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

Hajo Findeisen; Christian Görg; Helen Winter; Corinna Trenker; Christoph F. Dietrich; Amjad Alhyari; Friederike Eilsberger; Ehsan Safai Zadeh

doi:10.1055/a-2173-2361

Ultraschall in der Medizin - European Journal of Ultrasound, Table of Contents

Ultraschall Med 2024; 45(05): 484-492
DOI: 10.1055/a-2173-2361

Original Article

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

B-mode Ultraschall und Kontrastmittelverstärkter Ultraschall zur Beurteilung des Milzbefalls beim Hodgkin-Lymphom: retrospektive Analyse von n = 112 Patienten

Hajo Findeisen

¹Department for Internal Medicine, Red Cross Hospital Bremen, Bremen, Germany (Ringgold ID: RIN39539)

²Interdisciplinary Center of Ultrasound Diagnostics, University Hospital of Giessen and Marburg Campus Marburg, Marburg, Germany (Ringgold ID: RIN61061)

,

Christian Görg

³Interdisciplinary Center of Ultrasound Diagnostics; Gastroenterology, Endocrinology, Metabolism and Clinical Infectiology, University Hospital of Giessen and Marburg Campus Marburg, Marburg, Germany (Ringgold ID: RIN61061)

,

Helen Winter

²Interdisciplinary Center of Ultrasound Diagnostics, University Hospital of Giessen and Marburg Campus Marburg, Marburg, Germany (Ringgold ID: RIN61061)

,

Corinna Trenker

⁴Interdisciplinary Center of Ultrasound Diagnostics; Department of Hematology, Oncology and Immunology, University Hospital of Giessen and Marburg Campus Marburg, Marburg, Germany (Ringgold ID: RIN61061)

,

Christoph F. Dietrich

⁵Department General Internal Medicine, Kliniken Hirslanden Beau Site, Salem und Permanence, Bern, Switzerland

,

Amjad Alhyari

³Interdisciplinary Center of Ultrasound Diagnostics; Gastroenterology, Endocrinology, Metabolism and Clinical Infectiology, University Hospital of Giessen and Marburg Campus Marburg, Marburg, Germany (Ringgold ID: RIN61061)

,

Friederike Eilsberger

⁶Department of Nuclear Medicine, University Hospital of Giessen and Marburg Campus Marburg, Marburg, Germany (Ringgold ID: RIN61061)

,

Ehsan Safai Zadeh

²Interdisciplinary Center of Ultrasound Diagnostics, University Hospital of Giessen and Marburg Campus Marburg, Marburg, Germany (Ringgold ID: RIN61061)

⁷Department of Biomedical Imaging and Image-guided Therapy, Medical University of Vienna, Wien, Austria (Ringgold ID: RIN27271)

› Author Affiliations

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

Full Text

References

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
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
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
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
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
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
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
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
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
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
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
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
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
15 Omar A, Freeman S. Contrast-enhanced ultrasound of the spleen. Ultrasound (Leeds, England) 2016; 24 (01) 41-49
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
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
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
20 Görg C, Weide R, Schwerk WB. Malignant splenic lymphoma: sonographic patterns, diagnosis and follow-up. Clinical radiology 1997; 52 (07) 535-540
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)
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
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
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
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
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
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
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
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
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