A Preliminary Study for Quantitative Assessment with HFUS (High- Frequency Ultrasound) of Nodular Skin Melanoma Breslow Thickness in Adults Before Surgery: Interdisciplinary Team Experience

Author(s): Alfonso Reginelli*, Maria P. Belfiore, Anna Russo, Fabrizio Turriziani, Elvira Moscarella, Teresa Troiani, Gabriella Brancaccio, Andrea Ronchi, Emilio Giunta, Antonello Sica, Francesco Iovino, Fortunato Ciardiello, Renato Franco, Giuseppe Argenziano, Roberto Grassi, Salvatore Cappabianca

Journal Name: Current Radiopharmaceuticals

Volume 13 , Issue 1 , 2020

Become EABM
Become Reviewer

Graphical Abstract:


Abstract:

Background: Cutaneous melanoma is one of the most severe skin diseases. Nodular melanoma is the second melanoma subtype in order of frequency. The prognosis of skin melanoma depends on the vertical growth of the tumor (Breslow index). For this measurement, excisional biopsy is strongly recommended. This is, however, an invasive procedure and may cause damage to the lymphatic drainage system. The HFUS system, , can be extremely useful for determining tumor thickness in the preoperative phase, given its high resolution capacity. The aim of this preliminary study is to define the role of HFUS for the nodular skin melanoma Breslow thickness in adults before surgery by making a comparison with histological features.

Methods: In this study, 14 melanocytic lesions (8 male and 6 female) were evaluated with dermatoscopic clinical features strongly indicative of nodular melanoma. Out of these, excisional biopsy of 7 lesions was requested. The ultrasounds were performed preoperatively. The images were acquired through the first ultrasound scanner with ultra-high frequency probes (range from 50MHz to 70 MHz) available on the market under the EEC mark (Vevo "MD, FUJIFILM Visual Sonics, Amsterdam, the Netherlands) equipped with a linear probe of 50-70 MHz.

Results: From the ultrasonographic analysis of 14 nodular melanoma thickness was determined for the presence of two hyperechogenic laminae, separated by a hypo / anechoic space. The twelve lesions were in situ while the other two lesions showed ultrasonography for example; the satellite lesions (less than two centimeters from the primary lesion) and in transit (localizable to more than two centimeters from the primary lesion). Four of these lesions were ulcerated. A comparsion was made the 7 lesions on between the thickness calculated with this method, and that obtained on the bioptic piece. The presence of a positive concordance has been evident in all of the cases.

Conclusion: If further studies are needed to support its widespread clinical use, its is believed that, in expert hands and with an interdisciplinary team, HFUS is already capable to reliably calculate a Breslow index in a large majority of patients with cutaneous melanoma.

Keywords: Skin melanoma, nodular skin melanoma, high-frequency ultrasound (HFUS), breslow index.

[1]
Livingstone, E.; Windemuth-Kieselbach, C.; Eigentler, T.K.; Rompel, R.; Trefzer, U.; Nashan, D.; Rotterdam, S.; Ugurel, S.; Schadendorf, D. A first prospective population-based analysis investigating the actual practice of melanoma diagnosis, treatment and follow-up. Eur. J. Cancer, 2011, 47(13), 1977-1989.
[http://dx.doi.org/10.1016/j.ejca.2011.04.029] [PMID: 21612915]
[2]
Haddad, D.; Garvey, E.M.; Mihalik, L.; Pockaj, B.A.; Gray, R.J.; Wasif, N. Preoperative imaging for early-stage cutaneous melanoma: predictors, usage, and utility at a single institution. Am. J. Surg., 2013, 206(6), 979-985.
[http://dx.doi.org/10.1016/j.amjsurg.2013.08.017] [PMID: 24124660]
[3]
Garbe, C.; Peris, K.; Hauschild, A. Diagnosis and treatment of melanoma: European consensus- based interdisciplinary guideline—update 2012. Eur. J. Cancer, 2012, 48, 2375-2390.
[4]
Lassau, N.; Mercier, S.; Koscielny, S. Prognostic value of high- frequency sonography for the preoperative assessment of melanomas. AJR Am. J. Roentgenol., 1999, 172, 457-461.
[http://dx.doi.org/10.2214/ajr.172.2.9930803] [PMID: 9930803]
[5]
Weichenthal, M.; Mohr, P.; Breitbart, E.W. The velocity of ultrasound in human primary melanoma tissue - implications for the clinical use of high resolution sonography. BMC Dermatol., 2001, 1, 1.
[http://dx.doi.org/10.1186/1471-5945-1-1] [PMID: 11445001]
[6]
Kraus, W.; Schramm, P.; Hoede, N. First experiences with a high-resolution ultrasonic scanner in the diagnosis of malignant melanomas. Arch. Dermatol. Res., 1983, 275(4), 235-238.
[http://dx.doi.org/10.1007/BF00416667] [PMID: 6625649]
[7]
Music, M.M.; Hertl, K.; Kadivec, M.; Pavlović, M.D.; Hocevar, M.M.M. Musˇicˇ. Pre-operative ultrasound with a 12-15 MHz linear probe reliably differentiates between melanoma thicker and thinner than 1 mm. J. Eur. Acad. Dermatol. Venereol., 2010, 24(9), 1105-1108.
[PMID: 20236207]
[8]
Catalano, O.; Siani, A. Cutaneous melanoma: role of ultrasound in the assessment of locoregional spread. Curr. Probl. Diagn. Radiol., 2010, 39(1), 30-36.
[http://dx.doi.org/10.1067/j.cpradiol.2009.04.001] [PMID: 19931111]
[9]
Hoffmann, K.; Jung, J.; el Gammal, S.; Altmeyer, P. Malignant melanoma in 20-MHz B scan sonography. Dermatology (Basel), 1992, 185(1), 49-55.
[http://dx.doi.org/10.1159/000247403] [PMID: 1638071]
[10]
Balch, C.M.; Urist, M.M.; Karakousis, C.P.; Smith, T.J.; Temple, W.J.; Drzewiecki, K.; Jewell, W.R.; Bartolucci, A.A.; Mihm, M.C., Jr; Barnhill, R. Efficacy of 2-cm surgical margins for intermediate-thickness melanomas (1 to 4 mm). Results of a multi-institutional randomized surgical trial. Ann. Surg., 1993, 218(3), 262-267.
[http://dx.doi.org/10.1097/00000658-199309000-00005] [PMID: 8373269]
[11]
Brancaccio, G.; Napolitano, S.; Troiani, T.; Franco, R.; Iovino, F.; Reginelli, A.; Ciardiello, F.; Argenziano, G. Eighth American Joint Committee on Cancer (AJCC) melanoma classification: what about stage IIC? Br. J. Dermatol., 2018, 179(6), 1422-1423.
[http://dx.doi.org/10.1111/bjd.17145] [PMID: 30187449]
[12]
Hayashi, K.; Koga, H.; Uhara, H.; Saida, T. High-frequency 30-MHz sonography in preoperative assessment of tumor thickness of primary melanoma: usefulness in determination of surgical margin and indication for sentinel lymph node biopsy. Int. J. Clin. Oncol., 2009, 14(5), 426-430.
[http://dx.doi.org/10.1007/s10147-009-0894-3] [PMID: 19856051]
[13]
Fornage, B.D.; McGavran, M.H.; Duvic, M.; Waldron, C.A. Imaging of the skin with 20-MHz US. Radiology, 1993, 189(1), 69-76.
[http://dx.doi.org/10.1148/radiology.189.1.8372222] [PMID: 8372222]
[14]
Harland, C.C.; Kale, S.G.; Jackson, P.; Mortimer, P.S.; Bamber, J.C. Differentiation of common benign pigmented skin lesions from melanoma by high-resolution ultrasound. Br. J. Dermatol., 2000, 143(2), 281-289.
[http://dx.doi.org/10.1046/j.1365-2133.2000.03652.x] [PMID: 10951134]
[15]
Serrone, L.; Solivetti, F.M.; Thorel, M.F.; Eibenschutz, L.; Donati, P.; Catricalà, C. High frequency ultrasound in the preoperative staging of primary melanoma: a statistical analysis. Melanoma Res., 2002, 12(3), 287-290.
[http://dx.doi.org/10.1097/00008390-200206000-00013] [PMID: 12140386]
[16]
Argenziano, G.; Soyer, H.P.; Chimenti, S.; Talamini, R.; Corona, R.; Sera, F.; Binder, M.; Cerroni, L.; De Rosa, G.; Ferrara, G.; Hofmann-Wellenhof, R.; Landthaler, M.; Menzies, S.W.; Pehamberger, H.; Piccolo, D.; Rabinovitz, H.S.; Schiffner, R.; Staibano, S.; Stolz, W.; Bartenjev, I.; Blum, A.; Braun, R.; Cabo, H.; Carli, P.; De Giorgi, V.; Fleming, M.G.; Grichnik, J.M.; Grin, C.M.; Halpern, A.C.; Johr, R.; Katz, B.; Kenet, R.O.; Kittler, H.; Kreusch, J.; Malvehy, J.; Mazzocchetti, G.; Oliviero, M.; Ozdemir, F.; Peris, K.; Perotti, R.; Perusquia, A.; Pizzichetta, M.A.; Puig, S.; Rao, B.; Rubegni, P.; Saida, T.; Scalvenzi, M.; Seidenari, S.; Stanganelli, I.; Tanaka, M.; Westerhoff, K.; Wolf, I.H.; Braun-Falco, O.; Kerl, H.; Nishikawa, T.; Wolff, K.; Kopf, A.W. Dermoscopy of pigmented skin lesions: results of a consensus meeting via the Internet. J. Am. Acad. Dermatol., 2003, 48(5), 679-693.
[http://dx.doi.org/10.1067/mjd.2003.281] [PMID: 12734496]
[17]
Chang, J.W. Cutaneous melanoma: Taiwan experience and literature review. Chang Gung Med. J., 2010, 33(6), 602-612.
[PMID: 21199605]
[18]
Belfiore, M.P.; Berritto, D.; Iacobellis, F.; Rossi, C.; Nigro, G.; Rotundo, I.L.; Cozzolino, S.; Cappabianca, S.; Rotondo, A.; Grassi, R. A longitudinal study on BIO-14.6hamsters with dilated cardiomyopathy:micro-ecocardiographic evaluation. Cardiovac. Ultrasound., 2011.
[http://dx.doi.org/10.1186/1476-7120-9-39] [PMID: 22151912]
[19]
Samimi, M.; Perrinaud, A.; Naouri, M.; Maruani, A.; Perrodeau, E.; Vaillant, L.; Machet, L. High-resolution ultrasonography assists the differential diagnosis of blue naevi and cutaneous metastases of melanoma. Br. J. Dermatol., 2010, 163(3), 550-556.
[http://dx.doi.org/10.1111/j.1365-2133.2010.09903.x] [PMID: 20545694]
[20]
Rallan, D.; Bush, N.L.; Bamber, J.C.; Harland, C.C. Quantitative discrimination of pigmented lesions using three-dimensional high-resolution ultrasound reflex transmission imaging. J. Invest. Dermatol., 2007, 127(1), 189-195.
[http://dx.doi.org/10.1038/sj.jid.5700554] [PMID: 17068484]
[21]
Srivastava, A.; Hughes, L.E.; Woodcock, J.P.; Laidler, P. Vascularity in cutaneous melanoma detected by Doppler sonography and histology: correlation with tumour behaviour. Br. J. Cancer, 1989, 59(1), 89-91.
[http://dx.doi.org/10.1038/bjc.1989.17] [PMID: 2667611]
[22]
Giovagnorio, F.; Andreoli, C.; De Cicco, M.L. Color Doppler sonography of focal lesions of the skin and subcutaneous tissue. J. Ultrasound Med., 1999, 18(2), 89-93.
[http://dx.doi.org/10.7863/jum.1999.18.2.89] [PMID: 10206814]
[23]
Lassau, N.; Koscielny, S.; Avril, M.F.; Margulis, A.; Duvillard, P.; De Baere, T.; Roche, A.; Leclère, J. Prognostic value of angiogenesis evaluated with high-frequency and color Doppler sonography for preoperative assessment of melanomas. AJR Am. J. Roentgenol., 2002, 178(6), 1547-1551.
[http://dx.doi.org/10.2214/ajr.178.6.1781547] [PMID: 12034636]
[24]
Bessoud, B.; Lassau, N.; Koscielny, S.; Longvert, C.; Avril, M.F.; Duvillard, P.; Rouffiac, V.; Leclère, J.; Roche, A. High-frequency sonography and color Doppler in the management of pigmented skin lesions. Ultrasound Med. Biol., 2003, 29(6), 875-879.
[http://dx.doi.org/10.1016/S0301-5629(03)00035-8] [PMID: 12837502]
[25]
Lassau, N.; Spatz, A.; Avril, M.F.; Tardivon, A.; Margulis, A.; Mamelle, G.; Vanel, D.; Leclere, J. Value of high-frequency US for preoperative assessment of skin tumors. Radiographics, 1997, 17(6), 1559-1565.
[http://dx.doi.org/10.1148/radiographics.17.6.9397463] [PMID: 9397463]
[26]
Berritto, D.; Iacobellis, F.; Rossi, C.; Reginelli, A.; Cappabianca, S.; Grassi, R. Ultra high-frequency ultrasound: New capabilities for nail anatomy exploration. J. Dermatol., 2017, 44(1), 43-46.
[http://dx.doi.org/10.1111/1346-8138.13495] [PMID: 27401024]
[27]
Gambichler, T.; Moussa, G.; Bahrenberg, K.; Vogt, M.; Ermert, H.; Weyhe, D.; Altmeyer, P.; Hoffmann, K. Preoperative ultrasonic assessment of thin melanocytic skin lesions using a 100-MHz ultrasound transducer: a comparative study. Dermatol. Surg., 2007, 33(7), 818-824.
[PMID: 17598847]
[28]
Dancey, A.L.; Mahon, B.S.; Rayatt, S.S. A review of diagnostic imaging in melanoma. J. Plast. Reconstr. Aesthet. Surg., 2008, 61(11), 1275-1283.
[http://dx.doi.org/10.1016/j.bjps.2008.04.034] [PMID: 18694659]
[29]
Guitera, P.; Li, L.X.; Crotty, K.; Fitzgerald, P.; Mellenbergh, R.; Pellacani, G.; Menzies, S.W. Melanoma histological Breslow thickness predicted by 75-MHz ultrasonography. Br. J. Dermatol., 2008, 159(2), 364-369.
[http://dx.doi.org/10.1111/j.1365-2133.2008.08681.x] [PMID: 18565186]
[30]
Wang, S.Q.; Hashemi, P. Noninvasive imaging technologies in the diagnosis of melanoma. Semin. Cutan. Med. Surg., 2010, 29(3), 174-184.
[http://dx.doi.org/10.1016/j.sder.2010.06.006] [PMID: 21051011]
[31]
Machet, L.; Belot, V.; Naouri, M.; Boka, M.; Mourtada, Y.; Giraudeau, B.; Laure, B.; Perrinaud, A.; Machet, M.C.; Vaillant, L. Preoperative measurement of thickness of cutaneous melanoma using high-resolution 20 MHz ultrasound imaging: A monocenter prospective study and systematic review of the literature. Ultrasound Med. Biol., 2009, 35(9), 1411-1420.
[http://dx.doi.org/10.1016/j.ultrasmedbio.2009.03.018] [PMID: 19616369]
[32]
Kaikaris, V.; Samsanavičius, D. Kęstutis Maslauskas; Rimdeika, R.; Valiukevičienė, S.; Makštienė, J.; Pundzius, J. Measurement of melanoma thickness--comparison of two methods: ultrasound versus morphology. J. Plast. Reconstr. Aesthet. Surg., 2011, 64(6), 796-802.
[http://dx.doi.org/10.1016/j.bjps.2010.10.008] [PMID: 21123126]
[33]
Reginelli, A.; D’Andrea, A.; Clemente, A.; Izzo, A.; Urraro, F.; Scala, F.; Nardone, V.; Guida, C.; Scialpi, M.; Cappabianca, S. Does multiparametric US improve diagnostic accuracy in the characterization of small testicular masses? Gland Surg., 2019, 8(Suppl. 3), S136-S141.
[http://dx.doi.org/10.21037/gs.2019.04.03]
[34]
Voit, C.; Van Akkooi, A.C.; Schäfer-Hesterberg, G.; Schoengen, A.; Kowalczyk, K.; Roewert, J.C.; Sterry, W.; Eggermont, A.M. Ultrasound morphology criteria predict metastatic disease of the sentinel nodes in patients with melanoma. J. Clin. Oncol., 2010, 28(5), 847-852.
[http://dx.doi.org/10.1200/JCO.2009.25.7428] [PMID: 20065175]
[35]
Voit, C.A.; van Akkooi, A.C.; Schäfer-Hesterberg, G.; Schoengen, A.; Schmitz, P.I.; Sterry, W.; Eggermont, A.M. 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 melanoma? J. Clin. Oncol., 2009, 27(30), 4994-5000.
[http://dx.doi.org/10.1200/JCO.2008.19.0033] [PMID: 19738131]
[36]
Rubaltelli, L.; Beltrame, V.; Tregnaghi, A.; Scagliori, E.; Frigo, A.C.; Stramare, R. Contrast-enhanced ultrasound for characterizing lymph nodes with focal cortical thickening in patients with cutaneous melanoma. AJR Am. J. Roentgenol., 2011, 196(1), W8-12.
[http://dx.doi.org/10.2214/AJR.10.4711] [PMID: 21178038]
[37]
Barnhill, R.L.; Levy, M.A. Regressing thin cutaneous malignant melanomas (< or = 1.0 mm) are associated with angiogenesis. Am. J. Pathol., 1993, 143(1), 99-104.
[PMID: 7686347]
[38]
Straume, O.; Akslen, L.A. Expresson of vascular endothelial growth factor, its receptors (FLT-1, KDR) and TSP-1 related to microvessel density and patient outcome in vertical growth phase melanomas. Am. J. Pathol., 2001, 159(1), 223-235.
[http://dx.doi.org/10.1016/S0002-9440(10)61688-4] [PMID: 11438469]
[39]
Lassau, N.; Lamuraglia, M.; Koscielny, S.; Spatz, A.; Roche, A.; Leclere, J.; Avril, M.F. Prognostic value of angiogenesis evaluated with high-frequency and colour Doppler sonography for preoperative assessment of primary cutaneous melanomas: correlation with recurrence after a 5 year follow-up period. Cancer Imaging, 2006, 6, 24-29.
[http://dx.doi.org/10.1102/1470-7330.2006.0009] [PMID: 16644502]
[40]
Zappia, M.; Cuomo, G.; Martino, M.T.; Reginelli, A.; Brunese, L. The effect of foot position on Power Doppler Ultrasound grading of Achilles enthesitis. Rheumatol. Int., 2016, 36(6), 871-874.
[http://dx.doi.org/10.1007/s00296-016-3461-z] [PMID: 27002715]
[41]
Marneros, A.G. Tumor angiogenesis in melanoma. Hematol. Oncol. Clin. North Am., 2009, 23(3), 431-446. vii-viii.
[http://dx.doi.org/10.1016/j.hoc.2009.03.007] [PMID: 19464595]
[42]
Curry, R.A.; Tempkin, B.B. Sonography: introduction to Normal Structure and Function, 2015.
[43]
Wortsman, X.; Jemec, G.B.C. Dermatologic Ultrasound with Clinical and Histologic Correlations; Springer, 2013.
[http://dx.doi.org/10.1007/978-1-4614-7184-4]
[44]
Schmid-Wendtner, M.H.; Burgdorf, W. Ultrasound scanning in dermatology. Arch. Dermatol., 2005, 141(2), 217-224.
[http://dx.doi.org/10.1001/archderm.141.2.217] [PMID: 15724019]
[45]
Wortsman, X. Sonography of facial cutaneous basal cell carcinoma: a first-line imaging technique. J. Ultrasound Med., 2013, 32(4), 567-572.
[http://dx.doi.org/10.7863/jum.2013.32.4.567] [PMID: 23525381]
[46]
Sattler, E. [High frequency ultrasound] Hautarzt, 2015, 66(7), 493-498.
[http://dx.doi.org/10.1007/s00105-015-3581-5] [PMID: 25636803]
[47]
Szymańska, E.; Nowicki, A.; Mlosek, K.; Litniewski, J.; Lewandowski, M.; Secomski, W.; Tymkiewicz, R. Skin imaging with high frequency ultrasound - preliminary results. Eur. J. Ultrasound, 2000, 12(1), 9-16.
[http://dx.doi.org/10.1016/S0929-8266(00)00097-5] [PMID: 10996765]
[48]
Perrotta, F.M.; Astorri, D.; Zappia, M.; Reginelli, A.; Brunese, L.; Lubrano, E. An ultrasonographic study of enthesis in early psoriatic arthritis patients naive to traditional and biologic DMARDs treatment. Rheumatol. Int., 2016, 36(11), 1579-1583.
[http://dx.doi.org/10.1007/s00296-016-3562-8] [PMID: 27600991]
[49]
Tikjøb, G.; Kassis, V.; Søndergaard, J. Ultrasonic B-scanning of the human skin. An introduction of a new ultrasonic skin-scanner. Acta Derm. Venereol., 1984, 64(1), 67-70.
[PMID: 6203286]
[50]
Waller, J.M.; Maibach, H.I. Age and skin structure and function, a quantitative approach (I): blood flow, pH, thickness, and ultrasound echogenicity. Skin Res. Technol., 2005, 11(4), 221-235.
[http://dx.doi.org/10.1111/j.0909-725X.2005.00151.x] [PMID: 16221138]
[51]
Szymańska, E.; Maj, M.; Majsterek, M.; Litniewski, J.; Nowicki, A.; Rudnicka, L. [The usefulness of high frequency ultrasonography in dermatological practice--ultrasound features of selected cutaneous lesions]. Pol. Merkuriusz Lek., 2011, 31(181), 37-40.
[PMID: 21870707]
[52]
Lassau, N.; Chami, L.; Chebil, M.; Benatsou, B.; Bidault, S.; Girard, E.; Abboud, G.; Roche, A. Dynamic contrast-enhanced ultrasonography (DCE-US) and anti-angiogenic treatments. Discov. Med., 2011, 11(56), 18-24.
[PMID: 21276407]
[53]
Lassau, N.; Chebil, M.; Chami, L.; Bidault, S.; Girard, E.; Roche, A. Dynamic contrast-enhanced ultrasonography (DCE-US): a new tool for the early evaluation of antiangiogenic treatment. Target. Oncol., 2010, 5(1), 53-58.
[http://dx.doi.org/10.1007/s11523-010-0136-7] [PMID: 20379790]
[54]
Lassau, N.; Chami, L.; Benatsou, B.; Peronneau, P.; Roche, A. Dynamic contrast-enhanced ultrasonography (DCE- US) with quantification of tumor perfusion: a new diagnostic tool to evaluate the early effects of antiangiogenic treatment. Eur. Radiol. Suppl., 2007, 176, F89-F98.
[http://dx.doi.org/10.1007/s10406-007-0233-6]
[55]
Wortsman, X. Sonography of the primary cutaneous melanoma: a review. Radiol. Res. Pract., 2012, 2012814396
[http://dx.doi.org/10.1155/2012/814396] [PMID: 22550586]
[56]
Chami, L.; Lassau, N.; Chebil, M.; Robert, C. Imaging of melanoma: usefulness of ultrasonography before and after contrast injection for diagnosis and early evaluation of treatment. Clin. Cosmet. Investig. Dermatol., 2011, 4, 1-6.
[http://dx.doi.org/10.2147/CCID.S13499] [PMID: 21673868]
[57]
Vilana, R.; Puig, S.; Sanchez, M.; Squarcia, M.; Lopez, A.; Castel, T.; Malvehy, J. Preoperative assessment of cutaneous melanoma thickness using 10-MHz sonography. AJR Am. J. Roentgenol., 2009, 193(3), 639-643.
[http://dx.doi.org/10.2214/AJR.08.1387] [PMID: 19696275]
[58]
Cappabianca, S.; Colella, G.; Russo, A.; Pezzullo, M.; Reginelli, A.; Iaselli, F.; Rotondo, A. Maxillofacial fibrous dysplasia: personal experience with gadoliniumenhanced magnetic resonance imaging. Radiol. Med. (Torino), 2008, 113(8), 1198-1210.
[http://dx.doi.org/10.1007/s11547-008-0329-7] [PMID: 18836864]
[59]
Reginelli, A.; Santagata, M.; Urraro, F.; Somma, F.; Izzo, A.; Cappabianca, S.; Rotondo, A. Foreign bodies in the maxillofacial region: assessment with multidetector computed tomography. Semin. Ultrasound CT MR, 2015, 36(1), 2-7.
[http://dx.doi.org/10.1053/j.sult.2014.10.009] [PMID: 25639172]
[60]
Chini, M.G.; Malafronte, N.; Vaccaro, M.C.; Gualtieri, M.J.; Vassallo, A.; Vasaturo, M.; Castellano, S.; Milite, C.; Leone, A.; Bifulco, G.; De Tommasi, N.; Dal Piaz, F. Identification of Limonol Derivatives as Heat Shock Protein 90 (Hsp90) Inhibitors through a Multidisciplinary Approach. Chemistry, 2016, 22(37), 13236-13250.
[http://dx.doi.org/10.1002/chem.201602242] [PMID: 27492719]


Rights & PermissionsPrintExport Cite as

Article Details

VOLUME: 13
ISSUE: 1
Year: 2020
Page: [48 - 55]
Pages: 8
DOI: 10.2174/1874471012666191007121626

Article Metrics

PDF: 19
HTML: 5
EPUB: 1
PRC: 1