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10.1245/ASO.2004.06.014
Annals of Surgical Oncology 11:438-444 (2004)
© 2004 Society of Surgical Oncology
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ORIGINAL ARTICLES

Modified Mohs Micrographic Surgery in the Therapy of Dermatofibrosarcoma Protuberans: Analysis of 22 Patients

Joerg Wacker, MD, Benjamin Khan-Durani, MD and Wolfgang Hartschuh, MD

From the Department of Dermatology, University of Heidelberg, Heidelberg, Germany.

Correspondence: Address correspondence and reprint requests to: Wolfgang Hartschuh, MD, Universitäts-Hautklinik, Department of Dermatology, University of Heidelberg, Voßstrasse 2, D-69115 Heidelberg, Germany; Fax: 49-6221-565945; E-mail: wolfgang_hartschuh{at}med.uni-heidelberg.de


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
 REFERENCES
 
Background: Dermatofibrosarcoma protuberans (DFSP) is a very rare, low-grade malignant tumor. Local recurrence is frequent after incomplete resection either because of false diagnosis or inadequate standard surgical excision. This study evaluated the clinical outcome of micrographic surgery with paraffin sectioning in the therapy of DFSP.

Methods: Medical charts of 22 patients with histologically confirmed DFSP treated at our institution between 1987 and 2002 were reviewed.

Results: For 13 patients with primary and 9 with recurrent disease, tumor-free excision margins could be achieved, and all patients remained free of local recurrence during a mean follow-up of 54 months.

Conclusions: The results of our study and a review of the literature confirm the successful and recurrence-free treatment of DFSP with micrographic surgery as the treatment of choice for this locally invasive tumor. Particularly in recurrent lesions, we recommend the use of paraffin sectioning and three-dimensional histological evaluation as an accurate additional tool for treatment optimization.

Key Words: Dermatofibrosarcoma protuberans • Micrographic surgery • Local recurrence • Residual tumor


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
 REFERENCES
 
Dermatofibrosarcoma protuberans (DFSP) is a very rare fibrohistiocytic soft tissue tumor. Clinically DFSP shows the characteristics of a low-grade malignant tumor, with a slow, sometimes aggressive and locally infiltrative growth through the dermis into the subcutaneous fat tissue. Systemic metastasis is rare and usually occurs in recurrent lesions at later stages of the disease.1–5

The median age of diagnosis is 20 to 50 years; however, all age groups are affected. A slight male predominance has been suggested.6 Initial lesions present as red or skin-colored, sometimes pigmented, indurated plaques with surrounding red or blue discoloration.2,7 Atrophic skin manifestations have rarely been described.8,9

Symptoms are rare, and this frequently causes disregard of the lesions by patients. Plaques may persist at stable size or show slow and often indolent growth. Rapid increase of the growth rate can evolve after a period of dormancy and can cause characteristic protuberant nodules. Ulceration, induction of pain, and satellite lesions are observed in large tumors. DFSP predominates on the trunk (50%–60%) and upper limbs (25%). A total of 10% to 15% of the tumors are localized at the head and neck, but all other regions can be affected.7

The major principle of therapy is surgical resection of the tumor. Because of the locally invasive growth characteristics of DFSP, high local recurrence rates of up to 60% are dreaded complications. Extensive resections with surgical margins of 3 cm still lead to rates of recurrence of up to 20% caused by residual tumor cells after incomplete resection.10

Therefore, Mohs micrographic surgery (MMS), developed for precise margin control in the treatment of locally invasive malignant cutaneous tumors, was established for surgical therapy of DFSP.11–13 Micrographic surgery is defined as the resection of the visible tumor, including a small safety margin. The excision is followed by a complete histological evaluation of the excision margins, including the tumor base. This technique allows the topographic correlation and complete excision of residual tumor fractions.

Two different techniques of micrographic surgery have been established. The original MMS is performed on frozen sections. Horizontal sectioning (5–7 µm) is performed, thus allowing complete evaluation of the tumor base and the continuously visible outer peripheral margins of the excised tissue.14 Modified MMS was established by Breuninger and Schaumburg-Lever15 and uses paraffin-embedded sections. The complete outer margins, the base, and the central sections of the excised specimens are processed for histological evaluation.

In a retrospective study of 22 patients treated with modified MMS on paraffin sections at our institution, the clinical outcome, focusing on the absence of relapse, was analyzed.


   METHODS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
RESULTS
 DISCUSSION
 CONCLUSION
 REFERENCES
 
The medical charts of 22 patients with primary or recurrent DFSP who underwent surgical treatment between 1987 and 2002 were analyzed. Patient demographic data, tumor location, information regarding previous therapy, the number of necessary stages of micrographic surgery, and the recurrence-free interval were evaluated.

Surgical treatment was performed by using micrographic surgery with paraffin sectioning. The visible and palpable tumor or residual scar tissue was excised with an approximately 1- to 2-cm lateral excision margin of clinically unaffected skin from the visible tumor margin. The marked tissue was formalin-fixed, and 2- to 3-mm-wide and approximately 20-mm-long bands of the peripheral area of the specimens enclosing the lateral parts of the safety margin were removed. Subsequently, a horizontal section of the basis and vertical sections from the center of the tumor were taken. All specimens representing the entire outer surface of the resection margins were paraffin-embedded and cut for histological evaluation. The sections were stained with hematoxylin and eosin. In recurrent lesions or hypocellular tumor regions, additional immunohistological staining with an anti-CD34 antibody was performed to detect microscopic extensions of the tumor and to discriminate between scar tissue and residual tumor. Histologically positive excision margins gave rise to tumor mapping by stepwise extending of the excision margins. The skin defects were temporarily covered with synthetic wound dressings until complete excision was proven. Reconstruction was then performed by flaps or skin grafts.

The period of follow-up was determined by the duration from excision to the last examination. Patients who did not appear for follow-up were contacted by telephone.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
DISCUSSION
 CONCLUSION
 REFERENCES
 
A total of 22 cases were reviewed, and clinical outcomes were observed. The mean patient age at surgery was 41 years (range, 21–69 years). Fifteen patients were female, and seven were male. Eighteen tumors were located on the trunk and the neck, one tumor was parietal, and three were on the upper or lower limbs.

Thirteen of the tumors were primary DFSP. Nine of the patients with recurrent disease had received several surgical excisions at other institutions. Tumor size ranged from 1.5 to 15 cm; excised scar areas had a length of up to 15 cm.

Patients were treated with one to three stages of micrographic surgery to achieve histologically tumor free margins. After the first stage of surgery, including an initial lateral excision margin of 1 to 2 cm, 10 of 22 tumors were completely excised. Ten were excised en bloc after two stages. Two tumors required a third excision because of an extensive spread of residual tumor cells into deeper tissues, including both muscle and periost.

One patient needed resection of the cortical bone at the scalp because of periosteal and osseous infiltration by tumor cells. In one patient, deep infiltration into the pectoral muscle led to resection of the affected tissue (Figs. 1–3GoGo).



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  		FIG. 1. (A) A 21-year old female patient with dermatofibrosarcoma protuberans of the scalp. The lesion occurred 2 years previously and showed a constant increase of extension without symptoms. (B and C) After two stages of micrographic surgery, the scalp and, in the second stage, periost were excised. Still, residues of tumor cells were found, and parts of the parietal bone were extirpated. (D) The defect was closed with a split-skin graft because a complete histographical margin control is not possible in osseal tissue. Thus, precise control of the lesion was ensured, and alteration of the anatomy was avoided. The figure shows the condition 4 years after transplantation.

 


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  		FIG. 2. Primary atrophic dermatofibrosarcoma protuberans of a 49 year-old male patient. The tumor persisted for 16 years without recognizable alteration. Three stages of micrographic surgery were necessary to achieve tumor-free margins. The tumor had deeply penetrated fascia and muscle, which had to be excised.

 


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  		FIG. 3. Recurrent tumor of a 55-year-old female patient. The excision of the primary DFSP was performed 10 years earlier and was diagnosed as a dermatofibroma. The tumor grew for 1 year without any symptoms. After one stage of micrographic surgery, the tumor was completely excised.

 
Patients were monitored for recurrence over a mean interval of 54 months (range, 3–180 months). After surgical resection, none of the patients showed recurrent disease or distant metastasis (Table 1).


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  		TABLE 1. Patient characteristics and results of micrographic surgery (MS) with paraffin sectioning
 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
CONCLUSION
 REFERENCES
 
The premise for a sufficient surgical therapy of DFSP is complete excision of the tumor. Tumor biology—especially slow, infiltrative growth—and the subclinical spread of DFSP have been held responsible for the high rates of local recurrence after insufficient surgery.6 To prevent recurrent disease, extended safety margins have been recommended since the 1950s.16 However, despite safety margins of up to 5 cm, recurrence rates varying from 10% to 60% were reported until 2000. Micrographic surgery is not accepted unequivocally.17,18

The standard pathologic procedure for evaluation of tumor specimens includes the examination of a series of vertical sections of the tissue. These are taken at representative sites, and usually 2- to 4-mm intervals are chosen for a bread loaf–like preparation of the tissue specimen. This technique represents an accurate and sufficient way to determine complete resection for most solid and well-defined tumors. In cases of tumors with infiltrative growth, however, finger-like extensions may be present in the unexamined 2 to 4 mm of tissue between the examined sections. This may lead to false-negative interpretation of the excision margins.14 DFSP tends to grow in an asymmetrical manner, thereby rendering standard surgical therapy with wide excision margins and standard pathologic procedures insufficient.

In a large retrospective analysis of 159 patients with DFSP between 1958 and 1998, Bowne et al.19 reviewed histopathologic slides for negative microscopic margins after wide surgical excision and standard excisional processing. On pathologic review, only 58% of the patients had confirmed negative margins, and 42% had positive or close to positive (<1-mm) margins, leading to a recurrence rate of 21%. As a result of this study, the authors held the incomplete resection of tumor cells responsible for the high relapse rates of the disease.

A more comprehensive microscopic examination of the surgical margin can be achieved by using MMS. This technique is indicated for locally aggressive malignant cutaneous tumors that are removed sequentially. After excision of the clinically apparent tumor with narrow safety margins, horizontal frozen sections containing the entire periphery and the basis of the resected specimen are microscopically examined. Therefore, a complete evaluation of the three-dimensional border of the excised tissue and precise localization of residual tumor for subsequent removal is possible, yielding the highest cure rates. With MMS, a maximum amount of normal skin can be preserved while clear margins are achieved, leading to smaller skin defects and improved cosmetic results. With the implementation of MMS, this option was used in numerous patients with DFSP, and good clinical outcome was reported.10,20

In support of these notions, Ratner et al.21 determined the microscopic tumor extent of DFSP in 58 patients treated with MMS and estimated the safety margins needed with standard wide excision to eradicate all tumor cells. Negative margins would have been achieved in only 30% after a 1-cm-wide excision and in only 85% with a 3-cm excision margin. Two patients showed microscopic extensions of >10 cm away from the edge of the visible tumor.

A potential shortcoming of MMS may be the difficulty of discriminating between normal stromal cells and capillary tumor cell branches of residual DFSP in the peripheral areas of the tumor. DFSP mostly shows an expression of CD34 antigen and negativity for anti–factor XIIIa. The immunohistochemical detection of CD34 was initially applied to the differential diagnosis of DFSP versus benign fibrous histiocytoma.22,23 In addition, CD34 staining can be a very helpful tool in the detection of microscopic extensions of the tumor and in the discrimination between scar tissue and residual tumor, especially in hypocellular areas.24 However, on frozen sections, the transition zone between the end of the tumor and normal skin can be poorly defined with both hematoxylin and eosin and CD34 staining because of the presence of scattered dermal spindle cells. These cells are also seen on frozen sections of normal skin. Therefore, it is recommended that a control biopsy sample of normal skin from a similar anatomical site be taken during MMS on frozen sections to distinguish normal dermal spindle cells from DFSP.25

Further problems may arise when large tumor specimens and large amounts of subcutaneous fat have to be processed. Complete evaluation of all horizontal sections of the tumor is time consuming, and scattered tumor cells may remain undetected because of the large number of sections. Stojadinovic et al.17 reported a false-negative rate of 57% on frozen sections. Although only a median number of 3 (range, 1–20) frozen sections—the deep margins and only 1 or more lateral margins—were evaluated.

Nouri et al.26 observed no false-negative results in 20 patients with DFSP treated with MMS. However, the final stage of MMS was sent to pathology for paraffin sectioning and CD34 immunostaining to prove negative surgical margins. The authors proposed the final permanent pathology section to circumvent the difficulties described previously in distinguishing spindle cells in DFSP from fibroblasts or scar tissue.

Some authors recommend the modified MMS on paraffin-embedded sections with three-dimensional analysis of the excision margins established by Breuninger and Schaumburg-Lever15 and Breuninger.27 The method uses routine histology techniques, including immunohistochemistry for CD34. Further advantages of this method lie in the high quality of the resulting slides, the accuracy of the discrimination of fine tumor strands from normal skin, and the clear survey of the excised tumor. Only a small number of slides compared with the tumor size have to be evaluated. However, the complete procedure of tissue processing requires approximately 24 hours and thus requires a temporary covering of the defect with biosynthetic dressings.

At our institution, modified MMS is routinely used for the treatment of DFSP. Our patient group included many recurrent tumors that were pretreated at other institutions. In such patients, the differentiation of scar tissue and hypocellular areas of DFSP is very challenging and can be successfully and reliably performed only on paraffin sections.

Our series also included a large number of widespread tumors of up to 15 cm in size and extensive scars; this resulted in large excision specimens. Compared with the modified Mohs procedure on paraffin sections, an exorbitant number of frozen sections had to be evaluated in an extensive work-up.

Most recurrences tend to develop within 3 years.2,3,16 No patient in our group relapsed within the mean follow-up time of 54 months, and this outlines the favorable outcome of MMS in the therapy of DFSP.

When overall recurrence rates are compared, there is a clear benefit for micrographic surgery. Including our series, there are, to the best of our knowledge, 303 cases of DFSP documented in the literature that were treated with MMS (Table 2).[[28–41]:]: Most authors used standard MMS, but in some studies the combination of MMS and paraffin sections was performed. Only 6 of 303 patients showed recurrent disease, resulting in a recurrence rate of 2.0% (Table 2) compared with a recurrence rate of 10% to 60% for conventional surgery.


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  		TABLE 2. Micrographic surgery and recurrence rates in the treatment of dermatofibrosarcoma protuberans: review of the literature
 
Because 70% of DFSP may extend microscopically at least 1 cm beyond the visible edge of the lesion,16 we recommend an initial safety margin of at least 1 cm at the first stage of MMS. This may have contributed to the fact that no recurrent tumor was observed in our group.

A limited risk still remains of the persistence of residual tumor cells in recurrent lesions, particularly after multiple previous surgeries. In those cases, we propose a reconstruction of the wound defects with skin grafts. Thus, the anatomical structures can be maintained, and observation of the excised area at clinical follow-up is facilitated.


   CONCLUSION
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
REFERENCES
 
In our opinion, complete three-dimensional histological evaluation on paraffin sections, including immunohistochemistry for CD34, is the most accurate therapy for DFSP and is recommended especially in widespread tumors or recurrent disease. In either case, gross excision margins have to be displaced by micrographic surgery. This feasible procedure will decrease the high recurrence rates that are still found in the recent literature and will help to avoid unnecessary wide excisions that cause large skin defects.


   FOOTNOTES
 
By means of analysis of 22 patients with dermatofibrosarcoma protuberans and a review of the literature, we show that micrographic surgery is imperative to prevent relapse after surgical treatment of dermatofibrosarcoma protuberans, and it is recommended as the treatment of choice.

Received for publication June 11, 2003. Accepted for publication November 24, 2003.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
 REFERENCES
 

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