Sentinel Node Identification in Melanoma: Current Clinical Impact, New Emerging SPECT Radiotracers and Technological Advancements. An Update of the Last Decade

Author(s): Natale Quartuccio*, Massimiliano Siracusa, Marco Pappalardo, Annachiara Arnone, Gaspare Arnone

Journal Name: Current Radiopharmaceuticals

Volume 13 , Issue 1 , 2020

DOI : 10.2174/1874471012666191015100837

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Graphical Abstract:


Abstract:

Background: Melanoma is the most lethal skin cancer with a mortality rate of 262 cases per 100.000 cases. The sentinel lymph node (SLN) is the first lymph node draining the tumor. SLN biopsy is a widely accepted procedure in the clinical setting since it provides important prognostic information, which helps patient management, and avoids the side effects of complete lymph node dissection. The rationale of identifying and removing the SLN relies on the low probability of subsequent metastatic nodes in case of a negative histological exam performed in the SLN.

Discussion: Recently, new analytical approaches, based on the evaluation of scintigraphic images are also exploring the possibility to predict the metastatic involvement of the SLN. 99mTc-labeled colloids are still the most commonly used radiotracers but new promising radiotracers, such as 99mTc- Tilmanocept, are now on the market. In the last decades, single photon emission computed tomography- computerized tomography (SPECT/CT) has gained wider diffusion in clinical departments and there is large evidence about its superior diagnostic accuracy over planar lymphoscintigraphy (PL) in the detection of SLN in patients with melanoma. Scientists are also investigating new hybrid techniques combining functional and anatomical images for the depiction of SLN but further evidence about their value is needed.

Conclusion: This review examined the predictive and prognostic factors of lymphoscintigraphy for metastatic involvement of SLN, the currently available and emerging radiotracers and the evidence of the additional value of SPECT/CT over PL for the identification of SLN in patients with melanoma. Finally, the review discussed the most recent technical advances in the field.

Keywords: Melanoma, sentinel lymph node biopsy, 99mTc-Tilmanocept, 99mTc-colloids, SPECT/CT, hybrid imaging.

[1]
Karimkhani, C.; Green, A.C.; Nijsten, T.; Weinstock, M.A.; Dellavalle, R.P.; Naghavi, M.; Fitzmaurice, C. The global burden of melanoma: results from the Global Burden of Disease Study 2015. Br. J. Dermatol., 2017, 177(1), 134-140.
[http://dx.doi.org/10.1111/bjd.15510] [PMID: 28369739]
[2]
Arnone, G. Ruolo clinico dell’imaging integrato nel melanoma. Dermatologia e medicina interna;, Palminteri, G.; Lotti; Scerrato; Brai, Eds. Mattioli 1885. 1998, II, 1021-1029.
[3]
Prado, G.; Svoboda, R.M.; Rigel, D.S. What’s New in Melanoma. Dermatol. Clin., 2019, 37(2), 159-168.
[http://dx.doi.org/10.1016/j.det.2018.12.005] [PMID: 30850038]
[4]
Moncayo, V.M.; Aarsvold, J.N.; Alazraki, N.P. Lymphoscintigraphy and sentinel nodes. J. Nucl. Med., 2015, 56(6), 901-907.
[http://dx.doi.org/10.2967/jnumed.114.141432] [PMID: 25931478]
[5]
Bluemel, C.; Herrmann, K.; Giammarile, F.; Nieweg, O.E.; Dubreuil, J.; Testori, A.; Audisio, R.A.; Zoras, O.; Lassmann, M.; Chakera, A.H.; Uren, R.; Chondrogiannis, S.; Colletti, P.M.; Rubello, D. EANM practice guidelines for lymphoscintigraphy and sentinel lymph node biopsy in melanoma. Eur. J. Nucl. Med. Mol. Imaging, 2015, 42(11), 1750-1766.
[http://dx.doi.org/10.1007/s00259-015-3135-1] [PMID: 26205952]
[6]
Sim, F.H.; Taylor, W.F.; Ivins, J.C.; Pritchard, D.J.; Soule, E.H. A prospective randomized study of the efficacy of routine elective lymphadenectomy in management of malignant melanoma. Preliminary results. Cancer, 1978, 41(3), 948-956.
[http://dx.doi.org/10.1002/1097-0142(197803)41:3<948:AID-CNCR2820410324>3.0.CO;2-Z] [PMID: 638981]
[7]
Veronesi, U.; Adamus, J.; Bandiera, D.C.; Brennhovd, O.; Caceres, E.; Cascinelli, N.; Claudio, F.; Ikonopisov, R.L.; Javorski, V.V.; Kirov, S.; Kulakowski, A.; Lacour, J.; Lejeune, F.; Mechl, Z.; Morabito, A.; Rodé, I.; Sergeev, S.; van Slooten, E.; Szczygiel, K.; Trapeznikov, N.N.; Wagner, R.I. Delayed regional lymph node dissection in stage I melanoma of the skin of the lower extremities. Cancer, 1982, 49(11), 2420-2430.
[http://dx.doi.org/10.1002/1097-0142(19820601)49:11<2420:AID-CNCR2820491133>3.0.CO;2-2] [PMID: 7074555]
[8]
Tardelli, E.; Mazzarri, S.; Rubello, D.; Gennaro, M.; Fantechi, L.; Duce, V.; Romanini, A.; Chondrogiannis, S.; Volterrani, D.; Colletti, P.M.; Manca, G. Sentinel Lymph Node Biopsy in Cutaneous Melanoma: Standard and New Technical Procedures and Clinical Advances. A Systematic Review of the Literature. Clin. Nucl. Med., 2016, 41(12), e498-e507.
[http://dx.doi.org/10.1097/RLU.0000000000001370] [PMID: 27749418]
[9]
Wong, S.L.; Faries, M.B.; Kennedy, E.B.; Agarwala, S.S.; Akhurst, T.J.; Ariyan, C.; Balch, C.M.; Berman, B.S.; Cochran, A.; Delman, K.A.; Gorman, M.; Kirkwood, J.M.; Moncrieff, M.D.; Zager, J.S.; Lyman, G.H. Sentinel Lymph Node Biopsy and Management of Regional Lymph Nodes in Melanoma: American Society of Clinical Oncology and Society of Surgical Oncology Clinical Practice Guideline Update. J. Clin. Oncol., 2018, 36(4), 399-413.
[http://dx.doi.org/10.1200/JCO.2017.75.7724] [PMID: 29232171]
[10]
Andtbacka, R.H.; Gershenwald, J.E. Role of sentinel lymph node biopsy in patients with thin melanoma. J. Natl. Compr. Canc. Netw., 2009, 7(3), 308-317.
[http://dx.doi.org/10.6004/jnccn.2009.0023] [PMID: 19401063]
[11]
Cordeiro, E.; Gervais, M.K.; Shah, P.S.; Look Hong, N.J.; Wright, F.C. Sentinel Lymph Node Biopsy in Thin Cutaneous Melanoma: A Systematic Review and Meta-Analysis. Ann. Surg. Oncol., 2016, 23(13), 4178-4188.
[http://dx.doi.org/10.1245/s10434-016-5137-z] [PMID: 26932710]
[12]
Gershenwald, J.E.; Scolyer, R.A.; Hess, K.R.; Sondak, V.K.; Long, G.V.; Ross, M.I.; Lazar, A.J.; Faries, M.B.; Kirkwood, J.M.; McArthur, G.A.; Haydu, L.E.; Eggermont, A.M.M.; Flaherty, K.T.; Balch, C.M.; Thompson, J.F. American Joint Committee on Cancer Melanoma Expert, P.; the International Melanoma, D.; Discovery, P., Melanoma staging: Evidence-based changes in the American Joint Committee on Cancer eighth edition cancer staging manual. CA Cancer J Clin,, 2017, 67(6), 472-492.
[13]
Gyorki, D.E.; Sanelli, A.; Herschtal, A.; Lazarakis, S.; McArthur, G.A.; Speakman, D.; Spillane, J.; Henderson, M.A. Sentinel Lymph Node Biopsy in T4 Melanoma: An Important Risk-Stratification Tool. Ann. Surg. Oncol., 2016, 23(2), 579-584.
[http://dx.doi.org/10.1245/s10434-015-4894-4] [PMID: 26471491]
[14]
Borgognoni, L.; Sestini, S.; Gerlini, G.; Brandani, P.; Chiarugi, C.; Gelli, R.; Giannotti, V.; Crocetti, E. Sentinel Lymph Node Status is a Main Prognostic Parameter Needful for the Correct Staging of Patients with Melanoma Thicker than 4 mm: Single-Institution Experience and Literature Meta-Analysis. Journal of investigative surgery : the official journal of the Academy of Surgical Research,, 2017, 1-11.
[15]
Sondak, V.K.; Zager, J.S. Who is to blame for false-negative sentinel node biopsies in melanoma? Ann. Surg. Oncol., 2010, 17(3), 670-673.
[http://dx.doi.org/10.1245/s10434-009-0857-y] [PMID: 19953329]
[16]
Nieweg, O.E. False-negative sentinel node biopsy. Ann. Surg. Oncol., 2009, 16(8), 2089-2091.
[http://dx.doi.org/10.1245/s10434-009-0540-3] [PMID: 19521734]
[17]
Pappalardo, M.; Cheng, M-H. Abstract: A New Lymphoscintigraphy Staging for Unilateral Extremity Lymphedema Validation and Correlation between Nuclear Images and Clinical Findings. Plast. Reconstr. Surg. Glob. Open, 2018, 6(8S), 74-75.
[18]
Cheng, M.H.; Pappalardo, M.; Lin, C.; Kuo, C.F.; Lin, C.Y.; Chung, K.C. Validity of the Novel Taiwan Lymphoscintigraphy Staging and Correlation of Cheng Lymphedema Grading for Unilateral Extremity Lymphedema. Ann. Surg., 2018, 268(3), 513-525.
[19]
Pappalardo, M.; Cheng, M.H. Lymphoscintigraphy for the diagnosis of extremity lymphedema: Current controversies regarding protocol, interpretation, and clinical application. J. Surg. Oncol., 2019. Jun 18[Epub ahead of print]
[20]
Valdes Olmos, R.A.; Vidal-Sicart, S.; Manca, G.; Mariani, G.; Leon-Ramirez, L.F.; Rubello, D.; Giammarile, F. Advances in radioguided surgery in oncology. The quarterly journal of nuclear medicine and molecular imaging: official publication of the Italian Association of Nuclear Medicine (AIMN) [and] the International Association of Radiopharmacology (IAR). Section of the So, 2017, 61(3), 247-270. [and].
[21]
Alvarez Paez, A.M.; Brouwer, O.R.; Veenstra, H.J.; van der Hage, J.A.; Wouters, M.; Nieweg, O.E.; Valdés-Olmos, R.A. Decisive role of SPECT/CT in localization of unusual periscapular sentinel nodes in patients with posterior trunk melanoma: three illustrative cases and a review of the literature. Melanoma Res., 2012, 22(3), 278-283.
[http://dx.doi.org/10.1097/CMR.0b013e32835312b1] [PMID: 22456165]
[22]
Chapman, B.C.; Gleisner, A.; Kwak, J.J.; Hosokawa, P.; Paniccia, A.; Merkow, J.S.; Koo, P.J.; Gajdos, C.; Pearlman, N.W.; McCarter, M.D.; Kounalakis, N. SPECT/CT Improves Detection of Metastatic Sentinel Lymph Nodes in Patients with Head and Neck Melanoma. Ann. Surg. Oncol., 2016, 23(8), 2652-2657.
[http://dx.doi.org/10.1245/s10434-016-5175-6] [PMID: 26983744]
[23]
Manca, G.; Romanini, A.; Pellegrino, D.; Borsò, E.; Rondini, M.; Orlandini, C.; Zucchi, V.; Pasqualetti, F.; Mariani, G. Optimal detection of sentinel lymph node metastases by intraoperative radioactive threshold and molecular analysis in patients with melanoma. J. Nucl. Med., 2008, 49(11), 1769-1775.
[http://dx.doi.org/10.2967/jnumed.108.055350] [PMID: 18927334]
[24]
Martin, R.C., II; Edwards, M.J.; Wong, S.L.; Tuttle, T.M.; Carlson, D.J.; Brown, C.M.; Noyes, R.D.; Glaser, R.L.; Vennekotter, D.J.; Turk, P.S.; Tate, P.S.; Sardi, A.; Cerrito, P.B.; McMasters, K.M. For the University of Louisville Breast Cancer Study Group.Practical guidelines for optimal gamma probe detection of sentinel lymph nodes in breast cancer: results of a multi-institutional study. Surgery, 2000, 128(2), 139-144.
[http://dx.doi.org/10.1067/msy.2000.108064] [PMID: 10922983]
[25]
McMasters, K.M.; Reintgen, D.S.; Ross, M.I.; Wong, S.L.; Gershenwald, J.E.; Krag, D.N.; Noyes, R.D.; Viar, V.; Cerrito, P.B.; Edwards, M.J. Sentinel lymph node biopsy for melanoma: how many radioactive nodes should be removed? Ann. Surg. Oncol., 2001, 8(3), 192-197.
[http://dx.doi.org/10.1007/s10434-001-0192-4] [PMID: 11314933]
[26]
Morton, D.L.; Thompson, J.F.; Cochran, A.J.; Mozzillo, N.; Nieweg, O.E.; Roses, D.F.; Hoekstra, H.J.; Karakousis, C.P.; Puleo, C.A.; Coventry, B.J.; Kashani-Sabet, M.; Smithers, B.M.; Paul, E.; Kraybill, W.G.; McKinnon, J.G.; Wang, H-J.; Elashoff, R.; Faries, M.B. MSLT Group. Final trial report of sentinel-node biopsy versus nodal observation in melanoma. N. Engl. J. Med., 2014, 370(7), 599-609.
[http://dx.doi.org/10.1056/NEJMoa1310460] [PMID: 24521106]
[27]
Chakera, A.H.; Hesse, B.; Burak, Z.; Ballinger, J.R.; Britten, A.; Caracò, C.; Cochran, A.J.; Cook, M.G.; Drzewiecki, K.T.; Essner, R.; Even-Sapir, E.; Eggermont, A.M.; Stopar, T.G.; Ingvar, C.; Mihm, M.C., Jr; McCarthy, S.W.; Mozzillo, N.; Nieweg, O.E.; Scolyer, R.A.; Starz, H.; Thompson, J.F.; Trifirò, G.; Viale, G.; Vidal-Sicart, S.; Uren, R.; Waddington, W.; Chiti, A.; Spatz, A.; Testori, A. European Association of Nuclear Medicine-European Organisation for Research and. EANM-EORTC general recommendations for sentinel node diagnostics in melanoma. Eur. J. Nucl. Med. Mol. Imaging, 2009, 36(10), 1713-1742.
[http://dx.doi.org/10.1007/s00259-009-1228-4] [PMID: 19714329]
[28]
Marghoob, A.A.; Koenig, K.; Bittencourt, F.V.; Kopf, A.W.; Bart, R.S. Breslow thickness and clark level in melanoma: support for including level in pathology reports and in American Joint Committee on Cancer Staging. Cancer, 2000, 88(3), 589-595.
[http://dx.doi.org/10.1002/(SICI)1097-0142(20000201)88:3<589:AID-CNCR15>3.0.CO;2-I] [PMID: 10649252]
[29]
Beasley, G.M.; Hu, Y.; Youngwirth, L.; Scheri, R.P.; Salama, A.K.; Rossfeld, K.; Gardezi, S.; Agnese, D.M.; Howard, J.H.; Tyler, D.S.; Slingluff, C.L., Jr; Terando, A.M. Sentinel Lymph Node Biopsy for Recurrent Melanoma: A Multicenter Study. Ann. Surg. Oncol., 2017, 24(9), 2728-2733.
[http://dx.doi.org/10.1245/s10434-017-5883-6] [PMID: 28508145]
[30]
Beasley, G.M.; Speicher, P.; Sharma, K.; Seigler, H.; Salama, A.; Mosca, P.; Tyler, D.S. Efficacy of repeat sentinel lymph node biopsy in patients who develop recurrent melanoma. J. Am. Coll. Surg., 2014, 218(4), 686-692.
[http://dx.doi.org/10.1016/j.jamcollsurg.2013.12.025] [PMID: 24529806]
[31]
Balch, C.M.; Soong, S.J.; Gershenwald, J.E.; Thompson, J.F.; Reintgen, D.S.; Cascinelli, N.; Urist, M.; McMasters, K.M.; Ross, M.I.; Kirkwood, J.M.; Atkins, M.B.; Thompson, J.A.; Coit, D.G.; Byrd, D.; Desmond, R.; Zhang, Y.; Liu, P.Y.; Lyman, G.H.; Morabito, A. Prognostic factors analysis of 17,600 melanoma patients: validation of the American Joint Committee on Cancer melanoma staging system. J. Clin. Oncol., 2001, 19(16), 3622-3634.
[http://dx.doi.org/10.1200/JCO.2001.19.16.3622] [PMID: 11504744]
[32]
Gershenwald, J.E.; Thompson, W.; Mansfield, P.F.; Lee, J.E.; Colome, M.I.; Tseng, C.H.; Lee, J.J.; Balch, C.M.; Reintgen, D.S.; Ross, M.I. Multi-institutional melanoma lymphatic mapping experience: the prognostic value of sentinel lymph node status in 612 stage I or II melanoma patients. J. Clin. Oncol., 1999, 17(3), 976-983.
[http://dx.doi.org/10.1200/JCO.1999.17.3.976] [PMID: 10071292]
[33]
Statius Muller, M.G.; van Leeuwen, P.A.; de Lange-De Klerk, E.S.; van Diest, P.J.; Pijpers, R.; Ferwerda, C.C.; Vuylsteke, R.J.; Meijer, S. The sentinel lymph node status is an important factor for predicting clinical outcome in patients with Stage I or II cutaneous melanoma. Cancer, 2001, 91(12), 2401-2408.
[http://dx.doi.org/10.1002/1097-0142(20010615)91:12<2401:AID-CNCR1274>3.0.CO;2-I] [PMID: 11413531]
[34]
Morton, D.L.; Thompson, J.F.; Cochran, A.J.; Mozzillo, N.; Elashoff, R.; Essner, R.; Nieweg, O.E.; Roses, D.F.; Hoekstra, H.J.; Karakousis, C.P.; Reintgen, D.S.; Coventry, B.J.; Glass, E.C.; Wang, H.J. MSLT Group. Sentinel-node biopsy or nodal observation in melanoma. N. Engl. J. Med., 2006, 355(13), 1307-1317.
[http://dx.doi.org/10.1056/NEJMoa060992] [PMID: 17005948]
[35]
Uren, R.F.; Howman-Giles, R.; Chung, D.; Thompson, J.F. Guidelines for lymphoscintigraphy and F18 FDG PET scans in melanoma. J. Surg. Oncol., 2011, 104(4), 405-419.
[http://dx.doi.org/10.1002/jso.21770] [PMID: 21858836]
[36]
Mahieu-Renard, L.; Cammilleri, S.; Giorgi, R.; Gaudy-Marqueste, C.; Mundler, O.; Richard, M.A.; Grob, J.J. Slow dynamics of lymphoscintigraphic mapping is associated to the negativity of the sentinel node in melanoma patients. Ann. Surg. Oncol., 2008, 15(10), 2878-2886.
[http://dx.doi.org/10.1245/s10434-008-0080-2] [PMID: 18696157]
[37]
Nathanson, S.D.; Nelson, L.; Karvelis, K.C. Rates of flow of technetium 99m--labeled human serum albumin from peripheral injection sites to sentinel lymph nodes. Ann. Surg. Oncol., 1996, 3(4), 329-335.
[http://dx.doi.org/10.1007/BF02305661] [PMID: 8790844]
[38]
Uren, R.F.; Hawman-Giles, R.; Thompson, J.F. Variation in cutaneous lymphatic flow rates. Ann. Surg. Oncol., 1997, 4(3), 279-281.
[http://dx.doi.org/10.1007/BF02306624] [PMID: 9142392]
[39]
Uren, R.F.; Howman-Giles, R.B.; Thompson, J.F.; Roberts, J.; Bernard, E. Variability of cutaneous lymphatic flow rates in melanoma patients. Melanoma Res., 1998, 8(3), 279-282.
[http://dx.doi.org/10.1097/00008390-199806000-00012] [PMID: 9664151]
[40]
Nathanson, S.D.; Anaya, P.; Avery, M.; Hetzel, F.W.; Sarantou, T.; Havstad, S. Sentinel lymph node metastasis in experimental melanoma: relationships among primary tumor size, lymphatic vessel diameter and 99mTc-labeled human serum albumin clearance. Ann. Surg. Oncol., 1997, 4(2), 161-168.
[http://dx.doi.org/10.1007/BF02303800] [PMID: 9084854]
[41]
Harrell, M.I.; Iritani, B.M.; Ruddell, A. Tumor-induced sentinel lymph node lymphangiogenesis and increased lymph flow precede melanoma metastasis. Am. J. Pathol., 2007, 170(2), 774-786.
[http://dx.doi.org/10.2353/ajpath.2007.060761] [PMID: 17255343]
[42]
Ruddell, A.; Harrell, M.I.; Minoshima, S.; Maravilla, K.R.; Iritani, B.M.; White, S.W.; Partridge, S.C. Dynamic contrast-enhanced magnetic resonance imaging of tumor-induced lymph flow. Neoplasia (New York, N.Y.),, 2008, 10(7), 706-713.
[http://dx.doi.org/10.1593/neo.08342]
[43]
Paduch, R. The role of lymphangiogenesis and angiogenesis in tumor metastasis. Cell Oncol. (Dordr.), 2016, 39(5), 397-410.
[http://dx.doi.org/10.1007/s13402-016-0281-9] [PMID: 27126599]
[44]
Shields, J.D.; Borsetti, M.; Rigby, H.; Harper, S.J.; Mortimer, P.S.; Levick, J.R.; Orlando, A.; Bates, D.O. Lymphatic density and metastatic spread in human malignant melanoma. Br. J. Cancer, 2004, 90(3), 693-700.
[http://dx.doi.org/10.1038/sj.bjc.6601571] [PMID: 14760386]
[45]
Maza, S.; Valencia, R.; Geworski, L.; Sandrock, D.; Zander, A.; Audring, H.; Dräger, E.; Winter, H.; Sterry, W.; Munz, D.L. Influence of fast lymphatic drainage on metastatic spread in cutaneous malignant melanoma: a prospective feasibility study. Eur. J. Nucl. Med. Mol. Imaging, 2003, 30(4), 538-544.
[http://dx.doi.org/10.1007/s00259-003-1114-4] [PMID: 12582814]
[46]
Cammilleri, S.; Jacob, T.; Rojat-Habib, M.C.; Hesse, S.; Berthet, B.; Giorgi, R.; Bonerandi, J.J.; Mundler, O. High negative predictive value of slow lymphatic drainage on metastatic node spread detection in malignant limb and trunk cutaneous melanoma. Bull. Cancer, 2004, 91(7-8), E225-E228.
[PMID: 15381460]
[47]
Toubert, M.E.; Just, P.A.; Baillet, G.; Kerob, D.; Hindié, E.; Verola, O.; Revol, M.; Servant, J.M.; Basset-Seguin, N.; Lebbé, C.; Banti, E.; Rubello, D.; Moretti, J.L. Slow dynamic lymphoscintigraphy is not a reliable predictor of sentinel-node negativity in cutaneous melanoma. Cancer Biother. Radiopharm., 2008, 23(4), 443-450.
[http://dx.doi.org/10.1089/cbr.2008.0468] [PMID: 18771348]
[48]
Akhras, V.; Stanton, A.W.; Levick, J.R.; Mortimer, P.S. A quantitative examination of lymph drainage from perilesion skin in human melanoma. Lymphat. Res. Biol., 2012, 10(3), 107-111.
[http://dx.doi.org/10.1089/lrb.2012.0009] [PMID: 22984906]
[49]
Richtig, E.; Komericki, P.; Trapp, M.; Ott, A.; Bisail, B.; Egger, J. W.; Zalaudek, I. Ratio of marked and excised sentinel lymph nodes and scintigraphic appearance time in melanoma patients with negative sentinel lymph node. Eur. J. Surg. Oncol.; The journal of the European Society of Surgical Oncology and the British Association of Surgical Oncology,, 2010, 36(8), 783-8.
[http://dx.doi.org/10.1016/j.ejso.2010.05.003]
[50]
Conway, W.C.; Faries, M.B.; Nicholl, M.B.; Terando, A.M.; Glass, E.C.; Sim, M.; Morton, D.L. Age-related lymphatic dysfunction in melanoma patients. Ann. Surg. Oncol., 2009, 16(6), 1548-1552.
[http://dx.doi.org/10.1245/s10434-009-0420-x] [PMID: 19277787]
[51]
Glass, E.C.; Essner, R.; Morton, D.L. Kinetics of three lymphoscintigraphic agents in patients with cutaneous melanoma. J. Nucl. Med., 1998, 39(7), 1185-1190.
[PMID: 9669391]
[52]
Nathanson, S.D. Insights into the mechanisms of lymph node metastasis. Cancer, 2003, 98(2), 413-423.
[http://dx.doi.org/10.1002/cncr.11464] [PMID: 12872364]
[53]
Ogasawara, Y.; Ikeda, H.; Takahashi, M.; Kawasaki, K.; Doihara, H. Evaluation of breast lymphatic pathways with indocyanine green fluorescence imaging in patients with breast cancer. World J. Surg., 2008, 32(9), 1924-1929.
[http://dx.doi.org/10.1007/s00268-008-9519-7] [PMID: 18330628]
[54]
Uren, R.F.; Howman-Giles, R.B.; Chung, D.; Thompson, J.F. Role of lymphoscintigraphy for selective sentinel lymphadenectomy. Cancer Treat. Res., , 2005, 127, 15-38.
[http://dx.doi.org/10.1007/0-387-23604-X_2] [PMID: 16209076]
[55]
Mariani, G.; Gipponi, M.; Moresco, L.; Villa, G.; Bartolomei, M.; Mazzarol, G.; Bagnara, M.C.; Romanini, A.; Cafiero, F.; Paganelli, G.; Strauss, H.W. Radioguided sentinel lymph node biopsy in malignant cutaneous melanoma. J. Nucl. Med., 2002, 43(6), 811-827.
[PMID: 12050328]
[56]
Fujiwara, M.; Sawada, M.; Kasuya, A.; Matsushita, Y.; Yamada, M.; Fukamizu, H.; Magata, Y.; Tokura, Y.; Sakahara, H. Measurement of cutaneous lymphatic flow rates in patients with skin cancer: area extraction method. J. Dermatol., 2014, 41(6), 498-504.
[http://dx.doi.org/10.1111/1346-8138.12506] [PMID: 24909211]
[57]
Fujiwara, M.; Suzuki, T.; Takiguchi, T.; Fukamizu, H.; Tokura, Y. Lymphatic transit rate as a novel predictive parameter for nodal metastasis in primary truncal skin cancers. J. Dermatol., 2016, 43(2), 170-174.
[http://dx.doi.org/10.1111/1346-8138.13033] [PMID: 26211740]
[58]
Fujiwara, M.; Suzuki, T.; Kasuya, A.; Shimauchi, T.; Fukamizu, H.; Tokura, Y. Lymphatic transit rate as a predictive parameter for nodal metastasis in primary limb malignant melanoma. J. Dermatol. Sci., 2018, 90(1), 27-34.
[http://dx.doi.org/10.1016/j.jdermsci.2017.12.013] [PMID: 29289416]
[59]
Solari, N.; Gipponi, M.; Stella, M.; Queirolo, P.; di Somma, C.; Villa, G.; Piccardo, A.; Gualco, M.; Cardinale, F.; Cafiero, F. Predictive role of preoperative lymphoscintigraphy on the status of the sentinel lymph node in clinically node-negative patients with cutaneous melanoma. Melanoma Res., 2009, 19(4), 243-251.
[http://dx.doi.org/10.1097/CMR.0b013e32832e0b9a] [PMID: 19584766]
[60]
Ho, A.M.; Avery, R.; Krupinski, E.A.; Warneke, J.; Kuo, P.H. Predictive role of imaging in sentinel lymph node dissection for melanoma. Lymphology, 2014, 47(3), 134-141.
[PMID: 25420306]
[61]
Howard, J.H.; Ozao-Choy, J.J.; Hiles, J.M.; Sim, M.S.; Faries, M.B. Prognostic Value of Multiple Draining Lymph Node Basins in Melanoma: A Matched-Pair Analysis Based on the John Wayne Cancer Institute Experience. Front. Oncol., 2017, 7, 172.
[http://dx.doi.org/10.3389/fonc.2017.00172] [PMID: 28856118]
[62]
Dale, P.S.; Foshag, L.J.; Wanek, L.A.; Morton, D.L. Metastasis of primary melanoma to two separate lymph node basins: prognostic significance. Ann. Surg. Oncol., 1997, 4(1), 13-18.
[http://dx.doi.org/10.1007/BF02316805] [PMID: 8985512]
[63]
Federico, A. C.; Chagpar, A. B.; Ross, M. I.; Martin, R. C.; Noyes, R. D.; Goydos, J. S.; Beitsch, P. D.; Urist, M. M.; Ariyan, S.; Sussman, J. J.; McMasters, K. M.; Scoggins, C. R. Effect of multiplenodal basin drainage on cutaneous melanoma. rchives of surgery (Chicago, Ill. : 1960)., 2008, 632(7), 632-7. discussion 637-8.
[http://dx.doi.org/10.1001/archsurg.143.7.632]
[64]
McHugh, J.B.; Su, L.; Griffith, K.A.; Schwartz, J.L.; Wong, S.L.; Cimmino, V.; Chang, A.E.; Johnson, T.M.; Sabel, M.S. Significance of multiple lymphatic basin drainage in truncal melanoma patients undergoing sentinel lymph node biopsy. Ann. Surg. Oncol., 2006, 13(9), 1216-1223.
[http://dx.doi.org/10.1245/s10434-006-9014-z] [PMID: 16952026]
[65]
Persico, M.G.; Lodola, L.; Buroni, F.E.; Morandotti, M.; Pallavicini, P.; Aprile, C. (99m)Tc-human serum albumin nanocolloids: particle sizing and radioactivity distribution. J. Labelled Comp. Radiopharm., 2015, 58(9), 376-382.
[http://dx.doi.org/10.1002/jlcr.3317] [PMID: 26198778]
[66]
Cheng, G.; Kurita, S.; Torigian, D.A.; Alavi, A. Current status of sentinel lymph-node biopsy in patients with breast cancer. Eur. J. Nucl. Med. Mol. Imaging, 2011, 38(3), 562-575.
[http://dx.doi.org/10.1007/s00259-010-1577-z] [PMID: 20700739]
[67]
AGENCY. I. A. E., Radiopharmaceuticals for Sentinel Lymph Node Detection: Status and Trends; INTERNATIONAL ATOMIC ENERGY AGENCY: Vienna, 2015.
[68]
Hoh, C.K.; Wallace, A.M.; Vera, D.R. Preclinical studies of [99mTc]DTPA-mannosyl-dextran☆☆☆Supported in part by National Cancer Institute Grant CA72751 and University of California Breast Cancer Research Program Grants 2RB-0018 and 4IB-0051. Nucl. Med. Biol., 2003, 30(5), 457-464.
[http://dx.doi.org/10.1016/S0969-8051(03)00028-3] [PMID: 12831982]
[69]
Silvestri, C.; Christopher, A.; Intenzo, C.; Kairys, J.C.; Kim, S.; Willis, A.; Berger, A.C. Consecutive case series of melanoma sentinel node biopsy for Lymphoseek compared to sulfur colloids. J. Surg. Res., 2019, 233, 149-153.
[http://dx.doi.org/10.1016/j.jss.2018.07.042] [PMID: 30502241]
[70]
Wallace, A.M.; Hoh, C.K.; Ellner, S.J.; Darrah, D.D.; Schulteis, G.; Vera, D.R. Lymphoseek: a molecular imaging agent for melanoma sentinel lymph node mapping. Ann. Surg. Oncol., 2007, 14(2), 913-921.
[http://dx.doi.org/10.1245/s10434-006-9099-4] [PMID: 17146742]
[71]
Leong, S.P.; Kim, J.; Ross, M.; Faries, M.; Scoggins, C.R.; Metz, W.L.; Cope, F.O.; Orahood, R.C. A phase 2 study of (99m)Tc-tilmanocept in the detection of sentinel lymph nodes in melanoma and breast cancer. Ann. Surg. Oncol., 2011, 18(4), 961-969.
[http://dx.doi.org/10.1245/s10434-010-1524-z] [PMID: 21331809]
[72]
Sondak, V.K.; King, D.W.; Zager, J.S.; Schneebaum, S.; Kim, J.; Leong, S.P.; Faries, M.B.; Averbook, B.J.; Martinez, S.R.; Puleo, C.A.; Messina, J.L.; Christman, L.; Wallace, A.M. Combined analysis of phase III trials evaluating [99mTc]tilmanocept and vital blue dye for identification of sentinel lymph nodes in clinically node-negative cutaneous melanoma. Ann. Surg. Oncol., 2013, 20(2), 680-688.
[http://dx.doi.org/10.1245/s10434-012-2612-z] [PMID: 23054107]
[73]
Benke, M.; Wocial, K.; Lewandowska, W.; Rutkowski, P.; Teterycz, P.; Jarek, P.; Dedecjus, M. Value of planar lymphoscintigraphy (PL) versus SPECT/CT in evaluation of sentinel lymph node in trunk melanoma - one center, large series retrospective study. Nucl. Med. Rev. Cent. East. Eur., 2018, 21(2), 79-84.
[http://dx.doi.org/10.5603/NMR.a2018.0022] [PMID: 29956817]
[74]
Stoffels, I.; Boy, C.; Pöppel, T.; Kuhn, J.; Klötgen, K.; Dissemond, J.; Schadendorf, D.; Klode, J. Association between sentinel lymph node excision with or without preoperative SPECT/CT and metastatic node detection and disease-free survival in melanoma. JAMA, 2012, 308(10), 1007-1014.
[http://dx.doi.org/10.1001/2012.jama.11030] [PMID: 22968889]
[75]
Jimenez-Heffernan, A.; Ellmann, A.; Sado, H.; Huić, D.; Bal, C.; Parameswaran, R.; Giammarile, F.; Pruzzo, R.; Kostadinova, I.; Vorster, M.; Almeida, P.; Santiago, J.; Gambhir, S.; Sergieva, S.; Calderon, A.; Young, G.O.; Valdes-Olmos, R.; Zaknun, J.; Magboo, V.P.; Pascual, T.N. Results of a Prospective Multicenter International Atomic Energy Agency Sentinel Node Trial on the Value of SPECT/CT Over Planar Imaging in Various Malignancies. J. Nucl. Med., 2015, 56(9), 1338-1344.
[http://dx.doi.org/10.2967/jnumed.114.153643] [PMID: 26229148]
[76]
Vermeeren, L.; Valdés Olmos, R.A.; Klop, W.M.; Balm, A.J.; van den Brekel, M.W. A portable gamma-camera for intraoperative detection of sentinel nodes in the head and neck region. J. Nucl. Med., 2010, 51(5), 700-703.
[http://dx.doi.org/10.2967/jnumed.109.071407] [PMID: 20395319]
[77]
Vermeeren, L.; Valdés Olmos, R.A.; Klop, W.M.; van der Ploeg, I.M.; Nieweg, O.E.; Balm, A.J.; van den Brekel, M.W. SPECT/CT for sentinel lymph node mapping in head and neck melanoma. Head Neck, 2011, 33(1), 1-6.
[http://dx.doi.org/10.1002/hed.21392] [PMID: 20848414]
[78]
Vidal-Sicart, S.; Paredes, P.; Zanón, G.; Pahisa, J.; Martinez-Román, S.; Caparrós, X.; Vilalta, A.; Rull, R.; Pons, F. Added value of intraoperative real-time imaging in searches for difficult-to-locate sentinel nodes. J. Nucl. Med., 2010, 51(8), 1219-1225.
[http://dx.doi.org/10.2967/jnumed.110.074880] [PMID: 20660385]
[79]
KleinJan,G.H.; Karakullukçu, B.; Klop, W.M.C.; Engelen, T.; van den Berg, N.S.; van Leeuwen, F.W.B. Introducing navigation during melanoma-related sentinel lymph node procedures in the head-and-neck region. EJNMMI Res., 2017, 7(1), 65.
[http://dx.doi.org/10.1186/s13550-017-0312-1] [PMID: 28819936]
[80]
Marshall, M.V.; Rasmussen, J.C.; Tan, I.C.; Aldrich, M.B.; Adams, K.E.; Wang, X.; Fife, C.E.; Maus, E.A.; Smith, L.A.; Sevick-Muraca, E.M. Near-Infrared Fluorescence Imaging in Humans with Indocyanine Green: A Review and Update. Open surgical oncology journal (Online), 2010, 2(2), 12-25.
[81]
Frontado, L.M.; Brouwer, O.R.; van den Berg, N.S.; Mathéron, H.M.; Vidal-Sicart, S.; van Leeuwen, F.W.; Valdés Olmos, R.A. Added value of the hybrid tracer indocyanine green-99mTc-nanocolloid for sentinel node biopsy in a series of patients with different lymphatic drainage patterns. Rev. Esp. Med. Nucl. Imagen Mol., 2013, 32(4), 227-233.
[http://dx.doi.org/10.1016/j.remnie.2013.05.015] [PMID: 23567320]
[82]
de Bree, R.; Pouw, B.; Heuveling, D.A.; Castelijns, J.A. Fusion of Freehand SPECT and Ultrasound to Perform Ultrasound-Guided Fine-Needle Aspiration Cytology of Sentinel Nodes in Head and Neck Cancer. AJNR Am. J. Neuroradiol., 2015, 36(11), 2153-2158.
[http://dx.doi.org/10.3174/ajnr.A4426] [PMID: 26294647]
[83]
Bugby, S.L.; Lees, J.E.; Perkins, A.C. Hybrid intraoperative imaging techniques in radioguided surgery: present clinical applications and future outlook. Clin. Transl. Imaging, 2017, 5(4), 323-341.
[http://dx.doi.org/10.1007/s40336-017-0235-x] [PMID: 28804703]


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VOLUME: 13
ISSUE: 1
Year: 2020
Page: [32 - 41]
Pages: 10
DOI: 10.2174/1874471012666191015100837

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