{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T01:51:22Z","timestamp":1760147482389,"version":"build-2065373602"},"reference-count":52,"publisher":"MDPI AG","issue":"2","license":[{"start":{"date-parts":[[2023,2,6]],"date-time":"2023-02-06T00:00:00Z","timestamp":1675641600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"SFB1371","award":["395357507"],"award-info":[{"award-number":["395357507"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Veterinary Sciences"],"abstract":"<jats:p>Most canine intestinal tumours are B-cell or T-cell lymphomas or carcinomas. They have to be distinguished from cases of enteritis. Non-invasive biomarkers such as miRNAs would be a step towards faster diagnosis. The aim of this study was to investigate shifts in miRNA expression in tissue samples collected from cases of enteritis, carcinoma and lymphoma of the small and large intestine to better understand the potential of miRNA as biomarkers for tumour diagnosis and classification. We selected two oncogenic miRNAs (miR-18b and 20b), two tumour suppressive miRNAs (miR-192 and 194) and two potential biomarkers for neoplasms (miR-126 and 214). They were isolated from FFPE material, quantified by ddPCR, normalised with RNU6B and compared with normal tissue values. Our results confirmed that ddPCR is a suitable method for quantifying miRNA from FFPE material. Expression of miR-18b and miR-192 was higher in carcinomas of the small intestine than in those of the large intestine. Specific miRNA patterns were observed in cases of enteritis, B-cell and T-cell lymphoma and carcinoma. However, oncogenic miR-18b and 20b were not elevated in any group and miR-126 and 214 were down-regulated in T-cell and B-cell lymphoma, as well as in carcinomas and lymphoplasmacytic enteritis of the small intestine.<\/jats:p>","DOI":"10.3390\/vetsci10020125","type":"journal-article","created":{"date-parts":[[2023,2,7]],"date-time":"2023-02-07T01:35:17Z","timestamp":1675733717000},"page":"125","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":3,"title":["miRNA Profiles of Canine Intestinal Carcinomas, Lymphomas and Enteritis Analysed by Digital Droplet PCR from FFPE Material"],"prefix":"10.3390","volume":"10","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-1547-0713","authenticated-orcid":false,"given":"Alexandra","family":"Kehl","sequence":"first","affiliation":[{"name":"LABOKLIN GmbH & Co. KG, 97688 Bad Kissingen, Germany"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Mario","family":"Valkai","sequence":"additional","affiliation":[{"name":"LABOKLIN GmbH & Co. KG, 97688 Bad Kissingen, Germany"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Anna-Lena","family":"Van de Weyer","sequence":"additional","affiliation":[{"name":"LABOKLIN GmbH & Co. KG, 97688 Bad Kissingen, Germany"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6162-7515","authenticated-orcid":false,"given":"Maria","family":"Brockmann","sequence":"additional","affiliation":[{"name":"LABOKLIN GmbH & Co. KG, 97688 Bad Kissingen, Germany"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7269-5433","authenticated-orcid":false,"given":"Katja","family":"Steiger","sequence":"additional","affiliation":[{"name":"Comparative Experimental Pathology, School of Medicine, Technical University of Munich (TUM), 81675 Munich, Germany"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9990-1890","authenticated-orcid":false,"given":"Benjamin","family":"Schusser","sequence":"additional","affiliation":[{"name":"Reproductive Biotechnology, School of Life Sciences Weihenstephan, Technical University of Munich (TUM), 85354 Freising, Germany"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Heike","family":"Aupperle-Lellbach","sequence":"additional","affiliation":[{"name":"LABOKLIN GmbH & Co. KG, 97688 Bad Kissingen, Germany"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2023,2,6]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"577","DOI":"10.1016\/S0195-5616(85)50059-5","article-title":"Tumors of the Alimentary Tract","volume":"15","author":"Crow","year":"1985","journal-title":"Vet. Clin. N. Am. Small Anim. Pract."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"693","DOI":"10.1016\/j.cvsm.2012.04.006","article-title":"Alimentary neoplasia in geriatric dogs and cats","volume":"42","author":"Willard","year":"2012","journal-title":"Vet. Clin. N. Am. Small Anim. Pract."},{"key":"ref_3","doi-asserted-by":"crossref","unstructured":"Meuten, D.J. (2016). Tumors in Domestic Animals, John Wiley & Sons, Inc.","DOI":"10.1002\/9781119181200"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"329","DOI":"10.1016\/j.cvsm.2011.01.002","article-title":"Ultrasonography of small intestinal inflammatory and neoplastic diseases in dogs and cats","volume":"41","author":"Gaschen","year":"2011","journal-title":"Vet. Clin. N. Am. Small Anim. Pract."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"1130","DOI":"10.2460\/javma.229.7.1130","article-title":"Diagnostic value of cytologic examination of gastrointestinal tract tumors in dogs and cats: 83 cases (2001\u20132004)","volume":"229","author":"Bonfanti","year":"2006","journal-title":"J. Am. Vet. Med. Assoc."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"871","DOI":"10.1016\/j.cvsm.2014.05.007","article-title":"Cancer screening tests for small animals","volume":"44","author":"Schleis","year":"2014","journal-title":"Vet. Clin. N. Am. Small Anim. Pract."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"664718","DOI":"10.3389\/fvets.2021.664718","article-title":"Horizons in Veterinary Precision Oncology: Fundamentals of Cancer Genomics and Applications of Liquid Biopsy for the Detection, Characterization, and Management of Cancer in Dogs","volume":"8","author":"Chibuk","year":"2021","journal-title":"Front. Vet. Sci."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"122","DOI":"10.1080\/01652176.2016.1182230","article-title":"Investigation of cell-free DNA in canine plasma and its relation to disease","volume":"36","author":"Burnett","year":"2016","journal-title":"Vet. Q."},{"key":"ref_9","doi-asserted-by":"crossref","unstructured":"Flory, A., Kruglyak, K.M., Tynan, J.A., McLennan, L.M., Rafalko, J.M., Fiaux, P.C., Hernandez, G.E., Marass, F., Nakashe, P., and Ruiz-Perez, C.A. (2022). Clinical validation of a next-generation sequencing-based multi-cancer early detection \u201cliquid biopsy\u201d blood test in over 1000 dogs using an independent testing set: The CANcer Detection in Dogs (CANDiD) study. PLoS ONE, 17.","DOI":"10.1371\/journal.pone.0266623"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"2301","DOI":"10.1038\/s41598-017-02607-1","article-title":"Circulating microRNA-214 and -126 as potential biomarkers for canine neoplastic disease","volume":"7","author":"Heishima","year":"2017","journal-title":"Sci. Rep."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"281","DOI":"10.1016\/S0092-8674(04)00045-5","article-title":"MicroRNAs","volume":"116","author":"Bartel","year":"2004","journal-title":"Cell"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.ydbio.2006.08.028","article-title":"microRNAs as oncogenes and tumor suppressors","volume":"302","author":"Zhang","year":"2007","journal-title":"Dev. Biol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"35","DOI":"10.1007\/s40139-017-0123-0","article-title":"MicroRNAs in Cancer: Challenges and opportunities in early detection, disease monitoring, and therapeutic agents","volume":"5","author":"Chatterjee","year":"2017","journal-title":"Curr. Pathobiol. Rep."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"2087","DOI":"10.1111\/j.1349-7006.2010.01650.x","article-title":"Circulating microRNA in body fluid: A new potential biomarker for cancer diagnosis and prognosis","volume":"101","author":"Kosaka","year":"2010","journal-title":"Cancer Sci."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"117473","DOI":"10.1016\/j.lfs.2020.117473","article-title":"Circulating microRNAs as biomarkers in cancer diagnosis","volume":"248","author":"Sohel","year":"2020","journal-title":"Life Sci."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"502","DOI":"10.1111\/vco.12570","article-title":"Tumour-specific microRNA expression pattern in canine intestinal T-cell-lymphomas","volume":"18","author":"Joos","year":"2020","journal-title":"Vet. Comp. Oncol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"e00391-17","DOI":"10.1128\/MCB.00391-17","article-title":"Upregulation of MicroRNA 18b Contributes to the Development of Colorectal Cancer by Inhibiting CDKN2B","volume":"37","author":"Li","year":"2017","journal-title":"Mol. Cell. Biol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"1989","DOI":"10.1111\/jvim.16530","article-title":"Association of fecal and serum microRNA profiles with gastrointestinal cancer and chronic inflammatory enteropathy in dogs","volume":"36","author":"Lyngby","year":"2022","journal-title":"J. Vet. Intern. Med."},{"key":"ref_19","doi-asserted-by":"crossref","unstructured":"Konstantinidis, A.O., Pardali, D., Adamama-Moraitou, K.K., Gazouli, M., Dovas, C.I., Legaki, E., Brellou, G.D., Savvas, I., Jergens, A.E., and Rallis, T.S. (2020). Colonic mucosal and serum expression of microRNAs in canine large intestinal inflammatory bowel disease. BMC Vet. Res., 16.","DOI":"10.1186\/s12917-020-02287-6"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"717","DOI":"10.1016\/j.amjsurg.2013.12.023","article-title":"Differential expression of microRNA-320a, -145, and -192 along the continuum of normal mucosa to high-grade dysplastic adenomas of the colorectum","volume":"207","author":"Tsikitis","year":"2014","journal-title":"Am. J. Surg."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"678","DOI":"10.1111\/cas.13165","article-title":"Cluster microRNAs miR-194 and miR-215 suppress the tumorigenicity of intestinal tumor organoids","volume":"108","author":"Nakaoka","year":"2017","journal-title":"Cancer Sci."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"1421","DOI":"10.31557\/APJCP.2019.20.5.1421","article-title":"Plasma Level of MicroRNAs, MiR-107, MiR-194 and MiR-210 as Potential Biomarkers for Diagnosis Intestinal-Type Gastric Cancer in Human","volume":"20","author":"Parvaee","year":"2019","journal-title":"Asian Pac. J. Cancer Prev."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"607","DOI":"10.1158\/1940-6207.CAPR-13-0426","article-title":"miR-194 as a predictor for adenoma recurrence in patients with advanced colorectal adenoma after polypectomy","volume":"7","author":"Wang","year":"2014","journal-title":"Cancer Prev. Res."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"25377","DOI":"10.3390\/ijms161025377","article-title":"MicroRNA-214 and MicroRNA-126 Are Potential Biomarkers for Malignant Endothelial Proliferative Diseases","volume":"16","author":"Heishima","year":"2015","journal-title":"Int. J. Mol. Sci."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"19","DOI":"10.1177\/0300985810389316","article-title":"Recommended guidelines for submission, trimming, margin evaluation, and reporting of tumor biopsy specimens in veterinary surgical pathology","volume":"48","author":"Kamstock","year":"2011","journal-title":"Vet. Pathol."},{"key":"ref_26","unstructured":"Romeis-Mikroskopische Technik, Mulisch, M., and Welsch, U. (2015). 19. Aufl. 2015, Springer."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"S1","DOI":"10.1016\/j.jcpa.2008.01.001","article-title":"Histopathological standards for the diagnosis of gastrointestinal inflammation in endoscopic biopsy samples from the dog and cat: A report from the World Small Animal Veterinary Association Gastrointestinal Standardization Group","volume":"138","author":"Day","year":"2008","journal-title":"J. Comp. Pathol."},{"key":"ref_28","doi-asserted-by":"crossref","unstructured":"Head, K.W., Cullen, J.M., and Dubielzig, R.R. (2003). Histological Classification of Tumors of the Alimentary System of Domestic Animals, Armed Forces Institute of Pathology.","DOI":"10.1002\/9780470376928.ch8"},{"key":"ref_29","unstructured":"Valli, V.E., Jacobs, R., Parodi, A.L., Vernau, W., and Moore, P.F. (2002). Histological Classification of Hematopoietic Tumors of Domestic Animals, Armed Forces Institute of Pathology."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"447","DOI":"10.3389\/fonc.2018.00447","article-title":"Cancer Site-Specific Multiple microRNA Quantification by Droplet Digital PCR","volume":"8","author":"Laprovitera","year":"2018","journal-title":"Front. Oncol."},{"key":"ref_31","doi-asserted-by":"crossref","unstructured":"Filetti, V., Loreto, C., Falzone, L., Lombardo, C., Cannizzaro, E., Castorina, S., Ledda, C., and Rapisarda, V. (2021). Diagnostic and Prognostic Value of Three microRNAs in Environmental Asbestiform Fibers-Associated Malignant Mesothelioma. J. Pers. Med., 11.","DOI":"10.21203\/rs.3.rs-448056\/v1"},{"key":"ref_32","doi-asserted-by":"crossref","unstructured":"Kehl, A., T\u00f6rner, K., Jordan, A., Lorenz, M., Schwittlick, U., Conrad, D., Steiger, K., Schusser, B., and Aupperle-Lellbach, H. (2022). Pathological Findings in Gastrointestinal Neoplasms and Polyps in 860 Cats and a Pilot Study on miRNA Analyses. Vet. Sci., 9.","DOI":"10.3390\/vetsci9090477"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"1070","DOI":"10.1016\/j.leukres.2009.10.023","article-title":"Identification of suitable endogenous controls and differentially expressed microRNAs in canine fresh-frozen and FFPE lymphoma samples","volume":"34","author":"Mortarino","year":"2010","journal-title":"Leuk. Res."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"533","DOI":"10.1016\/j.urolonc.2009.05.008","article-title":"miRNA analysis of prostate cancer by quantitative real time PCR: Comparison between formalin-fixed paraffin embedded and fresh-frozen tissue","volume":"29","author":"Leite","year":"2011","journal-title":"Urol. Oncol."},{"key":"ref_35","doi-asserted-by":"crossref","unstructured":"Vojtechova, Z., Zavadil, J., Klozar, J., Grega, M., and Tachezy, R. (2017). Comparison of the miRNA expression profiles in fresh frozen and formalin-fixed paraffin-embedded tonsillar tumors. PLoS ONE, 12.","DOI":"10.1371\/journal.pone.0179645"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"61","DOI":"10.1016\/j.vascn.2019.02.002","article-title":"Factors affecting RNA quantification from tissue long-term stored in formalin","volume":"96","author":"Malnar","year":"2019","journal-title":"J. Pharmacol. Toxicol. Methods"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"621","DOI":"10.1002\/cncy.21729","article-title":"Prognostic impact of a 3-MicroRNA signature in cytological samples of small cell lung cancer","volume":"124","author":"Mancuso","year":"2016","journal-title":"Cancer Cytopathol."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"1333","DOI":"10.1373\/clinchem.2015.239459","article-title":"Data Normalization Strategies for MicroRNA Quantification","volume":"61","author":"Schwarzenbach","year":"2015","journal-title":"Clin. Chem."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"192","DOI":"10.2144\/btn-2019-0065","article-title":"qPCR-based methods for expression analysis of miRNAs","volume":"67","author":"Forero","year":"2019","journal-title":"Biotechniques"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"5699","DOI":"10.1158\/0008-5472.CAN-06-4478","article-title":"Oncogenic potential of the miR-106-363 cluster and its implication in human T-cell leukemia","volume":"67","author":"Landais","year":"2007","journal-title":"Cancer Res."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"1379643","DOI":"10.1155\/2016\/1379643","article-title":"The Three Paralogous MicroRNA Clusters in Development and Disease, miR-17-92, miR-106a-363, and miR-106b-25","volume":"2016","author":"Khuu","year":"2016","journal-title":"Scientifica"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"58","DOI":"10.1159\/000363303","article-title":"Underexpression of miR-126 and miR-20b in hereditary and nonhereditary colorectal tumors","volume":"87","author":"Yamaguchi","year":"2014","journal-title":"Oncology"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"246","DOI":"10.3389\/fgene.2014.00246","article-title":"An investigation into anti-proliferative effects of microRNAs encoded by the miR-106a-363 cluster on human carcinoma cells and keratinocytes using microarray profiling of miRNA transcriptomes","volume":"5","author":"Khuu","year":"2014","journal-title":"Front. Genet."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"467","DOI":"10.1038\/nrclinonc.2011.76","article-title":"MicroRNAs in body fluids--the mix of hormones and biomarkers","volume":"8","author":"Cortez","year":"2011","journal-title":"Nat. Rev. Clin. Oncol."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"1863","DOI":"10.3892\/or.2014.3004","article-title":"Plasma miR-122 and miR-192 as potential novel biomarkers for the early detection of distant metastasis of gastric cancer","volume":"31","author":"Chen","year":"2014","journal-title":"Oncol. Rep."},{"key":"ref_46","first-page":"8851035","article-title":"Diagnostic and Prognostic Role of miR-192 in Different Cancers: A Systematic Review and Meta-Analysis","volume":"2021","author":"Wang","year":"2021","journal-title":"Biomed Res. Int."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"333","DOI":"10.1016\/j.yexcr.2015.10.004","article-title":"Deregulation of miR-126 expression in colorectal cancer pathogenesis and its clinical significance","volume":"339","author":"Ebrahimi","year":"2015","journal-title":"Exp. Cell Res."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"203","DOI":"10.3892\/ijo.2013.2168","article-title":"MicroRNA-126 functions as a tumor suppressor in colorectal cancer cells by targeting CXCR4 via the AKT and ERK1\/2 signaling pathways","volume":"44","author":"Liu","year":"2014","journal-title":"Int. J. Oncol."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"233","DOI":"10.1007\/s11010-013-1707-6","article-title":"Expression of miR-126 suppresses migration and invasion of colon cancer cells by targeting CXCR4","volume":"381","author":"Li","year":"2013","journal-title":"Mol. Cell. Biochem."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"3465","DOI":"10.1002\/1878-0261.13218","article-title":"miR-126 downregulates CXCL12 expression in intestinal epithelial cells to suppress the recruitment and function of macrophages and tumorigenesis in a murine model of colitis-associated colorectal cancer","volume":"16","author":"Wu","year":"2022","journal-title":"Mol. Oncol."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"659","DOI":"10.2460\/ajvr.82.8.659","article-title":"Identification of serum microRNAs with differential expression between dogs with splenic masses and healthy dogs with histologically normal spleens","volume":"82","author":"Grimes","year":"2021","journal-title":"Am. J. Vet. Res."},{"key":"ref_52","doi-asserted-by":"crossref","unstructured":"Craig, K.K.L., Wood, G.A., Keller, S.M., Mutsaers, A.J., and Wood, R.D. (2019). MicroRNA profiling in canine multicentric lymphoma. PLoS ONE, 14.","DOI":"10.1371\/journal.pone.0226357"}],"container-title":["Veterinary Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2306-7381\/10\/2\/125\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T18:25:44Z","timestamp":1760120744000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2306-7381\/10\/2\/125"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,2,6]]},"references-count":52,"journal-issue":{"issue":"2","published-online":{"date-parts":[[2023,2]]}},"alternative-id":["vetsci10020125"],"URL":"https:\/\/doi.org\/10.3390\/vetsci10020125","relation":{},"ISSN":["2306-7381"],"issn-type":[{"type":"electronic","value":"2306-7381"}],"subject":[],"published":{"date-parts":[[2023,2,6]]}}}