Liver volumetry improves evaluation of treatment response to hepatic artery infusion chemotherapy in uveal melanoma patients with liver metastases

Zensen, Sebastian; Steinberg-Vorhoff, Hannah L; Milosevic, Aleksandar; Richly, Heike; Siveke, Jens T; Opitz, Marcel; Haubold, Johannes; Li, Yan; Forsting, Michael; Schaarschmidt, Benedikt Michael

doi:10.2478/raon-2024-0063

Abstract

Background

In uveal melanoma patients, short-term evaluation of treatment response to hepatic artery infusion chemotherapy (HAIC) using the Response Evaluation Criteria in Solid Tumors (RECIST) 1.1 criteria is challenging due to the diffuse metastatic spread. As liver enlargement can frequently be observed, this study aims to compare RECIST 1.1 and liver volumetry (LV) for the evaluation of HAIC treatment response.

Patients and methods

Treatment response was evaluated in 143 patients (mean age 65.1 ± 10.9 years, 54% female) treated by HAIC by RECIST 1.1 and LV on CT imaging performed before and after HAIC. In LV, different increases in liver volume were evaluated to set an effective threshold to distinguish between stable disease (SD) and progressive disease (PD). Overall survival (OS) was calculated as the time from first HAIC to patient death using Kaplan-Meier test and multivariate analysis was performed for RECIST 1.1 and LV.

Results

In the overall population, median OS (mOS) was 13.5 months (95% CI 11.2–15.8 months). In LV, a threshold of 10% increase in liver volume was suited to identify patients with significantly reduced OS (SD: 103/143 patients, mOS 15.9 months; PD: 40/143 patients, 6.6 months; p < 0.001). Compared to RECIST 1.1, LV was the only significant prognostic factor that was able to identify a decreased OS.

Conclusions

In uveal melanoma patients with liver metastases, LV with a threshold for liver volume increase of 10% was suitable to evaluate treatment response and would be able to be used as a valuable add-on or even alternative to RECIST 1.1.

References

Rowcroft A, Loveday BPT, Thomson BNJ, Banting S, Knowles B. Systematic review of liver directed therapy for uveal melanoma hepatic metastases. HPB (Oxford) 2020; 22: 497–505. doi: 10.1016/j.hpb.2019.11.002
Open DOI Search in Google Scholar Back to article
Singh AD, Turell ME, Topham AK. Uveal melanoma: trends in incidence, treatment, and survival. Ophthalmology 2011; 118: 1881–5. doi: 10.1016/j.ophtha.2011.01.040
Open DOI Search in Google Scholar Back to article
Rietschel P, Panageas KS, Hanlon C, Patel A, Abramson DH, Chapman PB. Variates of survival in metastatic uveal melanoma. J Clin Oncol 2005; 23: 8076–80. doi: 10.1200/JCO.2005.02.6534
Open DOI Search in Google Scholar Back to article
Damato BE, Coupland SE. Differences in uveal melanomas between men and women from the British Isles. Eye 2012; 26: 292–9. doi: 10.1038/eye.2011.272
Open DOI Search in Google Scholar Back to article
Diener-West M, Reynolds SM, Agugliaro DJ, Caldwell R, Cumming K, Earle JD, et al. Development of metastatic disease after enrolment in the COMS trials for treatment of choroidal melanoma: Collaborative Ocular Melanoma Study Group Report No. 26. Arch Ophthalmol 2005; 123: 1639–43. doi: 10.1001/archopht.123.12.1639
Open DOI Search in Google Scholar Back to article
Gragoudas ES, Egan KM, Seddon JM, Glynn RJ, Walsh SM, Finn SM, et al. Survival of patents with metastases from uveal melanoma. Ophthalmology 1991; 98: 383–90. doi: 10.1016/s0161-6420(91)32285-1
Open DOI Search in Google Scholar Back to article
Chew AL, Spilsbury K, Isaacs TW. Survival from uveal melanoma in Western Australia 1981–2005. Clin Exp Ophthalmol 2015; 43: 422–8. doi: 10.1111/ceo.12490
Open DOI Search in Google Scholar Back to article
Bedikian AY, Legha SS, Mavligit G, Carrasco CH, Khorana S, Plager C, et al. Treatment of uveal melanoma metastatic to the liver. A review of the M. D. Anderson cancer center experience and prognostic factors. Cancer 1995; 76: 1665–70. doi: 10.1002/1097-0142(19951101)76:9<;1665::aidcncr2820760925>3.0.co;2-j
Open DOI Search in Google Scholar Back to article
Schelhorn J, Richly H, Ruhlmann M, Lauenstein TC, Theysohn JM. A single-center experience in radioembolization as salvage therapy of hepatic metastases of uveal melanoma. Acta Radiol Open 2015; 4: 2047981615570417. doi: 10.1177/2047981615570417
Open DOI Search in Google Scholar Back to article
Heusner TA, Antoch G, Wittkowski-Sterczewski A, Ladd SC, Forsting M, Verhagen R, et al. Transarterial hepatic chemoperfusion of uveal melanoma metastases: survival and response to treatment. RoFo 2011; 183: 1151–60. doi: 10.1055/s-0031-1281743
Open DOI Search in Google Scholar Back to article
Leyvraz S, Piperno-Neumann S, Suciu S, Baurain JF, Zdzienicki M, Testori A, et al. Hepatic intra-arterial versus intravenous fotemustine in patients with liver metastases from uveal melanoma (EORTC 18021): a multicentric randomized trial. Ann Oncol 2014; 25: 742–6. doi: 10.1093/annonc/mdt585
Open DOI Search in Google Scholar Back to article
Duran R, Chapiro J, Frangakis C, Lin M, Schlachter TR, Schernthaner RE, et al. Uveal melanoma metastatic to the liver: the role of quantitative volumetric contrast-enhanced MR imaging in the assessment of early tumor response after transarterial chemoembolization. Transl Oncol 2014; 7: 447–55. doi: 10.1016/j.tranon.2014.05.004
Open DOI Search in Google Scholar Back to article
Erasmus JJ, Gladish GW, Broemeling L, Sabloff BS, Truong MT, Herbst RS, et al. Interobserver and intraobserver variability in measurement of non-small-cell carcinoma lung lesions: implications for assessment of tumor response. J Clin Oncol 2003; 21: 2574–82. doi: 10.1200/JCO.2003.01.144
Open DOI Search in Google Scholar Back to article
Thiesse P, Ollivier L, Di Stefano-Louineau D, Négrier S, Savary J, Pignard K, et al. Response rate accuracy in oncology trials: reasons for interobserver variability. Groupe Français d’Immunothérapie of the Fédération Nationale des Centres de Lutte Contre le Cancer. J Clin Oncol 1997; 15: 3507–14. doi: 10.1200/JCO.1997.15.12.3507
Open DOI Search in Google Scholar Back to article
Koitka S, Gudlin P, Theysohn JM, Oezcelik A, Hoyer DP, Dayangac M, et al. Fully automated preoperative liver volumetry incorporating the anatomical location of the central hepatic vein. Sci Rep 2022; 12: 16479. doi: 10.1038/s41598-022-20778-4
Open DOI Search in Google Scholar Back to article
Zensen S, Opitz MK, Ludwig JM, Haubold J, Richly H, Siveke JT, et al. Radiation dose aspects of hepatic artery infusion chemotherapy in uveal melanoma patients with liver metastases. Cardiovasc Intervent Radiol 2022; 45: 841–5. doi: 10.1007/s00270-022-03130-1
Open DOI Search in Google Scholar Back to article
Pinguet F, Culine S, Bressolle F, Astre C, Serre MP, Chevillard C, et al. A phase I and pharmacokinetic study of melphalan using a 24-hour continuous infusion in patients with advanced malignancies. Clin Cancer Res 2000; 6: 57–63. PMID: 10656432
Search in Google Scholar Back to article
Boone BA, Perkins S, Bandi R, Santos E, McCluskey K, Bartlett DL, et al. Hepatic artery infusion of melphalan in patients with liver metastases from ocular melanoma. J Surg Oncol 2018; 117: 940–6. doi: 10.1002/jso.24984
Open DOI Search in Google Scholar Back to article
Eisenhauer EA, Therasse P, Bogaerts J, Schwartz LH, Sargent D, Ford R, et al. New response evaluation criteria in solid tumours: revised RECIST guideline (version 1.1). Eur J Cancer 2009; 45: 228–47. doi: 10.1016/j.ejca.2008.10.026
Open DOI Search in Google Scholar Back to article
Landis JR, Koch GG. The measurement of observer agreement for categorical data. Biometrics 1977; 33: 159–74. PMID: 843571
Search in Google Scholar Back to article
Karydis I, Gangi A, Wheater MJ, Choi J, Wilson I, Thomas K, et al. Percutaneous hepatic perfusion with melphalan in uveal melanoma: a safe and effective treatment modality in an orphan disease. J Surg Oncol 2018; 117: 1170–8. doi: 10.1002/jso.24956
Open DOI Search in Google Scholar Back to article
Kalkmann J, Forsting M, Stattaus J. Liver volume variations as a parameter to assess therapy response in advanced metastatic liver disease. Onkologie 2011; 34: 30–4. doi: 10.1159/000323373
Open DOI Search in Google Scholar Back to article
Purkiss SF, Williams NS. Growth rate and percentage hepatic replacement of colorectal liver metastases. Br J Surg 1993; 80: 1036–8. doi: 10.1002/bjs.1800800838
Open DOI Search in Google Scholar Back to article
Opitz M, Zensen S, Ludwig JM, Weber M, Alatzides G, Seifert R, et al. Radiation dose aspects and establishment of diagnostic reference levels for90Y radioembolisation during angiographic procedure. J Radiol Prot 2022; 42(3). doi: 10.1088/1361-6498/ac8f9e
Open DOI Search in Google Scholar Back to article
Schaarschmidt BM, Wildgruber M, Kloeckner R, Nie J, Steinle V, Braat AJAT, et al. 90Y Radioembolization in the treatment of neuroendocrine neoplasms: results of an international multicenter retrospective study. J Nucl Med 2022; 63: 679–85. doi: 10.2967/jnumed.121.262561
Open DOI Search in Google Scholar Back to article
Schaarschmidt BM, Kloeckner R, Dertnig T, Demircioglu A, Müller L, Auer TA, et al. Real-life experience in the treatment of intrahepatic cholangiocarcinoma by 90Y radioembolization: a multicenter retrospective study. J Nucl Med 2023; 64: 529–35. doi: 10.2967/jnumed.122.264598
Open DOI Search in Google Scholar Back to article
Krasovitsky M, Lee YC, Sim H-W, Chawla T, Moore H, Moses D, et al. Interobserver and intraobserver variability of RECIST assessment in ovarian cancer. Int J Gynecol Cancer 2022; 32: 656–61. doi: 10.1136/ijgc-2021-003319
Open DOI Search in Google Scholar Back to article
Suzuki C, Torkzad MR, Jacobsson H, Aström G, Sundin A, Hatschek T, et al. Interobserver and intraobserver variability in the response evaluation of cancer therapy according to RECIST and WHO-criteria. Acta Oncol 2010; 49: 509–14. doi: 10.3109/02841861003705794
Open DOI Search in Google Scholar Back to article
Kuhl CK, Alparslan Y, Schmoee J, Sequeira B, Keulers A, Brümmendorf TH, et al. Validity of RECIST Version 1.1 for response assessment in metastatic cancer: a prospective, multireader study. Radiology 2019; 290: 349–56. doi: 10.1148/radiol.2018180648
Open DOI Search in Google Scholar Back to article
Gafita A, Rauscher I, Fendler WP, Murthy V, Hui W, Armstrong WR, et al. Measuring response in metastatic castration-resistant prostate cancer using PSMA PET/CT: comparison of RECIST 1.1, aPCWG3, aPERCIST, PPP, and RECIP 1.0 criteria. Eur J Nucl Med Mol Imaging 2022; 49: 4271–81. doi: 10.1007/s00259-022-05882-x
Open DOI Search in Google Scholar Back to article
Hagen F, Mair A, Bitzer M, Bösmüller H, Horger M. Fully automated whole-liver volume quantification on CT-image data: comparison with manual volumetry using enhanced and unenhanced images as well as two different radiation dose levels and two reconstruction kernels. PloS one 2021; 16: e0255374. doi: 10.1371/journal.pone.0255374
Open DOI Search in Google Scholar Back to article
Cai W, He B, Fan Y, Fang C, Jia F. Comparison of liver volumetry on contrast-enhanced CT images: one semiautomatic and two automatic approaches. J Appl Clin Med Phys 2016; 17: 118–27. doi: 10.1120/jacmp.v17i6.6485
Open DOI Search in Google Scholar Back to article
Suzuki K, Epstein ML, Kohlbrenner R, Garg S, Hori M, Oto A, et al. Quantitative radiology: automated CT liver volumetry compared with interactive volumetry and manual volumetry. AJR Am J Roentgenol 2011; 197: W706–12. doi: 10.2214/AJR.10.5958
Open DOI Search in Google Scholar Back to article