Trauma-induced recurrent of scalp dermatofibrosarcoma protuberans: a case report with a 6-year follow-up and literature review

Introduction

Dermatofibrosarcoma protuberans (DFSP) is a rare mesenchymal cell-derived soft tissue tumor. Its annual incidence is 0.00041% (1). DFSP was first named by Darier and Ferrand in 1924 (2). It is characterized by slow growth and local invasiveness with a high risk of local recurrence. Also, DFSP has a low risk of potential distant metastasis and only a small number of patients present with metastases to other organs. According to relevant studies, the proportion of patients with distant metastasis is less than 5% (3,4). Therefore, it is often referred to a benign/malignant borderline tumor or a potential low malignant tumor. In previous clinical study, the commonest site of incidence was the trunk (5). However, DFSP is extremely rarely located in the scalp. As a result, little is known about the triggers and the causes of recurrence of DFSP that occur on the scalp. For this reason, we have selected an interesting case from our institution for case report and literature review, with a view to providing some evidence for DFSP in diagnosis and treatment. The researchers were presented with the case of a young male patient who was admitted to the hospital of the authors in 2013 on account of a “scalp mass formed after external impact”, and followed up the case for 6 years. In 2019, the patient experienced recurrence of the local scalp mass after external impact. The researchers herein report the case by combining the relevant data of its pathogenesis, clinical manifestations, imaging findings, treatment methods, and immunohistochemical results. Further, the researchers retrospectively analyzed the current progress made in the research of DFSP. We present this article in accordance with the CARE reporting checklist (available at https://acr.amegroups.com/article/view/10.21037/acr-24-187/rc).

Case presentation

All procedures performed in this study were in accordance with the ethical standards of the institutional and/or national research committee(s) and with the Helsinki Declaration (as revised in 2013). Written informed consent was obtained from the patient for the publication of this case report and accompanying images. A copy of the written consent is available for review by the editorial office of this journal. The patient was a 34-year-old male who presented at the hospital of the authors in 2013 due to “a left posterior occipital scalp mass that had enlarged gradually for 18 years after external impact”. The patient informed the authors that 18 years prior, he had accidentally noticed a soft, non-tender mass growing in the left occipital region that could be pushed in a small area. At that time, he did not pay attention to it. Later, after external trauma, the scalp mass gradually increased in size, presenting a lavender red appearance, clearly demarcated with surrounding tissues, and about 5 cm × 6 cm in size. He presented to the hospital of the authors for further systematic diagnosis and treatment. The authors performed a relevant examination of this patient. A computed tomography (CT) scan of the patient’s head indicated a dome-shaped soft tissue dense shadow in the subcutaneous space of the left occipital region. The plain scan density was still uniform, the radiodensity was about 36 Hounsfield units (HU), the distal end of bilateral occipital artery was attached to the surface (mainly the left occipital artery), and there was no obvious blood supply to the tumor. Color Doppler ultrasound examination revealed a hypoechoic mass with a less uniform internal echo pattern, and the tumor could be seen in the blood-rich color. The patient underwent surgical treatment. Intraoperatively, the researchers found that the section of the tumor looked like pale fish flesh. Immunohistochemistry of this tumor revealed: vimentin (+), S100 (±), CD34 (+), neurofilament (NF) (−), CD68 (−), Ki67 (5%+), epithelial membrane antigen (EMA) (−), glial fibrillary acidic protein (GFAP) (−), muscle specific actin (HHF35) (−), P63 (−), progesterone receptor (PR) (−), tumor cell spindles, and mild atypia, suggestive of a potential schwannoma, but not excluding DFSP.

The researchers followed the patient for 6 years. In October 2019, the patient was admitted to the hospital on account of an 8-month history of a scalp mass that formed in the left posterior occipital region after physical trauma. The mass was soft and painless and had increased gradually in size, with dimensions of about 3 cm × 4 cm, and was mauve-red in color. It could be pushed and was clearly demarcated with surrounding tissues. A head CT scan revealed a slightly lower density shadow in the left parietal occipital scalp, with clear boundaries, close to the skull, and with uniform density (Figure 1A,1B). The radiodensity was about 36 HU, the occipital artery passed through the tumor surface, and there was no obvious blood supply to the tumor. surgical treatment. The researchers created an incision through the length and diameter of the tumor, and successively excised the skin and subcutaneous tissue. Intraoperatively, the researchers observed that the tumor tissue had subcutaneous invasion, a brittle texture, rich blood supply, blood supply from the occipital artery, and wrapped round the occipital nerve. The researchers used a blunt blade to separate these structures and completely excised the tumor tissue after achieving hemostasis. A cross-section of the tumor had the appearance of pale fish meat. Immunohistochemical assessment of the tumor revealed: vimentin (+), smooth muscle actin (SMA) (−), S100 (−), CD34 (+), NF (−), CD68 (−), Ki67 (15%), EMA (−), STAT6 (−), CD99 (±), and c1–2 (±) (Figure 1C-1E).

Figure 1 Radiological and pathological examinations. (A) The brain window of head CT shows the size of tumor. (B) The bone window of head CT shows the size of tumor. (C) H&E staining shows that tumor cells were fusiform and disordered in arrangement, with abundant cells and sparse cells in a few areas, accompanied by collagen fibers. Dilated or branching blood vessels could be seen. The magnification of the image is 10×. (D) H&E staining shows that fusiform, ovoid nucleus, fine chromatin, part of the nuclear membrane slightly irregular, little cytoplasm, eosinophilic, and visible nuclear division. The magnification of the image is 40×. (E) Immunohistochemistry of CD34 shows that the tumor cells tested diffusely and strongly positive for CD34. The magnification of the image is 20×. CT, computed tomography; H&E, hematoxylin and eosin.

There was some difference between the two pathological results obtained in 2013 and 2019. The immunohistochemistry results obtained in 2013 showed weak positivity for S100 and the researchers believed that there might be a slight error in the detection process. At the same time, researchers improved the immunohistochemistry of STAT6 and other related indicators to exclude the diagnosis of isolated fibrous tumors. In summary, the researchers considered the results of multiple immunohistochemical examinations and the clinical features of this case to be consistent with the diagnosis of dermal DFSP.

Discussion

DFSP is a rare fibroblast-derived sarcoma (6). Due to its nonspecific clinical manifestations and the long time it takes to achieve an accurate diagnosis, its initial misdiagnosis rate is relatively high. Therefore, incomplete resection and subsequent recurrence of the tumor are common. A study has shown that the local recurrence rate of DFSP is 10–60%, while the distant metastasis rate is less than 5% (7). Approximately 10% of DFSP cases are associated with trauma, surgical or burn scarring, or even immunization at the site of disease. However, the association between DFSP incidence and the above events has not been established clearly (8,9).

Diagnosis

Golden criteria of diagnosis

DFSP is a kind of cellular tumor, which is composed of spindle cells with slender nuclei, small cells with atypia, a low mitosis count in the collagen stroma, and tumor cells often spread along the fascia of subcutaneous adipose tissue. In general, CD34 is expressed diffusely in DFSP, as are vimentin, nestin, apolipoprotein D, cytokeratins, SMA, S100, CD56 factor XIIIa, stromelysin 3, and cathepsin K. Its histological subtypes include myxoid, pigmented or Bednar tumors, atrophic, sclerosing, granulosa cell, giant cell fibroblastoma, and tumors with fibrosarcoma transformation (FS-DFSP) (10).

Auxiliary imaging

Both CT and magnetic resonance imaging (MRI) scans of DFSP patients have obvious characteristics, which are helpful for qualitative diagnosis and preoperative evaluation, and have some value in clinical application. On CT/MRI scans, DFSP presents as a non-calcified, superficial, nodular mass with uniform density, and MRI scans show long T2 and short T1 signals (11,12). Similarly, DFSP should be considered when ultrasound indicates that a subcutaneous ovoid mass is prominent in the skin and presents a localized lobulated weak echo or irregular mixed echo (13). Ultrasound can clearly show the boundary, internal structure, and blood supply of the lesion, which are conducive to judging the surgical resection range and determining the postoperative treatment. In fact, preoperative imaging is useful in assessing the extent of DFSP, particularly if it is large, atypical, recurrent, or affects critical anatomical sites (14). In the European guidelines, preoperative ultrasound and MRI examinations are recommended (15). However, MRI scan is usually the first choice for high-resolution soft tissue imaging and CT examination is more useful in detecting tumor invasion (16).

Treatment

According to the National Comprehensive Cancer Network guidelines for soft tissue sarcoma, the initial treatment for DFSP is surgery, and complete surgical resection and tumor-free surgical incision margins are the basic principles for the treatment of DFSP (17). Common surgical procedures include Mohs surgery and conventional extensive resection requiring at least 2–4 cm of negative peripheral tumor (18,19). However, the European treatment guidelines suggest that DFSP should reach a cutting margin of 3 cm for extensive resection (20). Mohs surgery can ensure that the soft tissue defect of tumor resection is minimized and the pathological examination of the cutting edge yields negative results. However, this procedure requires that the procedure is repeated until the cutting edge is free of tumor cells (21). At present, there is no clinical trial evidence indicating the balance of advantages and disadvantages between Mohs surgery and extended resection. Moreover, Mohs surgery takes a long time and requires a lot of hospital equipment and surgical teams, and thus cannot be popularized at every hospital (22). Therefore, under the premise of oncology safety, the setting of the thinnest cutting margin in DFSP surgery still needs to be evaluated in a clinical trial with a large sample. Human scalp is an organ with complex biomechanical properties, and special attention should be paid to the consideration of surgical incision, including the mechanical characteristics of different directions and different times, in order to obtain a more beautiful and safer surgical incision (23). In addition, imatinib mesylate, a tyrosine kinase inhibitor, can be used for the treatment of patients with unresectable disease or who are intolerant (24).

Summary

The pathogenesis of DFSP is not yet clear and it is prone to misdiagnosis. In this case, the patient was diagnosed with scalp hematoma on three occasions at his first admission. At the second admission, the patient was once diagnosed with a scalp hematoma. Of course, this is related to a clear history of external impingement, and the researchers believe that repeated external stimulation may accelerate DFSP growth. In fact, some studies suggest that there is indeed a link between the tumor and the impact of local forces. In these studies, the researchers posited that radiation, the immune response, accidental trauma, insect bites, and post-burn scars may lead to chronic inflammation of the tissue and disruption of wound healing, so that CD34-positive cells in the tissue may be overstimulated in the process of mediating tissue repair and eventually render the tumor malignant (25-27). In this paper, the authors report a case of DFSP after repeated external trauma. The patient underwent surgical treatment at the authors’ hospital in 2013, and was followed up for 6 years. In 2019, the tumor recurred at the previously operated area. Notably, the patient also had a history of external trauma, which was the first case of this kind known to the authors and followed up. This case also provides some evidence-based medical evidence for the association between trauma and DFSP. In this case, the patient was admitted to the hospital in 2013 and 2019 due to scalp masses after sustaining external trauma to the head and underwent surgical resection. During the operation performed in 2013, the authors observed that the tumor, occipital artery, and greater occipital nerve were all located under the aponeurotic cap, and the tumor surface was covered by a false capsule so that the aponeurotic cap and periosteal membrane were not invaded. At the same time, the tumor was adhered to the occipital artery and greater occipital nerve, but they could barely be separated from each other. This finding may explain the weak positive immunohistochemical results of S100 index obtained in 2013, which the researchers believe may have been caused by incomplete separation of nerves on the tumor surface. During the surgery performed in 2019, the study authors found that the local blood supply to the scalp of the patient was significantly increased, and the tumor invaded part of the dermis and skull membrane. Moreover, within about 3 cm of the tumor diameter, the study authors found three small local lesions, which also indicated that the tumor often recurs locally or with metastasis. Based on this change, the study authors posit that before the surgical management of patients with recurrent DFSP, there is a need to create a plan to expand the resection of the lesion and to prepare for flap transfer. At the same time, in the pathological diagnosis, the immunohistochemical results obtained in 2019 showed a Ki67 index of 15%, which was significantly increased compared with the 5% obtained in 2013, indicating that the lesion had some malignant biological behavior, and that the degree of malignancy was likely to increase with each recurrence of the lesion. Further, intraoperative lesions were seen to invade the dermis of the skin and the underlying periosteum, and there were adjacent tumor metastases, which also provided some evidence for this reasoning.

Conclusions

DFSP is relatively rare in clinical practice, especially on the scalp. The researchers followed up this case for 6 years to analyze the pathogenesis, clinical manifestations, imaging manifestations, treatment methods, and immunohistochemical results of DFSP on the scalp. This case has gone through 6 years from the first diagnosis to relapse, and the history of the disease can be traced forward up to 18 years ago, and the whole medical history is 24 years long, which also illustrates with a practical example that DFSP has a characteristic that it has atypical clinical symptoms and long time to accurate diagnosis; thus, it is easily misdiagnosed. We proposed that head trauma may be a causative factor in the development and recurrence of DFSP on the scalp, which is interesting and attractive. According to this, we provide some basis for evidence-based medicine regarding the preoperative qualitative evaluation and treatment of this disease and has some value for clinical application. Possible directions for clinical and basic research on DFSP are also suggested.

Acknowledgments

We would like to express our gratitude to all those who helped us during the writing of this manuscript and thanks to all the peer reviewers for their opinions and suggestions.

Footnote

Reporting Checklist: The authors have completed the CARE reporting checklist. Available at https://acr.amegroups.com/article/view/10.21037/acr-24-187/rc

Peer Review File: Available at https://acr.amegroups.com/article/view/10.21037/acr-24-187/prf

Funding: This work was supported by Hunan Provincial Natural Science Foundation of China (No. 2020JJ6105) and the Hospital-Level Project of Zhuzhou Central Hospital in Hunan Province (No. 202009901).

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://acr.amegroups.com/article/view/10.21037/acr-24-187/coif). The authors have no 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. All procedures performed in this study were in accordance with the ethical standards of the institutional and/or national research committee(s) and with the Helsinki Declaration (as revised in 2013). Written informed consent was obtained from the patient for the publication of this case report and accompanying images. A copy of the written consent is available for review by the editorial office of this journal.

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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