Computer-aided assessment of the extra-cellular matrix during pancreatic carcinogenesis: a pilot study

Fabio Grizzi, Sirio Fiorino, Dorina Qehajaj, Adele Fornelli, Carlo Russo, Dario De Biase, Michele Masetti, Laura Mastrangelo, Matteo Zanello, Raffaele Lombardi, Andrea Domanico, Esterita Accogli, Andrea Tura, Leonardo Mirandola, Maurizio Chiriva-Internati, Robert S. Bresalier, Elio Jovine, Paolo Leandri, Luca Di Tommaso

Research output: Contribution to journalArticleResearchpeer-review

Abstract

Background: A hallmark of pancreatic ductal adenocarcinoma is the desmoplastic reaction, but its impact on the tumor behavior remains controversial. Our aim was to introduce a computer -aided method to precisely quantify the amount of pancreatic collagenic extra-cellular matrix, its spatial distribution pattern, and the degradation process. Methods: A series of normal, inflammatory and neoplastic pancreatic ductal adenocarcinoma formalin-fixed and paraffin-embedded Sirius red stained sections were automatically digitized and analyzed using a computer-aided method. Results: We found a progressive increase of pancreatic collagenic extra-cellular matrix from normal to the inflammatory and pancreatic ductal adenocarcinoma. The two-dimensional fractal dimension showed a significant difference in the collagenic extra-cellular matrix spatial complexity between normal versus inflammatory and pancreatic ductal adenocarcinoma. A significant difference when comparing the number of cycles necessary to degrade the pancreatic collagenic extra-cellular matrix in normal versus inflammatory and pancreatic ductal adenocarcinoma was also found. The difference between inflammatory and pancreatic ductal adenocarcinoma was also significant. Furthermore, the mean velocity of collagenic extra-cellular matrix degradation was found to be faster in inflammatory and pancreatic ductal adenocarcinoma than in normal. Conclusion: These findings demonstrate that inflammatory and pancreatic ductal adenocarcinomas are characterized by an increased amount of pancreatic collagenic extra-cellular matrix and by changes in their spatial complexity and degradation. Our study defines new features about the pancreatic collagenic extra-cellular matrix, and represents a basis for further investigations into the clinical behavior of pancreatic ductal adenocarcinoma and the development of therapeutic strategies.

LanguageEnglish
Article number61
Pages1-9
Number of pages9
JournalJournal of Translational Medicine
Volume17
Issue number1
DOIs
Publication statusPublished - 28 Feb 2019
Externally publishedYes

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Carcinogenesis
Adenocarcinoma
Degradation
Fractal dimension
Fractals
Paraffin
Spatial distribution
Formaldehyde
Tumors
Neoplasms

Bibliographical note

Copyright the Author(s) 2019. Version archived for private and non-commercial use with the permission of the author/s and according to publisher conditions. For further rights please contact the publisher.

Keywords

  • Degradation
  • Extra-cellular matrix
  • Fractals
  • Modeling
  • Pancreatic adenocarcinoma

Cite this

Grizzi, Fabio ; Fiorino, Sirio ; Qehajaj, Dorina ; Fornelli, Adele ; Russo, Carlo ; De Biase, Dario ; Masetti, Michele ; Mastrangelo, Laura ; Zanello, Matteo ; Lombardi, Raffaele ; Domanico, Andrea ; Accogli, Esterita ; Tura, Andrea ; Mirandola, Leonardo ; Chiriva-Internati, Maurizio ; Bresalier, Robert S. ; Jovine, Elio ; Leandri, Paolo ; Di Tommaso, Luca. / Computer-aided assessment of the extra-cellular matrix during pancreatic carcinogenesis : a pilot study. In: Journal of Translational Medicine. 2019 ; Vol. 17, No. 1. pp. 1-9.
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abstract = "Background: A hallmark of pancreatic ductal adenocarcinoma is the desmoplastic reaction, but its impact on the tumor behavior remains controversial. Our aim was to introduce a computer -aided method to precisely quantify the amount of pancreatic collagenic extra-cellular matrix, its spatial distribution pattern, and the degradation process. Methods: A series of normal, inflammatory and neoplastic pancreatic ductal adenocarcinoma formalin-fixed and paraffin-embedded Sirius red stained sections were automatically digitized and analyzed using a computer-aided method. Results: We found a progressive increase of pancreatic collagenic extra-cellular matrix from normal to the inflammatory and pancreatic ductal adenocarcinoma. The two-dimensional fractal dimension showed a significant difference in the collagenic extra-cellular matrix spatial complexity between normal versus inflammatory and pancreatic ductal adenocarcinoma. A significant difference when comparing the number of cycles necessary to degrade the pancreatic collagenic extra-cellular matrix in normal versus inflammatory and pancreatic ductal adenocarcinoma was also found. The difference between inflammatory and pancreatic ductal adenocarcinoma was also significant. Furthermore, the mean velocity of collagenic extra-cellular matrix degradation was found to be faster in inflammatory and pancreatic ductal adenocarcinoma than in normal. Conclusion: These findings demonstrate that inflammatory and pancreatic ductal adenocarcinomas are characterized by an increased amount of pancreatic collagenic extra-cellular matrix and by changes in their spatial complexity and degradation. Our study defines new features about the pancreatic collagenic extra-cellular matrix, and represents a basis for further investigations into the clinical behavior of pancreatic ductal adenocarcinoma and the development of therapeutic strategies.",
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author = "Fabio Grizzi and Sirio Fiorino and Dorina Qehajaj and Adele Fornelli and Carlo Russo and {De Biase}, Dario and Michele Masetti and Laura Mastrangelo and Matteo Zanello and Raffaele Lombardi and Andrea Domanico and Esterita Accogli and Andrea Tura and Leonardo Mirandola and Maurizio Chiriva-Internati and Bresalier, {Robert S.} and Elio Jovine and Paolo Leandri and {Di Tommaso}, Luca",
note = "Copyright the Author(s) 2019. Version archived for private and non-commercial use with the permission of the author/s and according to publisher conditions. For further rights please contact the publisher.",
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Grizzi, F, Fiorino, S, Qehajaj, D, Fornelli, A, Russo, C, De Biase, D, Masetti, M, Mastrangelo, L, Zanello, M, Lombardi, R, Domanico, A, Accogli, E, Tura, A, Mirandola, L, Chiriva-Internati, M, Bresalier, RS, Jovine, E, Leandri, P & Di Tommaso, L 2019, 'Computer-aided assessment of the extra-cellular matrix during pancreatic carcinogenesis: a pilot study', Journal of Translational Medicine, vol. 17, no. 1, 61, pp. 1-9. https://doi.org/10.1186/s12967-019-1817-3

Computer-aided assessment of the extra-cellular matrix during pancreatic carcinogenesis : a pilot study. / Grizzi, Fabio; Fiorino, Sirio; Qehajaj, Dorina; Fornelli, Adele; Russo, Carlo; De Biase, Dario; Masetti, Michele; Mastrangelo, Laura; Zanello, Matteo; Lombardi, Raffaele; Domanico, Andrea; Accogli, Esterita; Tura, Andrea; Mirandola, Leonardo; Chiriva-Internati, Maurizio; Bresalier, Robert S.; Jovine, Elio; Leandri, Paolo; Di Tommaso, Luca.

In: Journal of Translational Medicine, Vol. 17, No. 1, 61, 28.02.2019, p. 1-9.

Research output: Contribution to journalArticleResearchpeer-review

TY - JOUR

T1 - Computer-aided assessment of the extra-cellular matrix during pancreatic carcinogenesis

T2 - Journal of Translational Medicine

AU - Grizzi, Fabio

AU - Fiorino, Sirio

AU - Qehajaj, Dorina

AU - Fornelli, Adele

AU - Russo, Carlo

AU - De Biase, Dario

AU - Masetti, Michele

AU - Mastrangelo, Laura

AU - Zanello, Matteo

AU - Lombardi, Raffaele

AU - Domanico, Andrea

AU - Accogli, Esterita

AU - Tura, Andrea

AU - Mirandola, Leonardo

AU - Chiriva-Internati, Maurizio

AU - Bresalier, Robert S.

AU - Jovine, Elio

AU - Leandri, Paolo

AU - Di Tommaso, Luca

N1 - Copyright the Author(s) 2019. Version archived for private and non-commercial use with the permission of the author/s and according to publisher conditions. For further rights please contact the publisher.

PY - 2019/2/28

Y1 - 2019/2/28

N2 - Background: A hallmark of pancreatic ductal adenocarcinoma is the desmoplastic reaction, but its impact on the tumor behavior remains controversial. Our aim was to introduce a computer -aided method to precisely quantify the amount of pancreatic collagenic extra-cellular matrix, its spatial distribution pattern, and the degradation process. Methods: A series of normal, inflammatory and neoplastic pancreatic ductal adenocarcinoma formalin-fixed and paraffin-embedded Sirius red stained sections were automatically digitized and analyzed using a computer-aided method. Results: We found a progressive increase of pancreatic collagenic extra-cellular matrix from normal to the inflammatory and pancreatic ductal adenocarcinoma. The two-dimensional fractal dimension showed a significant difference in the collagenic extra-cellular matrix spatial complexity between normal versus inflammatory and pancreatic ductal adenocarcinoma. A significant difference when comparing the number of cycles necessary to degrade the pancreatic collagenic extra-cellular matrix in normal versus inflammatory and pancreatic ductal adenocarcinoma was also found. The difference between inflammatory and pancreatic ductal adenocarcinoma was also significant. Furthermore, the mean velocity of collagenic extra-cellular matrix degradation was found to be faster in inflammatory and pancreatic ductal adenocarcinoma than in normal. Conclusion: These findings demonstrate that inflammatory and pancreatic ductal adenocarcinomas are characterized by an increased amount of pancreatic collagenic extra-cellular matrix and by changes in their spatial complexity and degradation. Our study defines new features about the pancreatic collagenic extra-cellular matrix, and represents a basis for further investigations into the clinical behavior of pancreatic ductal adenocarcinoma and the development of therapeutic strategies.

AB - Background: A hallmark of pancreatic ductal adenocarcinoma is the desmoplastic reaction, but its impact on the tumor behavior remains controversial. Our aim was to introduce a computer -aided method to precisely quantify the amount of pancreatic collagenic extra-cellular matrix, its spatial distribution pattern, and the degradation process. Methods: A series of normal, inflammatory and neoplastic pancreatic ductal adenocarcinoma formalin-fixed and paraffin-embedded Sirius red stained sections were automatically digitized and analyzed using a computer-aided method. Results: We found a progressive increase of pancreatic collagenic extra-cellular matrix from normal to the inflammatory and pancreatic ductal adenocarcinoma. The two-dimensional fractal dimension showed a significant difference in the collagenic extra-cellular matrix spatial complexity between normal versus inflammatory and pancreatic ductal adenocarcinoma. A significant difference when comparing the number of cycles necessary to degrade the pancreatic collagenic extra-cellular matrix in normal versus inflammatory and pancreatic ductal adenocarcinoma was also found. The difference between inflammatory and pancreatic ductal adenocarcinoma was also significant. Furthermore, the mean velocity of collagenic extra-cellular matrix degradation was found to be faster in inflammatory and pancreatic ductal adenocarcinoma than in normal. Conclusion: These findings demonstrate that inflammatory and pancreatic ductal adenocarcinomas are characterized by an increased amount of pancreatic collagenic extra-cellular matrix and by changes in their spatial complexity and degradation. Our study defines new features about the pancreatic collagenic extra-cellular matrix, and represents a basis for further investigations into the clinical behavior of pancreatic ductal adenocarcinoma and the development of therapeutic strategies.

KW - Degradation

KW - Extra-cellular matrix

KW - Fractals

KW - Modeling

KW - Pancreatic adenocarcinoma

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DO - 10.1186/s12967-019-1817-3

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