Contrast-enhanced ultrasound for sentinel lymph node mapping in the routine staging of canine mast cell tumours: A feasibility study.


Journal

Veterinary and comparative oncology
ISSN: 1476-5829
Titre abrégé: Vet Comp Oncol
Pays: England
ID NLM: 101185242

Informations de publication

Date de publication:
Sep 2021
Historique:
revised: 10 08 2020
received: 15 06 2020
accepted: 22 08 2020
pubmed: 26 8 2020
medline: 27 1 2022
entrez: 26 8 2020
Statut: ppublish

Résumé

Canine mast cell tumours (MCTs) typically spread to lymph nodes (LNs) before reaching distant sites, and LN assessment is an important part of MCT staging. Sentinel LN (SLN) mapping techniques to identify draining LNs are being developed and could improve the accuracy of MCT staging. The primary objective of this feasibility study was to determine the safety and effectiveness of contrast-enhanced ultrasound (CEUS) to identify SLNs. Secondary objectives were to determine if the SLNs identified by CEUS coincided with the regional LN predicted by the anatomical lymphosomes, if previous MCT excision altered CEUS SLN findings, and if CEUS could identify MCT nodal metastases. Between June 2017 and March 2019, 59 dogs with 62 MCTs were enrolled. No adverse events related to CEUS were reported. CEUS detected at least 1 SLN in 59/62 MCTs (95.2%, 95% CI: 86.5-99.0%). In only 32/59 (54.2%) MCTs, clinicians would have correctly predicted the SLN(s) identified by CEUS. Among the 35 MCTs that had histological examination of the SLN(s), the prevalence of metastasis was 60% (95% CI: 42.1-76.1%). Additional staging procedures did not reveal any metastases in dogs with histologically non-metastatic SLNs. Integration of CEUS SLN mapping into the routine staging of MCTs is promising, but future studies are required to refine this procedure and to investigate if it would translate into a clinical benefit.

Identifiants

pubmed: 32840038
doi: 10.1111/vco.12647
doi:

Substances chimiques

Contrast Media 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

451-462

Informations de copyright

© 2020 The Authors. Veterinary and Comparative Oncology published by John Wiley & Sons Ltd.

Références

Blackwood L, Murphy S, Buracco P, et al. European consensus document on mast cell tumours in dogs and cats. Vet Comp Oncol. 2012;10:e1-e29.
Warland J, Amores-Fuster I, Newbury W, Brearley M, Dobson J. The utility of staging in canine mast cell tumours. Vet Comp Oncol. 2014;12:287-298.
Horta RS, Lavalle GE, Monteiro LN, Souza MCC, Cassali GD, Araujo RB. Assessment of canine mast cell tumor mortality risk based on clinical, histologic, immunohistochemical, and molecular features. Vet Pathol. 2018;55:212-223.
London C, Thamm DH. Mast cell tumors. In: Vail DM, Thamm DH, Liptak JM, eds. Withrow and MacEwen's Small Animal Clinical Oncology. St Louis: Elsevier; 2020:382-405.
Suami H, Yamashita S, Soto-Miranda MA, Chang DW. Lymphatic territories (lymphosomes) in a canine: an animal model for investigation of postoperative lymphatic alterations. PLoS One. 2013;8:e69222.
Suami H, Shin D, Chang DW. Mapping of lymphosomes in the canine forelimb: comparative anatomy between canines and humans. Plast Reconstr Surg. 2012;129:612-620.
Bezuidenbut A. The lymphatic system. In: Evans HE, Lahunta AD, eds. Miller's Anatomy of the Dog. 4th ed. St Louis: Elsevier; 2013:535-562.
Patsikas MN, Karayannopoulou M, Kaldrymidoy E, et al. The lymph drainage of the neoplastic mammary glands in the bitch: a lymphographic study. Anat Histol Embryol. 2006;35:228-234.
Skinner OT, Boston SE, CHdM S. Patterns of lymph node metastasis identified following bilateral mandibular and medial retropharyngeal lymphadenectomy in 31 dogs with malignancies of the head: patterns of head and neck lymphatic metastasis in dogs. Vet Comp Oncol. 2017 Sep;15(3):881-889.
Herring ES, Smith MM, Robertson JL. Lymph node staging of oral and maxillofacial neoplasms in 31 dogs and cats. J Vet Dent. 2002;19:122-126.
Green K, Boston SE. Bilateral removal of the mandibular and medial retropharyngeal lymph nodes through a single ventral midline incision for staging of head and neck cancers in dogs: a description of surgical technique: mandibular and retropharyngeal lymphadenectomy. Vet Comp Oncol. 2017;15(1):208-214.
Fournier Q, Cazzini P, Bavcar S, Pecceu E, Ballber C, Elders R. Investigation of the utility of lymph node fine-needle aspiration cytology for the staging of malignant solid tumors in dogs. Vet Clin Pathol. 2018;47:489-500.
Ferrari R, Marconato L, Buracco P, et al. The impact of extirpation of non-palpable/normal-sized regional lymph nodes on staging of canine cutaneous mast cell tumours: a multicentric retrospective study. Vet Comp Oncol. 2018;16:505-510.
Dogan NU, Dogan S, Favero G, Köhler C, Dursun P. The basics of sentinel lymph node biopsy: anatomical and pathophysiological considerations and clinical aspects. J Oncol. 2019;3415630.
Worley DR. Incorporation of sentinel lymph node mapping in dogs with mast cell tumours: 20 consecutive procedures. Vet Comp Oncol. 2014;12:215-226.
Ferrari R, Chiti LE, Manfredi M, et al. Biopsy of sentinel lymph nodes after injection of methylene blue and lymphoscintigraphic guidance in 30 dogs with mast cell tumors. Vet Surg. 2020;49(6):1099-1108.
Sugiyama S, Iwai T, Izumi T, et al. CT lymphography for sentinel lymph node mapping of clinically N0 early oral cancer. Cancer Imaging. 2019;19:72.
Randall EK, Jones MD, Kraft SL, Worley DR. The development of an indirect computed tomography lymphography protocol for sentinel lymph node detection in head and neck cancer and comparison to other sentinel lymph node mapping techniques. Vet Comp Oncol. 2020.
Rossi F, Korner M, Suarez J, et al. Computed tomographic-lymphography as a complementary technique for lymph node staging in dogs with malignant tumors of various sites. Vet Radiol Ultrasound. 2018;59:155-162.
Soultani C, Patsikas MN, Karayannopoulou M, et al. Assessment of sentinel lymph node metastasis in canine mammary gland tumors using computed tomographic indirect Lymphography. Vet Radiol Ultrasound. 2017;58:186-196.
Grimes JA, Secrest SA, Northrup NC, Saba CF, Schmiedt CW. Indirect computed tomography lymphangiography with aqueous contrast for evaluation of sentinel lymph nodes in dogs with tumors of the head. Vet Radiol Ultrasound. 2017;58:559-564.
Majeski SA, Steffey MA, Fuller M, Hunt GB, Mayhew PD, Pollard RE. Indirect computed tomographic lymphangiography for iliosacral lymphatic mapping in a cohort of dogs with anal sac gland adenocarcinoma: technique description. Vet Radiol Ultrasound. 2017;58:295-303.
Mayer MN, Silver TI, Lowe CK, Anthony JM. Radiographic lymphangiography in the dog using iodized oil. Vet Comp Oncol. 2013;11:151-161.
Nielsen Moody A, Bull J, Culpan AM, et al. Preoperative sentinel lymph node identification, biopsy and localisation using contrast enhanced ultrasound (CEUS) in patients with breast cancer: a systematic review and meta-analysis. Clin Radiol. 2017;72:959-971.
Lurie DM, Seguin B, Schneider PD, Verstraete FJ, Wisner ER. Contrast-assisted ultrasound for sentinel lymph node detection in spontaneously arising canine head and neck tumors. Invest Radiol. 2006;41:415-421.
Gelb HR, Freeman LJ, Rohleder JJ, Snyder PW. Feasibility of contrast-enhanced ultrasound-guided biopsy of sentinel lymph nodes in dogs. Vet Radiol Ultrasound. 2010;51:628-633.
Wang Y, Cheng Z, Li J, Tang J. Gray-scale contrast-enhanced ultrasonography in detecting sentinel lymph nodes: an animal study. Eur J Radiol. 2010;74:6.
Goldberg BB, Merton DA, Liu JB, Murphy G, Forsberg F. Contrast-enhanced sonographic imaging of lymphatic channels and sentinel lymph nodes. J Ultrasound Med. 2005;24:953-965.
Sever A, Broillet A, Schneider M, et al. Dynamic visualization of lymphatic channels and sentinel lymph nodes using intradermal microbubbles and contrast-enhanced ultrasound in a swine model and patients with breast cancer. J Ultrasound Med. 2010;29:1699-1704.
Cox K, Sever A, Jones S, et al. Validation of a technique using microbubbles and contrast enhanced ultrasound (CEUS) to biopsy sentinel lymph nodes (SLN) in pre-operative breast cancer patients with a normal grey-scale axillary ultrasound. Eur J Surg Oncol. 2013;39:760-765.
Nielsen KR, Klyver H, Chakera AH, Hesse B, Nielson MB. Sentinel node detection in melanomas using contrast-enhanced ultrasound. Acta Radiol. 2009;50(4):412-417.
Sever AR, Mills P, Weeks J, et al. Preoperative sentinel node identification with ultrasound using microbubbles in patients with breast cancer. Am J Roentgenol. 2011;196:251-256.
Xie F, Zhang D, Cheng L, et al. Intradermal microbubbles and contrast-enhanced ultrasound (CEUS) is a feasible approach for sentinel lymph node identification in early-stage breast cancer. World J Surg Oncol. 2015;13:319.
Esfehani M, Yazdankhah-Kenari A, Omranipour R, et al. Validation of contrast enhanced ultrasound technique to wire localization of sentinel lymph node in patients with early breast cancer. Indian J Surg Oncol. 2015;6:370-373.
Seiler GS, Brown JC, Reetz JA, et al. Safety of contrast-enhanced ultrasonography in dogs and cats: 488 cases (2002-2011). J Am Vet Med Assoc. 2013;242:1255-1259.
Liu J, Liu X, He J, et al. Percutaneous contrast-enhanced ultrasound for localization and diagnosis of sentinel lymph node in early breast cancer. Sci Rep. 2019;9:13545.
Wisner ER, Ferrara KW, Short RE, Ottoboni TB, Gabe JD, Patel D. Sentinel node detection using contrast-enhanced power Doppler ultrasound lymphography. Invest Radiol. 2003;38:358-365.
Pecceu E, Serra Varela JC, Handel I, Piccineli C, Milne E, Lawrence J. Ultrasound is a poor predictor of early or overt liver or spleen metastasis in dogs with high-risk mast cell tumours. Vet Comp Oncol. 2019;18(3):389-401.
Book AP, Fidel J, Wills T, Bryan J, Sellon R, Mattoon J. Correlation of ultrasound findings, liver and spleen cytology, and prognosis in the clinical staging of high metastatic risk canine mast cell tumors. Vet Radiol Ultrasound. 2011;52:548-554.
Stefanello D, Valenti P, Faverzani S, et al. Ultrasound-guided cytology of spleen and liver: a prognostic tool in canine cutaneous mast cell tumor. J Vet Intern Med. 2009;23:1051-1057.
Krick EL, Billings AP, Shofer FS, Watanabe S, Sorenmo K. Cytological lymph node evaluation in dogs with mast cell tumours: association with grade and survival. Vet Comp Oncol. 2009;7:130-138.
Weishaar KM, Thamm DH, Worley DR, Kamstock DA. Correlation of nodal mast cells with clinical outcome in dogs with mast cell tumour and a proposed classification system for the evaluation of node metastasis. J Comp Pathol. 2014;151:329-338.
Schneider M. SonoVue, a new ultrasound contrast agent. Eur Radiol. 1999;9(3):S347-S348.
Sever AR, Mills P, Hyvelin JM, et al. Percutaneous removal of sentinel lymph nodes in a swine model using a breast lesion excision system and contrast-enhanced ultrasound. Eur Radiol. 2012;22:545-550.
Brissot HN, Edery EG. Use of indirect lymphography to identify sentinel lymph node in dogs: a pilot study in 30 tumours. Vet Comp Oncol. 2017;15:740-753.
Goldfarb LR, Alazraki NP, Eshima D, Eshima LA, Herda SC, Halkar RK. Lymphoscintigraphic identification of sentinel lymph nodes: clinical evaluation of 0.22-micron filtration of Tc-99m sulfur colloid. Radiology. 1998;208:505-509.
Bluemel C, Herrmann K, Giammarile F, et al. EANM practice guidelines for lymphoscintigraphy and sentinel lymph node biopsy in melanoma. Eur J Nucl Med Mol Imaging. 2015;42:1750-1766.
Giammarile F, Schilling C, Gnanasegaran G, et al. The EANM practical guidelines for sentinel lymph node localisation in oral cavity squamous cell carcinoma. Eur J Nucl Med Mol Imaging. 2019;46:623-637.
Goldberg BB, Merton DA, Liu J-B, et al. Sentinel lymph nodes in a swine model with melanoma: contrast-enhanced lymphatic US. Radiology. 2004;230:727-734.
Favril S, Stock E, Hernot S, et al. Sentinel lymph node mapping by near-infrared fluorescence imaging and contrast-enhanced ultrasound in healthy dogs. Vet Comp Oncol. 2019;17:89-98.
Uren RF, Howman-Giles R, Thompson JF. Patterns of lymphatic drainage from the skin in patients with melanoma. J Nucl Med. 2003;44:570-582.
Saha S, Johnston G, Korant A, et al. Aberrant drainage of sentinel lymph nodes in colon cancer and its impact on staging and extent of operation. Am J Surg. 2013;205:302-305.
Kidner TB, Yoon JL, Faries MB, Morton DL. Epitrochlear sentinel lymph nodes in melanoma: interval or independent? Am Surg. 2012;78:702-705.
Thompson JJ, Pearl DL, Yager JA, Best SJ, Coomber BL, Foster RA. Canine subcutaneous mast cell tumor: characterization and prognostic indices. Vet Pathol. 2011;48:156-168.
Stefanello D, Buracco P, Sabattini S, et al. Comparison of 2- and 3-category histologic grading systems for predicting the presence of metastasis at the time of initial evaluation in dogs with cutaneous mast cell tumors: 386 cases (2009-2014). J Am Vet Med Assoc. 2015;246:765-769.
Gannon CJ, Rousseau DL Jr, Ross MI, et al. Accuracy of lymphatic mapping and sentinel lymph node biopsy after previous wide local excision in patients with primary melanoma. Cancer. 2006;107:2647-2652.
Sirvan SS, Demir IA, Irmak F, et al. Does wide excisional biopsy in skin cancer prevent finding the real sentinel lymph node? J Invest Surg. 2019;20:1-7.
Baginski H, Davis G, Bastian RP. The prognostic value of lymph node metastasis with grade 2 MCTs in dogs: 55 cases (2001-2010). J Am Anim Hosp Assoc. 2014;50:89-95.
Marconato L, Polton G, Stefanello D, et al. Therapeutic impact of regional lymphadenectomy in canine stage II cutaneous mast cell tumours. Vet Comp Oncol. 2018;16:580-589.
Hume CT, Kiupel M, Rigatti L, Shofer FS, Skorupski KA, Sorenmo KU. Outcomes of dogs with grade 3 mast cell tumors: 43 cases (1997-2007). J Am Anim Hosp Assoc. 2011;47:37-44.
Li J, Lu M, Cheng X, et al. How pre-operative sentinel lymph node contrast-enhanced ultrasound helps intra-operative sentinel lymph node biopsy in breast cancer: initial experience. Ultrasound Med Biol. 2019;45:1865-1873.
Tanis PJ, Nieweg OE, Valdés Olmos RA, Kroon BBR. Anatomy and physiology of lymphatic drainage of the breast from the perspective of sentinel node biopsy. J Am Coll Surg. 2001;192:399-409.

Auteurs

Quentin Fournier (Q)

Department of Small Animal Teaching Hospital, The Royal (Dick) School of Veterinary Studies and The Roslin Institute, University of Edinburgh, Edinburgh, UK.

Florence Thierry (F)

Department of Small Animal Teaching Hospital, The Royal (Dick) School of Veterinary Studies and The Roslin Institute, University of Edinburgh, Edinburgh, UK.
Occitanie Veterinary Hospital, Toulouse, France.

Maurizio Longo (M)

Department of Small Animal Teaching Hospital, The Royal (Dick) School of Veterinary Studies and The Roslin Institute, University of Edinburgh, Edinburgh, UK.
Department of Veterinary Medicine, Veterinary Teaching Hospital, University of Milan, Lodi, Italy.

Alexandra Malbon (A)

Easter Bush Pathology, The Royal (Dick) School of Veterinary Studies and The Roslin Institute, University of Edinburgh, Edinburgh, UK.

Paola Cazzini (P)

Easter Bush Pathology, The Royal (Dick) School of Veterinary Studies and The Roslin Institute, University of Edinburgh, Edinburgh, UK.

Jocelyn Bisson (J)

Department of Small Animal Teaching Hospital, The Royal (Dick) School of Veterinary Studies and The Roslin Institute, University of Edinburgh, Edinburgh, UK.

Samantha Woods (S)

Department of Small Animal Teaching Hospital, The Royal (Dick) School of Veterinary Studies and The Roslin Institute, University of Edinburgh, Edinburgh, UK.
Veterinary Specialists, Scotland, Livingston, Scotland.

Tiziana Liuti (T)

Department of Small Animal Teaching Hospital, The Royal (Dick) School of Veterinary Studies and The Roslin Institute, University of Edinburgh, Edinburgh, UK.

Spela Bavcar (S)

Department of Small Animal Teaching Hospital, The Royal (Dick) School of Veterinary Studies and The Roslin Institute, University of Edinburgh, Edinburgh, UK.

Articles similaires

Humans Students, Medical Robotic Surgical Procedures Feasibility Studies Female
Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice

Classifications MeSH