Abstract
Objectives
Early, accurate diagnosis is crucial for the prognosis of patients with soft tissue sarcomas. To this end, standardization of imaging algorithms, technical requirements, and reporting is therefore a prerequisite. Since the first European Society of Musculoskeletal Radiology (ESSR) consensus in 2015, technical achievements, further insights into specific entities, and the revised WHO-classification (2020) and AJCC staging system (2017) made an update necessary. The guidelines are intended to support radiologists in their decision-making and contribute to interdisciplinary tumor board discussions.
Materials and methods
A validated Delphi method based on peer-reviewed literature was used to derive consensus among a panel of 46 specialized musculoskeletal radiologists from 12 European countries. Statements were scored online by level of agreement (0 to 10) during two iterative rounds. Either “group consensus,” “group agreement,” or “lack of agreement” was achieved.
Results
Eight sections were defined that finally contained 145 statements with comments. Overall, group consensus was reached in 95.9%, and group agreement in 4.1%. This communication contains the first part consisting of the imaging algorithm for suspected soft tissue tumors, methods for local imaging, and the role of tumor centers.
Conclusion
Ultrasound represents the initial triage imaging modality for accessible and small tumors. MRI is the modality of choice for the characterization and local staging of most soft tissue tumors. CT is indicated in special situations. In suspicious or likely malignant tumors, a specialist tumor center should be contacted for referral or teleradiologic second opinion. This should be done before performing a biopsy, without exception.
Clinical relevance
The updated ESSR soft tissue tumor imaging guidelines aim to provide best practice expert consensus for standardized imaging, to support radiologists in their decision-making, and to improve examination comparability both in individual patients and in future studies on individualized strategies.
Key Points
• Ultrasound remains the best initial triage imaging modality for accessible and small suspected soft tissue tumors.
• MRI is the modality of choice for the characterization and local staging of soft tissue tumors in most cases; CT is indicated in special situations. Suspicious or likely malignant tumors should undergo biopsy.
• In patients with large, indeterminate or suspicious tumors, a tumor reference center should be contacted for referral or teleradiologic second opinion; this must be done before a biopsy.
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Introduction
Soft tissue sarcomas are rare, and comprise a heterogeneous group of entities [1], leading to diagnostic challenges. An early, accurate diagnosis is crucial for the prognosis of these patients. At the same time, clinical infrastructure differs considerably throughout Europe. The same is true for the attitudes towards the use of advanced imaging techniques. This results in notable variability in clinical practice.
Since the first consensus on soft tissue tumor imaging in adults of the European Society of Musculoskeletal Radiology (ESSR) in 2015, technical achievements, further insights into specific entities, the revised WHO-classification (2020) [1], and a new version of the American Joint Committee on Cancer (AJCC) staging system (2017) [2] made an update of the ESSR consensus guidelines necessary [3]. A Delphi process [4], evidence based on current literature where possible, enables to derive consensus on complex problems among a panel of experts [5], and has been used by the ESSR elsewhere recently [6].
The updated ESSR agreement for imaging of soft tissue tumor aims to provide best practice expert consensus guidelines for standardized imaging algorithms, techniques, and reporting in soft tissue tumors of adults. These recommendations are intended to support radiologists in their decision-making when first being confronted with a suspected soft tissue tumor and help them in their contribution to interdisciplinary tumor board meetings. Standardization can also be useful for follow-up in the individual patient, as comparison of serial examinations even when performed in different institutions can be compared reliably. Finally, standardized examinations may provide better databases for multicenter studies. Standardization may also facilitate evaluations of large datasets for optimization of individualized care.
Materials and methods
A validated Delphi method [5,6,7,8,9] on the base of peer-reviewed literature was used to derive consensus among a panel of 46 specialized musculoskeletal radiologists from 12 European countries, all being members of the tumor subcommittee of the ESSR. Institutional review board approval was not required for the present consensus as patients were not involved. Major sections were defined. For each section, working groups provided statements with comments, based on the current literature, following a search on PubMed and the Cochrane Library. The statements were validated by two orthopedic tumor surgeons and one pathologist specialized in musculoskeletal tumors. All statements were imported into an online questionnaire, using the online platform Google Forms® [10]. The panel members were then asked to score their level of agreement with each statement, on a scale from 0 to 10, with 10 being the highest grade of agreement. Minimum statement scoring by the panel was considered if a median of at least 8 and an interquartile range of less than 4 were achieved. For the statements which fulfilled these criteria, the level of agreement was calculated, and assigned as either “group consensus,” “group agreement,” or “lack of agreement.” “Group consensus” was defined as at least 80% of respondents scoring at least 8, “Group agreement” was defined as 67–79% of respondents scoring at least 8. “Lack of agreement” was assigned if the previous conditions were not met. Respondents also had the opportunity to make suggestions for altering the statements for future rounds of voting, especially if they disagreed with the statements.
A face-to-face meeting of the panelists was organized on the occasion of the ESSR congress in 2022, where open questions on the Delphi process were addressed, the preliminary results of round 1 were presented, and specific comments were discussed. After the meeting, round 1 was re-opened for further ratings. After termination of round 1, the statements without group consensus, and all statements with suggestions for any change were modified appropriately by the organizing panelist (I.-M. N.-H.). Additional statements were added as suggested. All these revised statements were circulated and further amended. All statements which had been changed since round 1 were then provided online for scoring in a second iterative questionnaire round. The results of round two were re-calculated and labeled as described for round 1. After round 2, the rating was terminated for each statement.
Results
Eight sections were defined that finally contained 145 statements overall. After round 2, all statements had reached either group consensus or group agreement. Group consensus was reached in 139/145 statements (95.9%), and group agreement was achieved in 6/145 statements (4.1%). None of the statements resulted in lack of agreement.
The first two of the eight sections included (1) primary diagnosis of soft tissue tumors, with background information and local imaging (62 statements, with 61 of them with group consensus, 1 with group agreement, and none with lack of agreement); (2) the role of referring hospitals and tumor reference centers (12 statements, 12/0/0, respectively). The statements of these two sections are described in detail in this part of the consensus (part I).
The remaining six sections will be published subsequently and will deal with whole-body staging in sarcoma at the time of primary diagnosis, non-malignant entities that require special management, pitfalls, and special aspects in soft tissue tumor imaging, imaging during and immediately after neoadjuvant therapy in soft tissue sarcoma, and post-therapeutic follow-up in sarcoma.
The first section of part I, primary diagnosis of soft tissue tumors, covers local imaging algorithms; Fig. 1 gives an overview. Statements and their level of agreement are provided in Table 1. They deal with background information requirements such as the past medical history (PMH) and the clinical situation. Updated detailed recommendations for an optimized soft tissue tumor imaging algorithm and technical requirements are also provided. Standards for reporting, now with a detailed checklist for clinical routine use, have been developed and can be found as supplementary material (figure S1). Recommendations relating to the role of guidelines and tumor reference centers, corresponding to the second section, are provided in Table 2, and are also addressed by Fig. 1. For all statements, comments with references are provided in the electronic supplementary material.
Discussion
The updated ESSR consensus guidelines aim to provide feasible best practice expert opinion pertaining to soft tissue tumor imaging. In comparison with the previous ESSR recommendations [11], the revised guidelines are updated to the current literature and re-structured. They provide minimal requirements and an optimized strategy in a systematic approach and contain relevant details.
The Delphi process was chosen as the panelists could perform their scoring anonymously and without the necessity to meet personally for rating [5]. However, additional face-to-face-meetings proved useful to clarify open questions regarding the procedure and to discuss concerns and re-phrasing of statements without consensus.
The extended expert panel included specialists from twelve European countries. The ESSR represents the European musculoskeletal radiologists [12]. Recruiting the panelists from the dedicated Musculoskeletal (MSK) tumor subcommittee of the ESSR allowed to form an adequate expert panel of active, representative, and leading specialists [13]. As group consensus (which reflects a considerably high level of agreement) could be reached in the majority of statements, and group agreement even in the remaining ones, this paper may help to provide feasible imaging algorithms taking into account different national infrastructure and approaches.
In this first part, the statements reflect the situation that any radiologist is confronted with in a patient with a newly suspected soft tissue tumor. Part I of our consensus therefore contains the imaging algorithm that we would recommend for primary diagnosis. It also contains detailed description of imaging methods for the tumor itself and the role of tumor reference centers and guidelines.
In the following paragraphs, we present a selection of the most clinically relevant statements with short discussion (the numbers correspond with Tables 1 and 2; the remaining comments are provided online).
Primary diagnosis, local imaging
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1.1.1. Regarding the past medical history, a standardized checklist, primarily filled out by the patient, and discussed with the radiologist, is considered advisable. The patient or the referring clinician should also be asked to provide previous imaging if available.
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1.1.2. Information about clinical symptoms and clinical examination findings should be available for the radiologist.
The past medical history of the patient is considered important and has to be taken into account not only by the clinician, but also by the radiologist. A standardized checklist, primarily filled out by the patient, and discussed with the radiologist, is considered advisable [14]. The information that should be available for example includes recent trauma [15, 16], anticoagulation [17], and a history of previous surgery or of radiation therapy [18,19,20]. Of note, patients often report a recent trauma that they relate to the tumor, which, however, may be unrelated, and misleading [15, 16]. It is very important that the diagnostic process is not prolonged during the process of obtaining this information.
The patient or the referring clinician should also be asked if, where and when, previous imaging had been performed. The previous imaging studies and their radiological report should be provided to the assessing radiologist (if available) [11].
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1.2.1. Ultrasound (US) is considered the appropriate initial triage imaging modality for a suspected soft tissue tumor, if accessible by US and small (< 5 cm). When US diagnosis is not typical for a diagnosis, refer to Magnetic Resonance Imaging (MRI) or even biopsy.
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Caveat: MRI should be performed prior to biopsy (if it will add to lesion characterization), not afterwards.
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1.2.2. MRI is the imaging technique of choice for characterization and local staging of large (> 5 cm) musculoskeletal soft tissue masses and masses with indeterminate ultrasound features.
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Primary MRI should be considered instead of US if, there is a clinical suspicion of malignancy, if the mass is deep, rapidly enlarging, and if there is osseous or joint involvement.
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1.2.3. Computed tomography (CT) can be considered instead of MRI for complex thoracic/ abdominal / other deep masses. CT should be performed in case of complex thoracic/ abdominal / other deep masses if MRI is unavailable or is contraindicated.
Ultrasound represents the initial triage imaging modality for accessible and small suspected soft tissue tumors [21,22,23,24]. Ultrasound is highly accurate for diagnosis of specific superficial lesions with typical ultrasound features [23, 25].
MRI is the modality of choice for the characterization and local staging of soft tissue tumors in most cases [26,27,28]. CT and MRI may have complementary roles, with the capability of CT to demonstrate intralesional mineralization patterns and potential bone involvement [29]. A deep soft tissue mass incidentally found at CT usually requires MRI examination. Tissue-specific evaluation and multiplanar capability of high-resolution MRI permit better tumor localization and characterization of pelvic/retroperitoneal masses [27, 30].
Suspicious or likely malignant tumors should undergo biopsy [11].
Role of tumor centers and guidelines
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2.1. Criteria for referral to a sarcoma treatment center include: Any patient with a tumor ≥ 5-cm, or with indeterminate or suspicious US/MRI findings, or with clinical suspicion of malignancy; Any patient with indeterminate MRI findings or those suspicious for malignancy.
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Teleradiologic second opinion from a tumor center is appropriate in patients with indeterminate or suspicious MRI findings. It should be offered to the local hospitals in all patients in whom soft tissue sarcoma is suspected.
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2.2. Patients with suspicion of sarcoma should be referred to the tumor reference center before biopsy or surgery (minimal requirement).
In patients with large, indeterminate, or suspicious tumors, a tumor reference center should be contacted for referral or teleradiologic second opinion, to avoid delay in diagnosis or unplanned surgery (“whoops procedure”) [31,32,33,34], both of which can result in a potentially worse prognosis [35,36,37,38]. A second opinion MRI report from an expert center increases the overall accuracy in the diagnosis of soft tissue tumors, with fewer false-negative and false-positive diagnoses [39,40,41].
Biopsy of suspected appendicular soft tissue sarcoma should be performed by a tumor radiologist-specialist, using image guidance, to minimize adverse outcomes, and with minimal delay [42].
In case of unplanned surgery of sarcoma, the patients should immediately be referred to a sarcoma center for further evaluation and treatment, in order to avoid a potentially worse prognosis [35].
Local radiologists should implement guidelines for early imaging by ultrasound and MRI with a designated pathway. Adherence to those guidelines should on the one hand help prioritize onward referral for suspicious lesions [22], and on the other hand help reduce the volume of benign lesions referred [22, 43].
The imaging strategies that become necessary when the histologic diagnosis is already known will be covered in consecutive parts of our guidelines. This includes recommendations for whole-body staging in the primary diagnosis, for therapy control, and for follow-up imaging, as well as special aspects and pitfalls.
If these guidelines lead to more standardized examinations, the resulting data may be better suited for multicenter studies, with an improved possibility to collect and analyze comparable large data volumes. Thus, these guidelines may help to develop more individualized imaging protocols for the diagnosis of soft tissue tumors in the future.
Limitations
Our consensus has got several limitations: The panelists came from European countries only. However, access to MRI is limited in many other parts of the world. In those areas, US and—if accessible—CT have to replace MRI. MRI contrast agents may be too expensive. Our guidelines take those points into account only to a certain extent. Tumor reference centers may be too distant, and teleradiologic consultation may not be available. In less-developed countries, only some parts of this consensus will be applicable at the moment. It is envisaged that these guidelines will however provide added impetus to health care professionals in these countries to canvass and optimize resources for better patient outcomes. The Delphi method itself has also got some limitations. Firstly, it is dependent on the expertise of the panelists. This was mostly overcome by including only ESSR-approved tumor specialists. Secondly, the possibility for open discussion is limited. On the other hand, this allows for distribution of critical remarks anonymously. Thus, the Delphi method had the advantage not to be biased by dominant participants. Thirdly, the process was time-consuming. This is a disadvantage that has been described for guidelines that contain multiple statements, such as our consensus [5]. As the Delphi process requires commitment to take part in several questionnaire rounds, we aimed to provide sufficient time for the participants to answer. Finally, it should be emphasized that these guidelines reflect the current knowledge and will require further updates in the future.
Conclusion
The updated ESSR guidelines for imaging of soft tissue tumors in adults aim to provide best practice expert consensus for standardized imaging and are intended to support radiologists in their decision-making. Standardization may improve the comparability of serial examinations in the individual patient and may also provide databases for multicenter studies and large data analysis for individualized strategies.
Abbreviations
- AJCC :
-
American Joint Committee on Cancer
- CT:
-
Computed tomography
- ESSR:
-
European Society of Musculoskeletal Radiology
- MRI:
-
Magnetic resonance imaging
- MSK:
-
Musculoskeletal
- PMH:
-
Past medical history
- US:
-
Ultrasound
- WHO:
-
World Health Organization
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We would like to thank the administration of the European Society of Musculoskeletal Radiology for their support.
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Noebauer-Huhmann, IM., Vanhoenacker, F.M., Vilanova, J.C. et al. Soft tissue tumor imaging in adults: European Society of Musculoskeletal Radiology-Guidelines 2023—overview, and primary local imaging: how and where?. Eur Radiol (2023). https://doi.org/10.1007/s00330-023-10425-5
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DOI: https://doi.org/10.1007/s00330-023-10425-5