Validity of ultrasound-guided aspiration needle biopsy in the diagnosis of micrometastases in sentinel lymph nodes in patients with cutaneous melanoma

Goran Šijan; Jefta V Kozarski; Nenad Stepić; Saša Milojević; Dara Stefanović; Željka Tatomirović; Ljiljana Jauković; Svetlana Vesanović; Milica Rajović

doi:10.2298/VSP150227042S

Goran Šijan Clinic for Plastic Surgery and Burns,Military Medical Academy, Belgrade, Serbia;Faculty of Medicine of the Military Medical Academy, University of Defence, Belgrade, Serbia
Jefta V Kozarski Clinic for Plastic Surgery and Burns,Military Medical Academy, Belgrade, Serbia;Faculty of Medicine of the Military Medical Academy, University of Defence, Belgrade, Serbia
Nenad Stepić Clinic for Plastic Surgery and Burns,Military Medical Academy, Belgrade, Serbia;Faculty of Medicine of the Military Medical Academy, University of Defence, Belgrade, Serbia
Saša Milojević Department of Cytology, Military Medical Academy, Belgrade, Serbia
Dara Stefanović Faculty of Medicine of the Military Medical Academy, University of Defence, Belgrade, Serbia; Institute for Radiology,Military Medical Academy, Belgrade, Serbia
Željka Tatomirović Faculty of Medicine of the Military Medical Academy, University of Defence, Belgrade, Serbia; Department of Cytology,Military Medical Academy, Belgrade, Serbia
Ljiljana Jauković Faculty of Medicine of the Military Medical Academy, University of Defence, Belgrade, Serbia; Institute for Nuclear Medicine, Military Medical Academy, Belgrade, Serbia
Svetlana Vesanović Private Practice for Plastic and Reconstructive Surgery “Vesanović dr Svetlana”, Belgrade, Serbia
Milica Rajović Clinic for Plastic Surgery and Burns, Military Medical Academy, Belgrade, Serbia

DOI: https://doi.org/10.2298/VSP150227042S

Keywords: endoscopic ultrasound-guided fine needle aspiration, neoplasm, micrometastasis, sentinel lymph node biopsy, skin, melanoma, diagnosis, sensitivity and specificity,

Abstract

Background/Aim. Cutaneous melanoma is one of the most aggressive solid cancers, that develops local, regional and distant metastases. The presence of metastases in lymph nodes is in correlation with Breslow tumor thickness. According to various researches, in melanoma with more than 4 mm Breslow thickness, lymph node micrometastases can be found in 60–70% of cases. Sentinel lymph nodes biopsy is a diagnostic procedure for lymph node micrometastasis detection, which is necessary for disease staging. In recent studies, ultrasound-guided fine needle aspiration with cytology (US FNAC) of the sentinel lymph node was used as less invasive procedure, but is not accepted as the standard procedure. The goal of this work was to define sensitivity, specification and precision of the ultrasound-guided fine needle aspiration method in comparison with standard sentinel lymph node biopsy. Methods. After obtaining the Ethics Committee’s permission, from 2012 to 2014 a total of 60 patients with cutaneous melanoma were enrolled, and divided into three groups: group I with thin melanoma, group II with intermediate thickness melanoma and group III with thick melanoma. The presence of micrometastases in sentinel regional lymph nodes was analyzed by US FNAC. The results obtained were compared to sentinel lymph nodes biopsy (SLNB) results. The golden standard for calculating the specific, sensitive and precise characteristics of the method of US FNAC of sentinel lymph nodes was histopathologic lymph node examination of sentinel lymph nodes acquired through biopsy. Results. Detection rate of US FNAC was 0% in the group I, 5% in the group II and 30% in the group III. SLNB detection rates were: 10% in the group I, 15% in the group II, and 45% in the group III. In melanoma thicker than 4 mm, 15% of the patients were false negative by US FNAC. The sensitivity of US FNAC for all the patients was 50%: in the group I, 0%; in the group II, 33.3%; and in the group III, 66.6%. The method specificity for all examined patients was 100% and accuracy 88%: group I, 90%; group II, 90%; group III, 85%. The FNAC and SLNB micrometastasis detection rate was significantly higher in melanoma with Breslow thickness > 4 mm (group 3) in comparison to thin and intermediate thickness tumors. Conclusion. The method of ultrasound-guided fine needle aspiration of sentinel lymph nodes, according to its sensitivity, has a place in the diagnostics of micrometastasis in regional lymph nodes only in thick melanoma, but not in thin and intermediary thickness melanoma. The results must be confirmed in a larger number of patients. If this observation could be confirmed, it would rationalize treatment of patients with thick melanoma, decrease the number of operations and shorten the time to make the diagnosis.

Author Biography

Jefta V Kozarski, Clinic for Plastic Surgery and Burns,Military Medical Academy, Belgrade, Serbia;Faculty of Medicine of the Military Medical Academy, University of Defence, Belgrade, Serbia

Specijalista za plastičnu, rekonstruktivnu i estetsku hirurgiju

References

Lens MB, Dawes M, Newton-Bishop JA, Goodacre T. Tumour thickness as a predictor of occult lymph node metastases in patients with stage I and II melanoma undergoing sentinel lymph node biopsy. Br J Surg 2002; 89(10): 1223−7.

Schäfer-Hesterberg G, Schoengen A, Sterry W, Voit C. Use of ultra-sound to early identify, diagnose and localize metastases in melanoma patients. Exp Rev Anticanc Ther 2007; 7(12): 1707−16.

Šijan G, Kozarski J, Stefanović D, Lalković M, Milićević S, Stanković G. Ultrasonographic findings validity in the identification of metastatic regional lymph nodes in patients with cutaneous melanoma. Vojnosanit Pregl 2010; 67(1): 25−31. (Serbian)

Voit CA, van Akkooi AC, Eggermont AM. Role of Ultrasound in the Assessment of the Sentinel Node of Melanoma Patients. AJR Am J Roentgenol 2010; 195(6): 474−5.

Catalano O, Setola SV, Vallone P, Raso MM, d'Errico Adolfo G. Sonography for locoregional staging and follow-up of cutaneous melanoma: how we do it. J Ultrasound Med 2010; 29(5): 791−802.

Sanki A, Uren RF, Moncrieff M, Tran KL, Scolyer RA, Lin HY, et al. Targeted High-Resolution Ultrasound Is Not an Effective Substitute for Sentinel Lymph Node Biopsy in Patients With Primary Cutaneous Melanoma. J Clin Oncol 2009; 27(33): 5614−9.

Kunte C, Schuh T, Eberle JY, Baumert J, Konz B, Volkenandt M, et al. The use of high-resolution ultrasonography for preopera-tive detection of metastases in sentinel lymph nodes of pa-tients with cutaneous melanoma. Dermatol Surg 2009; 35(11): 1757−65.

Tschammler A, Wirkner H, Ott G, Hahn D. Vascular patterns in reactive and malignant lymphadenopathy. Eur Radiol 1996; 6(4): 473−80.

Cafiero F, Peressini A, Gipponi M, Rainero ML, Villa G, Sertoli MR, et al. Sentinel node biopsy in patients with cutaneous me-lanoma. Semin Surg Oncol 1998; 15(4): 284−6.

Glass FL, Cottam JA, Reintgen DS, Fenske NA. Lymphatic map-ping and sentinel node biopsy in the management of high-risk melanoma. J Am Acad Dermatol 1998; 39(4 Pt 1): 603−10.

Gershenwald JE, Thompson W, Mansfield PF, Lee JE, Colome MI, Tseng CH, et al. Multi-institutional melanoma lymphatic map-ping experience: the prognostic value of sentinel lymph node status in 612 stage I or II melanoma patients. J Clin Oncol 1999; 17(3): 976−83.

Balch CM, Gershenwald JE, Soong S, Thompson JF, Atkins MB, Byrd DR, et al. Final version of 2009 AJCC melanoma staging and classification. J Clin Oncol 2009; 27(36): 6199−206.

Stebbins WG, Garibyan L, Sober AJ. Sentinel lymph node biopsy and melanoma: 2010 update: Part I. J Am Acad Dermatol 2010; 62(5): 723−34.

Bogdanov-Berezovsky A, Pagkalos VA, Silberstein E, Shoham Y, Xanthinaki AA, Krieger Y. Increasing the Efficacy of SLNB in Cases of Malignant Melanoma Located in Close Proximity to the Lymphatic Basin. ISRN Dermatol 2014; 2014: 920349.

Morton DL, Thompson JF, Essner R, Elashoff R, Stern SL, Nieweg OE, et al. Validation of the accuracy of intraoperative lymphat-ic mapping and sentinel lymphadenectomy for early-stage me-lanoma: a multicenter trial. Multicenter Selective Lymphade-nectomy Trial Group. Ann Surg 1999; 230(4): 453−65.

Wasserberg N, Tulchinsky H, Schachter J, Feinmesser M, Gutman H. Sentinel-lymph-node biopsy (SLNB) for melanoma is not complication-free. Eur J Surg Oncol 2004; 30(8): 851−6.

Dummer R, Hauschild A, Guggenheim M, Keilholz U, Pentheroudakis G. ESMO Guidelines Working . Cutaneous melanoma: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol 2012; 23 (Suppl 7): vii86−vii91.

Garbe C, Peris K, Hauschild A, Saiag P, Middleton M, Spatz A, et al. Diagnosis and treatment of melanoma. European consensus-based interdisciplinary guideline.Update 2012. Eur J Cancer 2012; 48(15): 2375−90.

Pflugfelder A, Kochs C, Blum A, Capellaro M, Czeschik C, Dettenborn T, et al. S3-Guideline “Diagnosis, therapy and follow-up of melanoma” - short version. J Dtsch Dermatol Ges 2013; 11(6): 563−602.

NCCN Clinical Practice guidelines in oncology v2. 2014. Available from: http://www.nccn.org/professionals/physician_gls/ pdf/melanoma.pdf.

Clinical Practice Guidelines for the Management of Melanoma in Australia and New Zealand. 2010. Available from: www. publications /_files_nhmrc/ /attachments/cp111.pdf.

Wong SL, Balch CM, Hurley P, Agarwala SS, Akhurst TJ, Cochran A, et al. Sentinel lymph node biopsy for melanoma: American Society of Clinical Oncology and Society of Surgical Oncology joint clinical practice guideline. J Clin Oncol 2012; 30(23): 2912−8.

Chakera AH, Hesse B, Burak Z, Ballinger JR, Britten A, Caracò C, et al. EANM-EORTC general recommendations for sentinel node diagnostics in melanoma. Eur J Nucl Med Mol Imaging 2009; 36(10): 1713−42.

Reintgen D, Pendas S, Jakub J, Swor G, Giuliano R, Bauer J, et al. National trials involving lymphatic mapping for melanoma: the Multicenter Selective Lymphadenectomy Trial, the Sunbelt Melanoma Trial, and the Florida Melanoma Trial. Semin On-col 2004; 31(3): 363−73.

Rajovic M, Jaukovic L, Kandolf-Sekulovic L, Šijan G, Zolotarevski L, Novakovic M. Sentinel lymph node status -clinicopathological and prognostic associations - initial experience from the single center. 6th World Meeting of Interdisciplinary Melanoma/Skin Cancer Centres & 8th EADO Congress; 2012 November 14−17; Barcelona, Spain: European Academy of Dermatology and Venerology; 2012.

Rajovic M, Jaukovic L, Zolotarevski L, Šijan G, Novakovic M. Sen-tinel lymph node tumor burden and its correlation to clinico-pathologic characteristics of primary melanoma and ﬁ nding of non-sentinel lymph node in completelymph node dis-section. J Dtsch Dermatol Ges 2013;11(Suppl 7): 63−4.

Testori A, Rastrelli M, de Fiori E, Soteldo J, Vigna PD, Trifirò G, et al. Radio-guided ultrasound lymph node localization: feasibility of a new technique for localizing and excising nonpalpable lymph nodes ultrasound suspicious for melanoma metastases. Melanoma Res 2010; 20(3): 197−202.

Voit C, van Akkooi AC, Schafer-Hesterberg G, Schoengen A, Ko-walczyk K, Roewert JC, et al. Ultrasound Morphology Criteria Predict Metastatic Disease of the Sentinel Nodes in Patients With Melanoma. J Clin Oncol 2010; 8(5): 847−52.

Murali R, Thompson JF, Uren RF, Scolyer RA. Fine-needle biopsy of metastatic melanoma: clinical use and new applications. Lancet Oncol 2010; 11(4): 391−400.

Voit CA, van Akkooi AC, Schafer-Hesterberg G, Schoengen A, Schmitz PI, Sterry W, et al.. Rotterdam Criteria for Sentinel Node (SN) Tumor Burden and the Accuracy of Ultrasound (US) -Guided Fine-Needle Aspiration Cytology (FNAC): Can US-Guided FNAC Replace SN Staging in Patients With Mela-noma. J Clin Oncol 2009; 27(30): 4994−5000.

Doubrovsky A, Scolyer RA, Murali R, McKenzie PR, Watson GF, Lee SC, et al. Diagnostic Accuracy of Fine Needle Biopsy for Metastatic Melanoma and Its Implications for Patient Man-agement. Ann Surg Oncol 2007; 15(1): 323−32.

Sanki A, Uren RF, Moncrieff M, Tran KL, Scolyer RA, Lin HY, et al. Targeted High-Resolution Ultrasound Is Not an Effective Substitute for Sentinel Lymph Node Biopsy in Patients With Primary Cutaneous Melanoma. J Clin Oncol 2009; 27(33): 5614−9.

Starritt EC, Uren RF, Scolyer RA, Quinn MJ, Thompson JF. Ultra-sound examination of sentinel nodes in the initial assessment of patients with primary cutaneous melanoma. Ann Surg On-col 2005; 12(1): 18−23.

Voit C, Kron M, Schäfer G, Schoengen A, Audring H, Lukowsky A, et al. Ultrasound-guided Fine Needle Aspiration Cytology prior to Sentinel Lymph Node Biopsy in Melanoma Patients. Ann Surg Oncol 2006; 13(12): 1682−9.

Voit CA, Gooskens SL, Siegel P, Schaefer G, Schoengen A, Röwert J, et al. Ultrasound-guided fine needle aspiration cytology as an addendum to sentinel lymph node biopsy can perfect the staging strategy in melanoma patients. Eur J Cancer 2014; 50(13): 2280−8.

Voit CA, van Akkooi AJ, Schäfer-Hesterberg G, Sterry W, Eggermont AM. The value of preoperative ultrasound (after lym-phoscintigraphy) in conjunction with pre-sentinel lymph node biopsy fine-needle aspiration outweighs the usage of ultra-sound alone in conjunction with lymphoscintigraphy: the need for an algorithm. Melanoma Res 2010; 20(4): 357−9.