Qualitative and quantitative MRI analysis of alveolar soft part sarcoma: correlation with histological grade and Ki-67 expression

Our study highlights the clinical, MRI, and pathological manifestations of ASPS and the important role of MRI features in distinguishing between high- and low-grade ASPS. The differentiation is critical, given the insidious nature of ASPS, which often presents as asymptomatic, with early metastasis and resistance to conventional chemotherapy. The correlation we observed between qualitative MRI features (distant metastasis, intratumoral necrosis, and tumor enhancement), semi-quantitative features (TIC type), and quantitative features (ADC values) with histological grades and Ki-67 expression levels offers a new avenue for non-invasive preoperative assessment. This is particularly important in the context of ASPS, where conventional biopsy techniques present risks and limitations due to tumor heterogeneity and potential for cell dissemination.

ASPS is a rare, malignant, highly vascularized tumor with distinctive morphological features that differ from other STSs, it exhibits some typical clinical, pathological, and MRI characteristics. It predominantly affects young to middle-aged females, characterized by characteristic nest-like structures separated by fibrous connective tissue rich in blood sinuses, and cells arranged in a “glandular” or “organ-like” pattern [3]. In our study, the nest-like or glandular structures and sinus-like blood vessels within tumors were observed. Due to its rich vascularity and slow blood flow, these tumors often display multiple tortuous blood vessels within and around the mass, resulting in slightly increased signal intensity on T1WI and high signal intensity on DWI, which is in line with our study results [12].

ASPS typically shows moderate or marked enhancement on contrast-enhanced scans due to its rich vascularity. Qiao et al [13] analyzed 14 cases of ASPS and found that they all exhibited significant enhancement on contrast-enhanced scans. In our study, we found that 19 patients showed marked enhancement compared to the tumor T1WI signal, especially in high-grade ASPS patients, which is consistent with literature reports. The TIC as a semi-quantitative parameter of DCE-MRI can comprehensively reflect vascular permeability, perfusion, and microcirculation status. Malignant lesions typically exhibit abundant blood flow perfusion, appearing as rapid peak enhancement on the TIC curve, whereas benign lesions often display flat TIC curves [12, 14, 15]. Several studies on musculoskeletal tumors have shown that contrast-enhanced scans are helpful in differentiating between benign and malignant lesions, with Type III TIC curves often indicating malignant tumors, but both benign and malignant lesions can present as Type I or Type II curves [14,15,16]. In our study, we found that TIC types in ASPS helped distinguish between high and low grades, with Type III curves being predominant, reflecting that higher-grade tumors have a richer capillary network, consistent with the feature of ASPS being highly vascularized. Our findings regarding the relationship between MRI characteristics and tumor grade further underscore the potential of MRI in providing insights beyond basic diagnostic imaging. For instance, the significant enhancement patterns observed in contrast-enhanced scans reflect ASPS’s rich vascularity, aligning with previous studies and suggesting that MRI can capture the unique vascular profile of these tumors.

Moreover, the ability of MRI to identify distant metastases, a predictor of high-grade ASPS, underscores its potential in early detection and staging, which is crucial for effective treatment planning. ASPS patients are often asymptomatic, and distant metastasis may have already occurred at the time of diagnosis [1,2,3]. In our study, 31 cases had distant metastases at the initial diagnosis, involving the lungs, brain, bones, and lymph nodes. We found that the high-grade group had a significantly higher metastasis rate than the low-grade group, and distant metastasis was an independent predictor of high-grade ASPS. The rich blood supply in ASPS, along with the presence of large, tortuous blood vessels within and around the tumor, may be important factors contributing to early distant metastasis [13,14,15,16]. In previous studies, tumor necrosis was considered a reliable predictor of high-grade STS, and for STS patients with necrosis volume less than 50%, necrosis volume exceeding 50% indicated a worse prognosis [17, 18]. In our study, we found that high-grade ASPS exhibited more necrosis, consistent with literature reports.

DWI reflects the rate of diffusion of water molecules, and the typical feature of malignant tumors is high cell density and reduced extracellular space, resulting in restricted water molecule diffusion and consequently lower ADC values. Chhabra et al [19] found that tumor size, central enhancement, and ADC values could be used to differentiate the histological grade of musculoskeletal soft tissue malignant tumors. In our study, we found that the ADC values in high-grade ASPS tumors were lower than those in low-grade tumors. The positive correlation between cell density and tumor grade can explain the ability of DWI to assess ASPS histological grade. In breast cancer, hepatocellular carcinoma, cervical cancer, and other solid tumors, ADC values have been reported to be negatively correlated with Ki-67 expression [20,21,22]. Lee et al [23] first found a weak negative correlation between ADC values and Ki-67 expression in STS, and in subsequent reports, Yuan et al [24] found a moderate negative correlation between ADC and D values and Ki-67 expression in a rhabdomyosarcoma mouse model. Fang et al [25] found that histogram features such as ADCmean and ADCmin were negatively correlated with Ki-67 expression in fibrosarcoma. In our study of ASPS, the observation of a negative correlation between ADC values and Ki-67 expression levels further supports the use of MRI in the non-invasive assessment of tumor aggressiveness and proliferation activity. This correlation not only validates the utility of MRI in differentiating tumor grades but also opens avenues for its use in monitoring treatment response and potentially guiding therapy adjustments.

While our study establishes a strong correlation between MRI characteristics and ASPS histological grades, it also raises important considerations regarding the specificity and stability of qualitative diagnosis in different STS subtypes. The varying manifestations of conventional MRI features like peritumoral enhancement and edema, which did not predict high-grade ASPS in our study, suggest the need for a more nuanced understanding of MRI readings in different soft tissue sarcoma contexts. Furthermore, our findings on the molecular characteristics of ASPS, particularly the expression of TFE3, add a layer of complexity to the disease’s diagnostic landscape. Although our study showed universal positive expression of TFE3 across all samples, the lack of significant statistical difference in histological grade raises questions about the marker’s predictive power, possibly limited by our study’s small sample size.

Histopathological confirmation provides precise evidence of the disease and detailed biological insights, while MRI offers crucial visual information regarding tumor anatomical location, size, relationship with surrounding tissues, and treatment response. Given that tumor heterogeneity can impact histological diagnosis from percutaneous biopsies, MRI serves as an additional non-invasive diagnostic tool, thereby complementing the limitations of biopsies. Our study indicates that MRI features such as distant metastases, heterogeneous tumor enhancement, and low ADC values (< 1.052 × 10−3 mm2/s) contribute to the diagnosis of high-grade ASPS. Additionally, when observing an ADC less than 0.997 × 10−3 mm2/s, high expression of Ki-67 suggests a poorer prognosis for patients. These insights aid physicians in determining the nature of the tumor, and evaluating tumor enhancement characteristics, growth rate, and prognosis, thus providing crucial evidence for the selection of treatment modalities and prognosis assessment for ASPS patients [23, 26, 27]. Our study indicated that high-grade ASPS typically exhibits lower ADC values, and ADC values are inversely correlated with Ki-67 expression levels. Therefore, ADC values can serve as an important indicator for predicting the malignancy and prognosis of ASPS. Based on ADC values, physicians can more accurately assess the severity of ASPS and devise personalized treatment plans. In summary, MRI examination results have a significant impact on the clinical decisions and management strategies for ASPS patients.

Several limitations should be considered. Firstly, this study involved a relatively small number of ASPS patients, which may impact the generalizability and reliability of the results. Expanding the sample size could contribute to a more comprehensive understanding of ASPS characteristics. Secondly, due to the heterogeneity of tumors, measuring ADC only in the largest lesion slice may lead to misdiagnosis. Thirdly, the results of this study were applicable only to cases with known histological diagnoses, lacking applicability. For situations where histological diagnosis has not been conducted or diagnostic uncertainty exists, these results may not be effectively applicable. Lastly, this study primarily focused on initial diagnosis-related features and predictive factors, but lacked long-term follow-up data for patients, making it impossible to assess treatment outcomes and survival rates.

In conclusion, our study underscores the MRI manifestations of ASPS and the vital role of MRI in the preoperative assessment of ASPS, providing clinicians with valuable information on tumor diagnosis, grading, and proliferation activity. By leveraging both conventional MRI and DWI, we can enhance our understanding of this rare tumor’s characteristics, aiding in the development of tailored treatment strategies.

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