreatic samples (n = 20). RESULTS: Quantitative reverse-transcription PCR analysis confirmed that miRNA levels are affected in PDAC FNAs and correlate well with the changes observed in the training set of frozen pancreatic samples. Analysis of the amounts produced for a few specific miRNAs enabled identification of PDAC samples. The combination of miR-196a and miR-217 biomarkers further improved the ability to distinguish between healthy tissue, PDAC, and chronic pancreatitis in the training set (P = 8.2 × 10-10), as well as segregate PDAC FNA samples from other FNA samples (P = 1.1 × 10-5). Furthermore, we showed that miR-196a production is likely specific to PDAC cells and that its incidence paralleled the progression of PDAC. CONCLUSIONS: To the best of our knowledge, this study is the first to evaluate the diagnostic potential of miRNAs in a clinical setting and has shown that miRNA analysis of pancreatic FNA biopsy samples can aid in the pathologic evaluation of suspicious cases and may provide a new strategy for improving the diagnosis of pancreatic diseases.

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