Dural metastases in breast cancer: progression pattern, treatment and prognosis—a single center experience

Introduction

Intracranial meningeal metastases including leptomeningeal metastasis (LM) and dural metastasis (DM) are typically considered to be a late manifestation of malignant tumors with poor prognosis. Commonly included in the analysis of central nervous system metastases, DM shares a similar prognosis with intracerebral metastases. Usually, it occurs after or concomitant diagnosis of distant metastasis to other organs. Compared with leptomeningeal metastases, meningeal metastases involving the dura mater are less prevalent. Early autopsy reports found that dural metastases accounted for approximately 8–9% of patients with advanced disseminated cancer (1-3). More recent studies have reported a higher incidence of DM ranging between 11% and 50% of all cases (3-6). One important reason for the significant variation in diagnostic rates is that the majority of dural metastases are initially asymptomatic, some are incidentally detected on imaging during routine follow-up. In recent years, the diagnostic rate of DM has gradually increased. A combination of factors such as advances in diagnostic work-up, increased awareness of clinicians, improved systemic control and prolonged survival in patients as a result of therapeutic improvements may have contributed the increasing incidence and prevalence of intracranial meningeal metastases diagnoses. Otherwise, with modern neuroimaging evolvement, an increasing possibility of DM could be identified which facilitate the recognition of the relatively rare central nervous system complication of systemic cancer.

A higher proportion of subjects with breast cancer was found to develop meningeal metastasis compared to subjects with other cancers from previous studies (4,7,8). Given breast cancer remains high prevalence worldwide, even with a rare incidence rate, intracranial meningeal metastases can cause substantial morbidity and mortality. Although the majority of patients with dural metastases lack neurological symptoms, among symptomatic patients, the gradual onset of headaches and other signs of increased intracranial pressure are the most common presenting symptoms (5,9). Other rare symptoms include manifestations related to compression of the cranial nerves at the base of the skull, such as facial numbness and asymmetry.

At present no efficient and recommended treatment for DM has been proved, and the reported results are far from encouraging. Given DM are located outside the blood-brain barrier (BBB), systemic therapy should be considered with asymptomatic patients first (10,11). For symptomatic patients or those unsuitable for systemic therapy, radiotherapy including whole brain radiotherapy (WBRT) and stereotactic radiosurgery (SRS) are considering therapeutic options, helping to delay neurological deterioration and to improve the symptom burden (4,9,12-16). All applied methods are aimed to improve the neurological status, alleviating pain and preventing the further development of symptoms from the central nervous system. Remaining one of the most challenging clinical scenario in breast cancer treatment, an optimal treatment regimen for the patients with DM should be considered. We presented this manuscript in accordance with the STROBE reporting checklist (available at https://cco.amegroups.com/article/view/10.21037/cco-24-30/rc).

Methods

Study population

In this study, we retrospectively reviewed radiological information of breast cancer patients diagnosed with dural metastases with/without brain parenchymal metastases at Ruijin Hospital between 2014 and 2021. The terms used for the search included breast cancer, meningeal, dural, thickening, and enhancement. Including baseline evaluation, all the reviewed patients underwent at least one contrast-enhanced head magnetic resonance imaging (MRI). All scans used the following parameters: 1.5T MRI scanner, dosage of Gd-based contrast agent determined based on the patient’s body weight as 0.2 mg/kg, scanning range from the vertex of the skull to the foramen magnum, with the slice thickness of 1 mm. Presenting as a dural-based lesion that enhances intensely during the MRI enhanced T1 phase, whether as a single mass, multiple masses, nodular pattern, or diffuse thickening, can be diagnosed as dural metastases. We also excluded cases of meningeal invasion subsequent to brain parenchyma. The MR image of each patient was independently verified by the same consultant radiologist.

Data collection

Electronic medical records of study population were scrutinised and recorded for patient demographics. Clinical data including general information such as age, menstrual status; initial dates of diagnosis of breast cancer, distant metastases and dural metastases; dates of last follow-up or death; metastatic organs; tumor characteristics [hormone and human epidermal growth factor receptor 2 (HER2) receptor status, tumor-node-metastasis (TNM) stages]; sites of DM; symptoms at diagnosis of DM; presence of skull bone or spinal metastasis or not; brain parenchymal metastases prior to/at time of DM diagnosis; initial and subsequent treatment (radiotherapy) of the DM; clinical outcomes of DM treatment were retrieved for further analyses.

Statistical analysis

We analyzed median survival time according to whether radiation therapy was received or not and median time from the bone diagnosis to DM. Overall survival (OS) was defined as dates from diagnosis of DM to death from any causes. The proportion of prior or synchronous parenchymal brain metastasis at time of diagnosis of DM and the proportion of skull bone or spinal bony disease prior to diagnosis of DM, distribution of DM involved sites were also calculated in this study.

Percentages and means were employed for the analyses of demographic data, clinicopathological features, DM involved sites, symptoms and management approaches. OS estimates were calculated using Kaplan-Meier method. Logistic regression was employed to identify significant variables relative to treatment decision. P values of less than 0.05 were considered significant. Multivariate analysis was performed using the Cox regression model to assess the effect of patient characteristics and other prognostic factors influencing the OS.

Ethical statement

The study was conducted in accordance with the Declaration of Helsinki (as revised in 2013) and received approval by the Ethics Committee of Ruijin Hospital, affiliated with the School of Medicine at Shanghai Jiao Tong University (No. 298). This study extracts information from the medical records of past patients, where the research risk is minimal and obtaining informed consent from the subjects is not feasible. Approval for the waiver of informed consent has been granted by the Ethics Committee.

Results

Clinical characteristics

From 2014 to 2021, a total of 66 breast cancer patients were review and recruited into final analysis. Patients’ general characteristics are summarized in Table 1. The mean age at breast cancer diagnosis was 52 years old, ranging from 22 to 81 years old. Nearly half of the study cohorts (43.9%) were distributed to hormone receptors (HR) positive subtype followed by triple-negative breast cancer (TNBC) and HER2+ subtypes successively with the proportion of 25.8% and 21.2% respectively. There were six patients whose subtype could not be determined due to the ambiguous status of HER2 gene. The distant metastatic disease (stage IV) at initial diagnosis had a higher proportion than epidemiological statistical data reported accounting for 24.2% of the study population (17).

Dural metastases

Nearly half of the patients (48.5%, 32 cases) suffered from previous or synchronous parenchymal brain metastases at diagnosis of DM indicating a late stage of the disease. Over half of the patients presented with multiple symptoms (44 patients, 66.7%), among which the most frequent solitary presenting symptoms was headache (15 patients, 34.1%). Frontoparietal dura had a significant predominance among all areas of involvement accounting for 43.9% (29/66) of the patients, temporal dura and parietal dura ranked as the second and third (21/66 and 16/66, respectively). Cranial neural sheath invasion was not rare in our study. According to the radiological images, 7 patients were determined to have of manifestations cranial neural sheath invasion whose symptoms were related to compression of the cranial nerves at the base of the skull, such as facial numbness and asymmetry. The majority of the study population had diffusive lesions in the dura, while focal-type was observed in a smaller amount of patients. The exact distribution of dural invasion was demonstrated in Figure 1. The metastases were classified into three morphological types in terms of the MRI images: nodular, thickened with nodules, and diffuse thickened. The proportions of the three types are as follows: nodular type accounts for 33.3% (22/66), thickened with nodules type accounts for 27.3% (18/66), and diffuse thickening type accounts for 39.4% (26/66). Among patients with the nodular type, the proportion of HR-negative is 13/22 (59.1%), which is significantly higher than the other two types with a P value less than 0.05, while the thickened with nodules type was 3/18 (16.7%), and the diffuse thickening type was 9/26 (34.6%). In the thickened with nodules type, the proportion of HER2-positive is 0 out of 14, with no significant differences observed in the distribution of the remaining proportions.

Figure 1 Distribution of DM sites. The frontoparietal dura was the most frequently involved site, followed by temporal dura and parietal dura, ranking second and third. DM, dural metastases.

Fifty-four patients (81.8%) had extensive bone metastasis displayed as extensive metastasis of axial skeleton (≥5 lesions) prior to/at the diagnosis of DM, and among these individuals, 44 cases (66.7%) had synchronous cranial bone metastases. Out of 37 cases, the occurrence of intracranial dura mater metastases located at the exact site of skull metastases accounted for more than half of the study population. Liver remained the most common visceral metastases organs (34 patients, 51.5%), while lungs were marginally second in prevalence (32 cases, 48.5%). At diagnosis of DM, most of the patients (57.6%, 38 cases) had accepted at least third line system treatment, indicating a late stage of disease.

Radiation

Patients with symptoms or extensive DM lesions or concomitant multiple skull metastases or with multiple synchronous parenchymal brain metastases not indicated for PRT received WBRT. Patients with manifestations of leptomeningeal invasion were recommended to receive CSI. Other factors, such as the patient’s systemic treatment status, the patient’s preferences, and the doctors’ choices, may also influence the selection of radiotherapy regimens. Forty-two patients received radiotherapy to DM, including 25 with WBRT, four with CSI, and 13 with DM and/or brain parenchyma lesions (including stereotactic radiotherapy, SRT). WBRT was delivered by IMRT method with 6 MV photon beams once daily 5 days per week. Dose was given in 2 or 3 Gy/fraction, with a total of 40 or 30 Gy. SRT with 6 MV FFF photon beams was given at the single dose of 7or 8 Gy in five fractions for DM and/or brain parenchyma lesions for patients with limited focus. The radiotherapy was delivered with the linac device of Edge or TrueBeam. Among all patients who underwent radiation therapy, 20 patients received immediate radiotherapy upon the diagnosis of DM; 14 of them had concurrent brain parenchymal metastases, and 15 exhibited neurological symptoms. Twenty-one patients initially underwent systemic treatment at first diagnosis of DM, followed by radiotherapy after progression. One patient, who had previously received radiotherapy for brain metastatic lesions, has developed dural metastases with distant metastases progression meanwhile. Of 24 patients who did not receive radiotherapy, 19 had isolated dural metastases, and five had concurrent brain parenchymal metastases.

Whether to accept WBRT were associated with concurrent brain parenchymal metastases status, metastatic volume of DM and leptomeningeal invasion, with P value of 0.01, 0.008 and 0.003, respectively. Radiotherapeutic strategy is highly affected by associated metastatic volume of DM and concurrent brain parenchymal metastases status (P=0.002, 0.03), while neurological symptoms, HR and HER2 status, number of systemic treatment lines were not relevant with radiotherapeutic decisions. More chances were those with leptomeningeal invasion distributed to WBRT group (17/29 vs. 7/37, P=0.001), and more chances were to have concurrent parenchymal brain lesions (19/27 vs. 13/37, P=0.01).

Survival

There were 50 survival status retrieved through follow-up system while 43 deaths were observed for any causes. Multivariate analysis indicates that initial diagnosis age, brain metastasis status, neurological symptoms and systemic treatment status and are significant prognostic factors (P=0.002, 0.03, 0.02, 0.001 and 0.02, respectively). Patients with younger initial diagnosis age, concurrent brain parenchymal metastases, neurological symptoms and systemic treatment of three or more lines have a poorer prognosis. Biological subtype was not a factor that statistically significantly influenced survival in Cox analysis (P=0.97). Among those with bone metastases, the median duration from bone metastasis to the diagnosis of DM was 419 days. The median survival time from the diagnosis of DM was 458 days in patients who received radiotherapy compared with 225 days in patients who did not receive radiotherapy, with an hazard ratio (HR) 0.65 [95% confidence interval (CI): 0.302–1.305] and P value of 0.06 (Figure 2). The median survival time of nodular type and diffuse thickened type was 447 and 381 days respectively, while the thickened with nodules type was 225 days with a P value of 0.39 (Figure 3).

Figure 2 Kaplan-Meier survival curve of DM patients accepted irradiation or not. The median survival time from the diagnosis of DM was 458 days in patients who received radiotherapy compared with 225 days in patients who did not receive radiotherapy, with an HR 0.65 (95% CI: 0.302–1.305) and P value of 0.06. DM, dural metastasis; HR, hazard ratio; CI, confidence interval.

Figure 3 Survival curve of DM morphological pattern. There is no difference in the median survival time among the three different morphological types of dural metastasis (P=0.39). DM, dural metastasis.

Discussion

In recent years, with advancements of breast cancer treatment, the prognosis of breast cancer patients has continuously improved (18,19). As breast cancer constitutes a major tumor type that metastasizes to the meninges, the management of DM should earn an increasing attention in the treatment of advanced breast cancer. The specific dissemination modes of DM remain unclear, and there are primarily three hypotheses: direct invasion from skull metastases, hematogenous spread, and post-surgical seeding. Among them, direct extension from skull metastasis is considered to be a common pattern, especially in the setting of extensive bony metastases (4,5,12,20,21). Surgical implantation is relatively rare among the three approaches (5,22,23). A study by Boram Ha found that among patients who underwent brain metastasis resection surgery without receiving radiotherapy after the procedure (including whole-brain and partial-brain radiotherapy), the proportion of those who developed leptomeningeal or DM was 43% (21 out of 55 patients) (12). In our study, we mainly explored patients without any brain surgery, approximately 81.1% of patients exhibited extensive bone metastases, with 66.7% had skull metastases. More interestingly, more than half of the study population prohibited a direct dural invasion at the skull metastases sites, providing new clinical evidence to direct-invasion hypothesis (Figure 4). In this study, we also categorized the morphological types of DM on MRI into three types. Survival analysis revealed that the survival duration for patients with the nodular type of DM was 447 days, which was the best prognosis among the three types. The survival duration for the mixed morphology, which is the combination of diffuse thickening and nodular type, was the shortest at 225 days. Nevertheless, there was no statistically significant difference in prognosis among these three groups, which is consistent with previous report (24). However, this study found that the proportion of the thickened with nodules type was relatively low among the three, and there may be two modes of hematogenous metastasis and direct infiltration, which could lead to differences in prognosis.

Figure 4 The arrow in the image indicates the sites of dural metastases, exhibiting thickening or nodular lesions. Direct dural invasions at the skull metastases sites can also be observed at the corresponding site of the DM focus. DM, dural metastasis.

Dural metastases that evolve from bone metastases often exhibit a gradual progression. This study revealed that the median time from the detection of bone metastases to the development of dural metastases exceeded 12 months. During this period, the majority of patients experienced distant metastases to other organs and even brain parenchymal involvement. At the time of DM diagnosis, most patients had disease progression after more than three lines system treatment.

The incidence of asymptomatic meningeal metastases reported in previous literature ranges from 11% to 50%, and it gradually increases with the availability of MRI (25). Consistent with previous reports, over half of the patients presented with neurological symptoms in this study. Given the frequent coexistence of brain metastases and the common involvement of cranial nerves, neurological symptoms were prevalent in this study, with headaches and nausea emerging as the predominant manifestations. A variety of treatment modalities have been employed to treat DM including surgery, radiation, and chemotherapy, while no clear standard of care has been established due to the rarity of DM and a lack of prospective data. Being situated beyond the blood-brain-barrier, the presence of DM renders it feasible to administer systemic drugs. Consequently, identifying suitable candidates for systemic treatment becomes a significant consideration. Dural metastases typically coincide with distant metastases, representing widespread dissemination of systemic disease. Due to the need to control systemic lesions and the anatomical location of dura, systemic therapy may be an effective treatment approach for asymptomatic or mildly symptomatic DM patients. To our knowledge, no survival benefit was obtained through chemotherapy, and there is no reports of antibody-drug conjugate (ADC) drugs such as DS-8201 in the treatment of DM. Surgical treatment is primarily applicable to solitary DM lesions in cases of stable systemic status. Due to effective systemic control, surgery to DM lesion may improve the overall prognosis (5). As an important local treatment modality, radiation therapy plays a significant role in controlling local progression and alleviating symptoms. It holds a crucial position in the treatment of brain metastases and leptomeningeal metastases. WBRT with 30 Gy delivered in 10 fractions is usually used for symptomatic treatment as palliative radiation (15). In addition, SRS can also be considered to apply as part of multidisciplinary treatment plans, with excellent tolerance and local tumor control rate (26). A retrospective analysis conducted by Boram Ha on patients who underwent surgery for breast cancer brain metastases found that both WBRT and PRT can reduce the probability of postoperative leptomeningeal carcinomatosis or dural metastasis (LMCDM) (12). This suggests that radiation therapy plays a role in reducing postoperative hematogenous meningeal metastasis. Similarly, Patel et al. reported a lower leptomeningeal carcinomatosis (LMC) rate of 13% during 18-month follow-up with WBRT and 31% with SRS (P=0.045) (13). Hsieh et al. also reported a similar result of LMC with WBRT (P=0.02) (14). A study by Sakaguchi et al. explored the therapeutic value of WBRT in patients with DM alone. The study results showed that patients with DM alone who received WBRT experienced symptom improvement and a reduction in death related to DM, suggesting radiation may be an effective treatment option for symptomatic DM patients (9). The studies stated above are all from retrospective analyses and lack substantial prospective research conclusions. However, there are still clinical significance, indicating that radiation therapy play a role in palliative treatment for breast patients with DM.

In our study, it was observed that patients who received radiation therapy (including WBRT and PRT) had a superior median survival time compared to those who did not, nearly doubling that of the untreated patients (458 vs. 225 days). Unfortunately, no statistical significance has been reached with P value of 0.06, which may be related to factors including the size of the study population, status of extracranial metastases and selection bias, as patients may receive palliative radiation when they are not deemed to be candidates for other treatments. From this point of view, it’s indeed that there are more concurrent brain parenchymal metastases, higher volume of DM and more symptomatic cases distributed to the radiation treatment group.

Although previous reports and the results of this study both support the clinical application of radiation therapy in DM, there is currently no consensus on whether to undergo radiation therapy, the optimal timing of radiation intervention, or the most suitable target volume and segmentation plan. This study also explores the issue of radiation therapy decision-making through relevant analysis. The factors typically considered when deciding whether to administer radiation therapy to those with DM include the presence of neurological symptoms, the presence of concurrent brain parenchymal metastases, control of extracranial lesions, the number of systemic treatment lines, molecular subtypes, and more. However, in this study, we found that the decision of radiotherapeutic strategy was associated with the DM burden and the presence of concurrent brain parenchymal metastasis but was not related to receptor status, systemic treatment status, or symptoms. The choice of radiation therapy regimen (whether to receive WBRT) was influenced by concurrent brain metastases, the DM burden, and leptomeningeal invasion but was unrelated to other clinical factors. Clearly, patients who received radiation therapy generally had more complex central nervous system metastatic conditions. As for the timing to initiate radiation therapy, in our study, among the patients who received radiation therapy, half of them underwent radiation therapy immediately upon the diagnosis of DM, while the other half continued systemic treatment until progression of meningeal lesions during the follow-up. Among those with immediate radiation therapy, half of them had concurrent brain metastases or leptomeningeal involvement, and the rest suffered neurological symptoms. We recommend WBRT to those with massive DM, and PRT may be more feasible to patients with limited lesions.

There are several limitations inherent to retrospective studies. Due to the relative rarity of DM, the limited number of study cases has resulted in selection bias and reduced statistical power. The wide time span of study cases, evolution in breast cancer treatment, advancements in radiation therapy techniques, and increased awareness of clinicians would all impact patient outcomes, and the lack of follow-up data could further impair the conclusions. Given the inherent bias in retrospective analyses, a large prospective study of breast cancer patients with DM is needed to precisely define the optimal timing and segmentation plan of radiotherapy.

Conclusions

In this study, we reviewed and analyzed data from 66 breast cancer patients diagnosed with DM. By mapping the progression pattern of DM evolving from long-term bone metastases, our findings provided new clinical evidence to direct-invasion hypothesis. Three morphological patterns were determined by MRI including nodular, thickened with nodules, and diffuse thickened types. The frontoparietal area was found to be the most commonly involved site and compression to cranial nerves could cause neurological symptoms. The use of radiotherapy (including WBRT and PRT) should be considered in the comprehensive treatment decisions for patients with high DM burden, concurrent brain parenchymal metastases, and those with neurological symptoms, for radiation would improve prognosis in these patients. We recommend WBRT to those with massive DM, and PRT may be more feasible to patients with limited lesions. On the other hand, these factors would significantly influence the decision-making process for radiotherapy, aiding in the identification of the optimal timing and best candidates for administering radiotherapy.

Acknowledgments

Funding: This work was supported in part by the National Natural Science Foundation of China (No. 81702601).

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://cco.amegroups.com/article/view/10.21037/cco-24-30/rc

Data Sharing Statement: Available at https://cco.amegroups.com/article/view/10.21037/cco-24-30/dss

Peer Review File: Available at https://cco.amegroups.com/article/view/10.21037/cco-24-30/prf

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://cco.amegroups.com/article/view/10.21037/cco-24-30/coif). All authors report the funding from the National Natural Science Foundation of China (No. 81702601). The authors have no other conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. The study was conducted in accordance with the Declaration of Helsinki (as revised in 2013) and received approval by the Ethics Committee of Ruijin Hospital, affiliated with the School of Medicine at Shanghai Jiao Tong University (No. 298). This study extracts information from the medical records of past patients, where the research risk is minimal and obtaining informed consent from the subjects is not feasible. Approval for the waiver of informed consent has been granted by the Ethics Committee.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

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