B-Mode Ultrasound and Contrast-Enhanced Ultrasound for the Detection of Splenic Involvement in Hodgkin Lymphoma: A Retrospective Analysis of 112 Patients

Abstract

Purpose To assess splenic involvement using B-mode ultrasound (US) and contrast-enhanced ultrasound (CEUS) compared with standard imaging with contrast-enhanced computerized tomography (CT) / 18-fluorodeoxyglucose positron-emission tomography (PET-CT) in patients with Hodgkin lymphoma.

Materials and Methods Imaging data from 112 patients from 12/2003 to 10/2022 with histologically confirmed Hodgkin lymphoma during staging or relapse were analyzed for splenic lymphoma involvement. In all patients, standard imaging (CT/PET-CT), along with B-mode US and CEUS examinations, was performed. Evidence of focal splenic lesions (FSLs) found by imaging procedures was suggestive of splenic involvement. Follow-up imaging was performed in each patient after treatment, and treatment response indicated definitive splenic involvement.

Results 40 patients (35.7%) were identified by imaging modalities as having splenic involvement, which was confirmed by response during follow-up. Standard CT/PET-CT imaging detected splenic involvement in 36/112 patients (32.1%). FSLs were detected with B-mode US in 38 patients (33.9%) and CEUS in 36 patients (32.1%). The sensitivity of standard imaging, B-mode US, and CEUS was 90%, 95%, and 90%, respectively.

Conclusion B-mode US examination is a diagnostic method used in addition to standard imaging for the detection of splenic involvement in Hodgkin lymphoma. CEUS does not provide additional benefit compared to B-mode US and the standard reference procedure.

Zusammenfassung

Ziel Beurteilung des Milzbefalls (MB) mit B-mode-Ultraschall (US) und kontrastverstärktem Ultraschall (CEUS) im Vergleich zur Standardbildgebung mit kontrastverstärkter Computertomografie (CT)/18-Fluordesoxyglucose-Positronen-Emissionstomografie (PET-CT) bei Patienten mit Hodgkin-Lymphom (HL).

Material und Methode Bei 112 Patienten mit histologisch bestätigtem HL wurde von 12/2003 bis 10/2022 der MB im Rahmen des Staging bei Erstdiagnose oder bei Rezidiv untersucht. Bei allen Patienten wurde eine Standardbildgebung (CT/PET-CT), zusammen mit B-mode-US und CEUS durchgeführt. Der Nachweis von fokalen Milzläsionen (FSLs) war ein Hinweis auf einen MB. Das bildgebende Ansprechen auf die Behandlung sicherte im Verlauf den MB.

Ergebnisse 40 (35,7%) Patienten wiesen einen MB auf. Multiple FSLs konnten bei 38 und eine solitäre FSL bei 2 Patienten dargestellt werden. Ein großnodulärer (>3cm) MB wurde in 7 Fällen (17,5%), ein kleinnodulärer (1–3cm) in 29 (72,5%) und ein diffuser (<1cm) in 4 Fällen (10%) beschrieben. Die Standardbildgebung konnte den MB in 36 Fällen (32,1%), der B-mode-US in 38 (33,9%) und der CEUS in 36 Fällen (32,1%) nachweisen. Die Sensitivität lag bei 90% mit der Standardbildgebung, bei 95% mit dem B-mode-US und bei 90% mit CEUS.

Schlussfolgerungen B-mode-US ist eine zusätzliche Bildgebungsmethode, die einen MB bei HL im Vergleich zur Standardbildgebung mit einer hohen Sensitivität nachweisen kann. Der CEUS bietet keinen zusätzlichen diagnostischen Nutzen – im Vergleich zum B-mode-US und zur Standardbildgebung.

Keywords

Hodgkin Lymphoma - CEUS - b-mode ultrasound - staging - spleen - Contrast-enhanced ultrasound

Publication History

Received: 30 May 2023

Accepted after revision: 28 August 2023

Article published online:
20 October 2023

• References

• 1 Eichenauer DA, Aleman BMP, André M. et al. Hodgkin lymphoma: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Annals of Oncology 2018; 29: iv19-iv29 DOI: 10.1093/annonc/mdy080. (PMID: 29796651)
• 2 Hoppe RT, Advani RH, Ai WZ. et al. Hodgkin Lymphoma, Version 2.2020, NCCN Clinical Practice Guidelines in Oncology. Journal of the National Comprehensive Cancer Network JNCCN 2020; 18 (06) 755-781 DOI: 10.6004/jnccn.2020.0026. (PMID: 32502987)
• 3 Cheson BD, Fisher RI, Barrington SF. et al. Recommendations for initial evaluation, staging, and response assessment of Hodgkin and non-Hodgkin lymphoma: the Lugano classification. Journal of clinical oncology official journal of the American Society of Clinical Oncology 2014; 32 (27) 3059-3068 DOI: 10.1200/JCO.2013.54.8800. (PMID: 25113753)
• 4 Rueffer U, Sieber M, Stemberg M. et al. Spleen involvement in Hodgkin's lymphoma: assessment and risk profile. Annals of hematology 2003; 82 (07) 390-396 DOI: 10.1007/s00277-003-0631-3. (PMID: 12764547)
• 5 Munker R, Stengel A, Stäbler A. et al. Diagnostic accuracy of ultrasound and computed tomography in the staging of Hodgkinʼs disease. Verification by laparotomy in 100 cases. Cancer 1995; 76 (08) 1460-1466 DOI: 10.1002/1097-0142(19951015)76:8<1460::aid-cncr2820760825>3.0.co;2-y. (PMID: 8620424)
• 6 Kadin ME, Glatstein E, Dorfman RF. Clinicopathologic studies of 117 untreated patients subjected to laparotomy for the staging of Hodgkin's disease. Cancer 1971; 27 (06) 1277-1294 DOI: 10.1002/1097-0142(197106)27:6<1277:aidcncr2820270602>3.0.co;2-t. (PMID: 5088206)
• 7 Paluska TR, Sise MJ, Sack DI. et al. Incidental CT findings in trauma patients: incidence and implications for care of the injured. J Trauma 2007; 62 (01) 157-161 DOI: 10.1097/01.ta.0000249129.63550.cc. (PMID: 17215748)
• 8 Trenker C, Görg C, Freeman S. et al. WFUMB Position Paper-Incidental Findings, How to Manage: Spleen. Ultrasound in medicine & biology 2021; 47 (08) 2017-2032 DOI: 10.1016/j.ultrasmedbio.2021.03.032. (PMID: 34052061)
• 9 Strobel D, Bernatik T, Blank W et. al. Incidence of bleeding in 8172 percutaneous ultrasound-guided intraabdominal diagnostic and therapeutic interventions – results of the prospective multicenter DEGUM interventional ultrasound study (PIUS study). Ultraschall in Med 2015; 36 (02) 122-131 DOI: 10.1055/s-0034-1399282. (PMID: 25876060)
• 10 Safai Zadeh E, Dietrich CF, Görg C. et al. Spleen biopsy: “pros and cons” or better “when and when not?”. Z Gastroenterol 2021; 59 (08) 879-885 DOI: 10.1055/a-1404-3926.
• 11 Dietrich CF, Nolsøe CP, Barr RG. et al. Guidelines and Good Clinical Practice Recommendations for Contrast-Enhanced Ultrasound (CEUS) in the Liver-Update 2020 WFUMB in Cooperation with EFSUMB, AFSUMB, AIUM, and FLAUS. Ultrasound Med Biol 2020; 46 (10) 2579-2604 DOI: 10.1016/j.ultrasmedbio.2020.04.030.
• 12 Picardi M, Soricelli A, Pane F. et al. Contrast-enhanced harmonic compound US of the spleen to increase staging accuracy in patients with Hodgkin lymphoma: a prospective study. Radiology 2009; 251 (02) 574-582 DOI: 10.1148/radiol.2512081293.
• 13 Leitlinienprogramm Onkologie (Deutsche Krebsgesellschaft, Deutsche Krebshilfe, AWMF). Diagnostik, Therapie und Nachsorge des Hodgkin Lymphoms bei erwachsenen Patienten, Langversion 3.1, 2022; AWMF-Registernummer: 018/029 OL. Accessed October 07, 2022 at: https://www.leitlinienprogramm-onkologie.de/leitlinien/hodgkin-lymphom/
• 14 Sidhu PS, Cantisani V, Dietrich CF. et al. The EFSUMB Guidelines and Recommendations for the Clinical Practice of Contrast-Enhanced Ultrasound (CEUS) in Non-Hepatic Applications: Update 2017 (Long Version). Ultraschall in Med 2018; 39 (02) e2-e44 DOI: 10.1055/a-0586-1107. (PMID: 29510439)
• 15 Omar A, Freeman S. Contrast-enhanced ultrasound of the spleen. Ultrasound (Leeds, England) 2016; 24 (01) 41-49 DOI: 10.1177/1742271X15617214.
• 16 Lim AK, Patel N, Eckersley RJ. et al. Evidence for spleen-specific uptake of a microbubble contrast agent: a quantitative study in healthy volunteers. Radiology 2004; 231 (03) 785-788 DOI: 10.1148/radiol.2313030544.. (PMID: 15118114)
• 17 Fuchs M, Borchmann P, Greil R. et al. Hodgkin Lymphom. Onkopedia-guidelines by the German (DGHO), Austrian (ÖGHO) and Swiss (SSH-SGH, SGMO) Societies for Hematology and Medical Oncology. February 2021. German.. Accessed January 23, 2023 at: https://www.onkopedia.com/de/onkopedia/guidelines/hodgkin-lymphom/@@guideline/html/index.html
• 18 Follows GA, Barrington SF, Bhuller KS. et al. Guideline for the first-line management of Classical Hodgkin Lymphoma – A British Society for Haematology guideline. British journal of haematology 2022; 197 (05) 558-572 DOI: 10.1111/bjh.18083. (PMID: 35191541)
• 19 Goerg C, Schwerk WB, Goerg K. et al. Sonographic patterns of the affected spleen in malignant lymphoma. Journal of clinical ultrasound 1990; 18 (07) 569-574 DOI: 10.1002/jcu.1870180708. (PMID: 2170456)
• 20 Görg C, Weide R, Schwerk WB. Malignant splenic lymphoma: sonographic patterns, diagnosis and follow-up. Clinical radiology 1997; 52 (07) 535-540 DOI: 10.1016/s0009-9260(97)80331-5. (PMID: 9240707)
• 21 Picardi M, Giordano C, Trastulli F. et al. Sulfur Exafluoride Contrast-Enhanced Ultrasound Showing Early Wash-Out of Marked Degree Identifies Lymphoma Invasion of Spleen with Excellent Diagnostic Accuracy: A Monocentric Study of 260 Splenic Nodules. Cancers 2022; 14 (08) DOI: 10.3390/cancers14081927.
• 22 Görg C, Faoro C, Bert T. et al. Contrast enhanced ultrasound of splenic lymphoma involvement. European journal of radiology 2011; 80 (02) 169-174 DOI: 10.1016/j.ejrad.2009.11.012. (PMID: 20005061)
• 23 Görg C, Bert T. Contrast enhanced sonography of focal splenic lesions with a second-generation contrast agent. Ultraschall in Med 2005; 26 (06) 470-477 DOI: 10.1055/s-2005-858904. (PMID: 16453218)
• 24 Tafuto S, Catalano O, Barba G. et al. Real-time contrast-enhanced specific ultrasound in staging and follow-up of splenic lymphomas. Front Biosci 2006; 11: 2224-2229 DOI: 10.2741/1965. (PMID: 16720309)
• 25 Yu X, Yu J, Liang P. et al. Real-time contrast-enhanced ultrasound in diagnosing of focal spleen lesions. Eur J Radiol 2012; 81 (03) 430-436 DOI: 10.1016/j.ejrad.2010.12.052.. (PMID: 21273021)
• 26 Stang A, Keles H, Hentschke S. et al. Differentiation of benign from malignant focal splenic lesions using sulfur hexafluoride-filled microbubble contrast-enhanced pulse-inversion sonography. AJR. American journal of roentgenology 2009; 193 (03) 709-721 DOI: 10.2214/AJR.07.3988.
• 27 Safai Zadeh E, Görg C, Post C. et al. Evaluation and Classification of Incidentally Detected Splenic Lesions Based on B-Mode and Contrast-Enhanced Ultrasound. Ultraschall in Med 2023; 1-8 DOI: 10.1055/a-2001-5516.
• 28 Moran CM, Inglis S, McBride K. et al. The Imaging Performance of Diagnostic Ultrasound Scanners Using the Edinburgh Pipe Phantom to Measure the Resolution Integral – 15 Years of Experience. Ultraschall in Med 2022; 43 (04) 393-402 DOI: 10.1055/a-1194-3818.. (PMID: 32590848)
• 29 Miwa K, Wagatsuma K, Nemoto R. et al. Detection of sub-centimeter lesions using digital TOF-PET/CT system combined with Bayesian penalized likelihood reconstruction algorithm. Ann Nucl Med 2020; 34: 762-771 DOI: 10.1007/s12149-020-01500-8.
• 30 Falk S, Müller H, Stutte HJ. Hodgkinʼs disease in the spleen. A morphological study of 140 biopsy cases. Virchows Arch A Pathol Anat Histopathol 1987; 411 (04) 359-64 DOI: 10.1007/BF00713381.