Mohs Micrographic Surgery for Deeply Penetrating,Expanding Benign Cutaneous Neoplasms

DANIEL S. BEHROOZAN, MD,�y LEONARD H. GOLDBERG, MD, FRCP,�z

ADRIENNE S. GLAICH, MD,� BARUCH KAPLAN, MD,y AND VALDA N. KAYE, MDJ

The authors have indicated no significant interest with commercial supporters.

Mohs micrographic surgery

(MMS) is an effective

technique for the removal of cu-

taneous malignancies. High cure

rates are achieved by using precise

surgical margin control while

providing maximal normal tissue

preservation, thus optimizing

subsequent wound healing and

cosmesis.1

The indications for MMS include

malignant tumors with poorly

defined borders, histology, tumor

size, level of invasion, anatomic

location, reduced patient immu-

nity, and recurrence after previous

treatment. MMS is indicated for

locally aggressive tumors that are

difficult to eradicate by routine

measures and recurrent tumors

following conventional surgical

excision.1–8 MMS has been used

successfully for the excision of

basal cell carcinoma, squamous

cell carcinoma, squamous cell

carcinoma in situ, keratoacantho-

ma, microcystic adnexal carcino-

ma, dermatofibroma sarcoma

protuberans, and extramammary

Paget’s disease.1 Recent reports

have also shown MMS to be suc-

cessfully used for melanoma, es-

pecially the lentigo maligna

subtype.9

We report four cases of deeply

penetrating, enlarging, histologi-

cally benign cutaneous neoplasms

that were removed by MMS. All

diagnostic biopsy specimens were

evaluated by a board-certified

dermatopathologist (V.N.K.) be-

fore performing MMS. The aim of

this article is to provide evidence

to expand the indications of

MMS to include certain benign

tumors with aggressive growth

characteristics. This includes

widely growing or deeply

penetrating benign cutaneous

neoplasms, especially in anatomic

areas where tissue preservation is

critical (Table 1).

Case Reports

Patient 1

A 45-year-old woman presented

with an enlarging 1.6�2.0-cm

red nodule on her right temple

(Figure 1A). The lesion had been

previously biopsied as a benign

cylindroma, and it was left with-

out further treatment. It contin-

ued to grow in width and depth,

however. Ten years later, after the

tumor had increased to double its

size, a second biopsy specimen

again revealed a dermal tumor

consistent with cylindroma. Is-

lands of epithelial cells varied in

size and shape and were separated

by a hyaline sheath and narrow

band of collagen in a ‘‘jigsaw

puzzle’’ configuration (Figure 2).

Duct-like structures were also

present. The tumor had pene-

trated the dermis and the deep

subdermal fat, and its exact mar-

gins could not be ascertained

clinically. It was located on the

sideburn in a cosmetically sensi-

tive area. Despite the benign na-

ture of the tumor, the patient

elected for MMS as a tissue-

conserving surgical excision pro-

cedure. The tumor was excised in

two stages. The final defect

penetrated the deep subcutaneous

fat and abutted the subcutaneous

musculoaponeurotic system

(Figure 1B).

& 2006 by the American Society for Dermatologic Surgery, Inc. � Published by Blackwell Publishing �ISSN: 1076-0512 � Dermatol Surg 2006;32:958–965 � DOI: 10.1111/j.1524-4725.2006.32204.x

9 5 8

�DermSurgery Associates, Houston, Texas; yDivision of Dermatology, David Geffen School of Medicineat UCLA, Los Angeles, California; zDepartment of Dermatology, Weill Medical College of CornellUniversity, New York, NY; yPrivate Practice, Tel Aviv, Israel; JDepartments of Dermatology and Pa-thology, University of Minnesota, Minneapolis, Minnesota

Patient 2

A 55-year-old woman was re-

ferred for treatment of an enlarg-

ing 0.6�0.5-mm flesh-colored

papule on her nasal tip (Figure

3A). The clinical size of the pa-

tient’s tumor had doubled over 6

months. Histologic examination

revealed a proliferation of slender

basaloid nests within dense fi-

brous tissue and focal calcifica-

tion and chronic inflammation

throughout the superficial and

middermis consistent with des-

moplastic trichoepithelioma (Fig-

ure 4). The margin of this tumor

could not be clearly detected

clinically. The patient requested

MMS due to the poorly defined

margins and cosmetically sensitive

location of the tumor. The tumor

was cleared after five stages and

resulted in a full-thickness dermal

defect measuring 1.7� 1.5 cm

(Figure 3B) that was repaired with

a full-thickness skin graft.

Patient 3

A 44-year-old man presented with

a 1-year history of a painless, en-

larging 4� 5-cm firm, yellowish

subcutaneous nodule over the

outer surface of the right heel

(Figure 5A).10 An incisional

biopsy revealed poorly circum-

scribed islands of cells with ample

cytoplasm and a distinct granular

appearance within the dermis and

subcutaneous tissue, consistent

with a granular cell tumor (Figure

6). Three stages of MMS were

needed to clear the lesion, and the

final defect (Figure 5B) was al-

lowed to granulate and epithe-

lialize.

Patient 4

A 49-year-old man presented for

removal of an enlarging 3.0�2.5-

cm tumor on the mid–scalp vertex

(Figure 7A). The tumor had de-

veloped over a 3-month period

and was deeply invasive on clini-

cal examination. Incisional biopsy

yielded a diagnosis of pilo-

matrixoma. Microscopically, ir-

regular islands of epithelial cells

composed of two cell types were

situated deep in the dermis and

surrounded by a fibrous stroma

(Figure 8). Cells toward the pe-

riphery had basophilic nuclei and

scanty cytoplasm with indistinct

TABLE 1. Suggested Indications

for Mohs in Benign Tumors

Size

Enlarging

Diagnosis (Table 2)

Poorly defined margins

Location in cosmetically critical

areas

Recurrence

Penetration beyond the dermis

Figure 1. Patient 1: (A) cylindroma before treatment; (B) defect after two stages of Mohs micrographic surgery.

TABLE 2. Nonmalignant Prolif-

erating Cutaneous Neoplasms

Cylindroma

Desmoplastic trichoepithelioma

Granular cell tumor

Pilomatrixoma

Proliferating pilar tumor

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cellular borders. Shadow cells

were present centrally and had a

central, unstained area with a

distinct border. Focal calcification

was present. Owing to the large

size and unclear depth of pene-

tration, it was decided that MMS

would be the most efficient and

certain method to completely ex-

cise this tumor. One stage of

MMS was needed to clear the

tumor with the final defect pene-

trating to the galea aponeurotica

(Figure 7B).

Discussion

The management of tumors with

aggressive histologic or clinical

growth patterns similar to malig-

nant tumors is a clinical conun-

drum. The conundrum is that the

surgeon does not want to remove

too much normal tissue for a be-

nign tumor, but on the other

hand, does not want to leave ac-

tively enlarging tumor either at

the depth or at the lateral mar-

gins. This report demonstrates

four such tumors. The ability to

check margins with microscopic

control by the Mohs technique to

verify complete removal and save

unnecessary removal of normal

tissue is a logical and effective

method by which to extirpate

these aggressive benign cutaneous

neoplasms.

Excision of cutaneous neoplasms

with difficult to determine mar-

gins, whether due to their depth

or poorly defined clinical margins,

Figure 2. Histology of tumor of Patient 1: (A) Tumor present in the dermis composed of islands of epithelialcells (hematoxylin and eosin, �2); (B) higher magnification shows the hyaline sheath and narrow bandsof collagen that separate the nests of epithelial cells in a ‘‘jigsaw puzzle’’ configuration (hematoxylin andeosin, � 10).

Figure 3. Patient 2: (A) Desmoplastic trichoepithelioma before treatment; (B) defect after five stages withMohs micrographic surgery.

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should ideally be carried out with

frozen section control of margins.

This approach reduces the risk of

the embarrassing postoperative

visit where the patient is informed

of the incompleteness of surgical

excision and the variable need for

repetition of the entire surgical

process. Tumors that may benefit

from this surgical approach in-

clude, but are not limited to,

cylindroma, desmoplastic tricho-

epithelioma, granular cell tumor,

pilomatrixoma, and proliferating

pilar tumor (Table 2).

Once the decision is made to ver-

ify margins with frozen section

control, the choice is between

MMS with en face evaluation of

margins or ‘‘breadloafing’’ to ob-

tain representative sections of the

margins. MMS with en face ex-

amination of margins is more

accurate and desirable when

available.11 For this reason, MMS

was chosen as the excisional

technique of choice in all the

tumors described in this report. If

MMS is not available, however,

excision with routine frozen sec-

tion examination is far superior to

excision without frozen section

control.

Cylindroma

Cylindromas are adnexal neo-

plasms of apocrine or eccrine

sweat glands. They present singly

or in multiplicity and occur most

commonly on the scalp but may

develop on the face, neck, arms,

and trunk.12 Histologically,

sharply circumscribed nodules

composed of nests of basaloid

cells in close apposition are

Figure 4. Histology of tumor from Patient 2: superficial andmiddermis with basaloid nests with dense fibrous tissue, focalcalcification, and chronic inflammation (toluidine blue, �4).

Figure 5. Patient 3: (A) granular cell tumor before treatment; (B) resulting defect after three stages of Mohsmicrographic surgery. Figures reproduced with permission of editor (Chilkuri S, Peterson SR, Goldberg LH.Granular cell tumor of the heel treated with Mohs technique. Dermatol Surg 2004; 30:1046–9).

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arrayed within the dermis in a

complex ‘‘jigsaw puzzle’’ pat-

tern.15 A thick band of periodic

acid-Schiff–positive hyaline base-

ment membrane material envelops

the individual nests, and droplets

of similar composition are often

scattered centrally within these

small nests. This benign adnexal

proliferation may recur if not

completely excised. Recurrence

becomes a problem when cylin-

dromas occur in areas of cosmetic

importance or when tumors are

rapidly expanding and deeply

penetrating. For example, Patient

1 required MMS for a cylindroma

of the temple to microscopically

map out the tumor and remove

proliferating cells that were deep-

ly penetrating and had previously

been incompletely excised by

conventional surgical modalities.

Desmoplastic Tricho-

epithelioma

Desmoplastic trichoepitheliomas

are benign adnexal tumors that

generally present as firm, skin-

colored to erythematous papules

or plaques.16 They most often

occur in sun-exposed areas, espe-

cially on the face. Lesions can also

develop on the scalp, neck, and

upper trunk.17 Clinically, desmo-

plastic trichoepitheliomas may

resemble basal cell carcinoma,

Figure 6. Histology of tumor from Patient 3: dermis and sub-cutaneous tissue with poorly circumscribed islands with agranular appearance (hematoxylin and eosin, � 40).

Figure 7. Patient 4: (A) pilomatrixoma before treatment; (B) full-thickness defect to the galea aponeurotica aftercomplete excision with Mohs micrographic surgery.

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sebaceous hyperplasia, conven-

tional trichoepithelioma, gran-

uloma annulare, or scar.17

Histologically, the tumor shares

features with morpheaform basal

cell carcinoma, trichoepithelioma,

syringoma, microcystic adnexal

carcinoma, basaloid follicular ha-

martoma, and trichoadenoma.17

Microscopically, desmoplastic tri-

choepitheliomas are composed of

narrow strands of basaloid tumor

cells arrayed in a background of

thickened collagen bundles and

keratinous cysts. These benign le-

sions, however, can be clinically

and histologically misdiagnosed

as a malignancy. The clinical and

histologic picture often mimics

other conditions, making diagno-

sis challenging, often necessitating

reexcision or resampling for de-

finitive diagnosis. Smaller tumors

can be surgically excised. Other

alternatives include dermabrasion

and laser surgery, although these

options may be associated with an

increased rate of recurrence be-

cause they have poorly defined

clinical margins.18,19

Granular Cell Tumor

Granular cell tumors typically

present as an asymptomatic, skin-

colored or brownish-red, firm

dermal or subcutaneous papulo-

nodule in the head and neck re-

gion. These tumors occur mainly

in adults and most commonly oc-

cur on the tongue. Two-thirds of

the cases are reported in women

and two-thirds of the cases are

reported in black persons.20,21

Microscopically, the dermis con-

tains a poorly circumscribed nod-

ule or a peripheral infiltrative

pattern of polygonal, pale-stained

cells. The cells have abundant,

granular, faintly eosinophilic cy-

toplasm with round, dark nu-

clei.22 The presence of necrosis,

increased mitotic rate, and spind-

ling of the cells is suggestive of

aggressive behavior.23 Histologi-

cally benign granular cell tumors

have been retrospectively diag-

nosed as malignant upon meta-

static spread to regional lymph

nodes, lung, liver, or bone.24,25

Treatment is complete excision.

If incompletely excised, this

tumor has a high local recurrence

rate due to the plexiform or

perineurial growth pattern. The

large size of the lesion and rapid

growth were indications for MMS

in Patient 3.10

Pilomatrixoma

Pilomatrixomas are benign tu-

mors originating from follicular

matrical cells. They present as a

superficial, firm, solitary, skin-

colored to faint blue nodule or

cyst most commonly in the head

and neck region or the upper

trunk.26–29 Pilomatrixomas are

most often seen in childhood, but

can occur at any age. Microscopic

examination shows sharply de-

marcated dermal nodules encap-

sulated by compressed fibrous

tissue located in the lower dermis

and extending into the subcuta-

neous fat.26,27 Irregular islands of

epithelial cells are arranged in a

circular configuration with nucle-

ated basaloid cells on the periph-

ery and enucleated shadow cells in

Figure 8. Histology of tumor from Patient 4: (A) deep dermis with irregular islands of epithelial cells surroundedby a fibrous stroma (hematoxylin and eosin, � 2); (B) note the basophilic cells peripherally, shadow cellscentrally and focal calcification (hematoxylin and eosin, �20).

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the center. Calcification and ossi-

fication are evident mostly in

shadow cell regions. These tumors

are usually treated by surgical

excision;27 however, they may

commonly recur due to poorly

defined clinical borders and in-

complete histologic margin con-

trol. MMS may be employed to

ensure complete excision with

negative margins in a tissue spar-

ing fashion as seen with Patient 4.

Proliferating Trichilemmal

Tumor

Proliferating trichilemmal tumors

(PTT) represent a group of nodu-

lar and occasionally cystic neo-

plasms that are characterized

microscopically by abrupt kera-

tinization. These nodular tumors

in men and women equally most

commonly occur on the scalp.

They are usually well circum-

scribed with smooth borders, but

may be multinodular. The micro-

scopic pattern of proliferating pi-

lar tumors consist of a large,

sharply circumscribed nodule in

the deep reticular dermis and

subcutis or in the subcutaneous

compartment exclusively.30 Both

cystic and solid patterns are evi-

dent at low magnification, with

cystic areas exhibiting the pattern

of an isthmic (pilar) cyst. The

constituent keratinocytes are

mostly isthmic keratinocytes with

dense eosinophilic cytoplasm, and

the centers of both solid and cystic

areas display an abrupt transition

to compact keratin, usually with

little intervening granular layer.

These tumors may also exhibit

shadow cells, areas of calcifica-

tion, and/or focal necrosis. PTTs

display varying degrees of atypia.

The neoplastic cells contain en-

larged vesicular nuclei with

prominent nucleoli, some degree

of hyperchromasia, and mitotic

figures. Because some examples

of PTT may represent low-grade

forms of squamous cell carcino-

ma, tumors marked with cyto-

logic atypicality, extensive

necrosis, a lack of circumscrip-

tion, or a large number of mitotic

figures should be excised com-

pletely.31,32 MMS may be utilized

to ensure negative margins with a

tissue-sparing effect.33

Conclusion

The treatment of tumors of the

skin, whether benign or malig-

nant, is largely based on surgical

modalities. Regardless of poten-

tial histopathologic confusion and

sample errors encountered when

performing initial incisional or

punch biopsies, clinicopathologic

considerations are imperative to

the therapeutic decision-making

process. Clinical considerations

for therapeutic decision making

should include the size of the

tumor, clarity of the margins, and

location on or near cosmetically

sensitive areas.

The cases described above illus-

trate the potential for uncommon

benign tumors to behave in clin-

ically malignant patterns by ex-

panding rapidly, penetrating

widely, or invading deep struc-

tures. These features define a

more aggressive behavior pattern

despite a histopathologically be-

nign diagnosis. The cases above

illustrate the importance of com-

plete excision to prevent recur-

rence or local anatomic invasion,

distortion, or destruction. This,

combined with the often cosmet-

ically sensitive locations of these

tumors, underscores the impor-

tance of the complete margin

control and tissue-sparing benefits

of MMS. The failure to examine

100% of the margins and identify

microscopic extensions of disease

may contribute to local recurrence

following routine surgical exci-

sion.

When a disparity is encountered

in a clinically malignant appear-

ing lesion and a histologically be-

nign biopsy report is obtained, the

clinician must always consider the

possibility of biopsy sample error.

Rebiopsy of the tumor is often

recommended; however, an addi-

tional benefit of MMS includes

the complete tumor excision and

the ability to detect coexistence of

adnexal neoplasms. For example,

the association of cylindroma

with eccrine spiroadenoma is not

uncommon.

In conclusion, the use of MMS for

eradication of histologically be-

nign adenxal tumors of the skin

that grow aggressively with

poorly defined clinical margins or

those that are deeply invasive is

described. While routine surgical

excision may be used as a primary

modality for treatment of simple

tumors, the availability of micro-

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scopic frozen tissue mapping of

tumor margins is a superior tech-

nique for tumor clearance with

high success rates with tissue-

sparing results. Tissue sparing

leads to ease of reconstruction,

especially in cosmetically sensitive

areas. The treatment of aggressive

benign cutaneous neoplasms, as

described in this report by the

Mohs method, results in a defin-

itive and potentially the most

cost-effective method by which to

approach these tumors.

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Address correspondence and reprintrequests to: Leonard H. Goldberg,MD, DermSurgery Associates, 7515Main Street, Suite 240, Houston,TX 77030, or e-mail: goldb1@dermsurgery.org.

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