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.
References
1. Shriner DL Jr, McCoy DK, Goldberg DJ,
Wagner RF. Mohs micrographic sur-
gery. J Am Acad Dermatol 1998;39:
79–97.
2. Hruza GJ. Mohs micrographic surgery.
Otolaryngol Clin North Am 1990;23:
845–64.
3. Bieley HC, Kirsner RS, Reyes BA, Gar-
land LD. The use of Mohs micrographic
surgery for determination of residual
tumor in incompletely excised basal cell
carcinoma. J Am Acad Dermatol
1992;26:754–6.
4. Lambert DR, Siegle RJ. Skin cancer: a
review with consideration of treatment
options including Mohs micrographic
surgery. Ohio Med 1990;86:745–7.
5. Goldberg DJ, Schwartz RA. Basal cell
carcinoma: cosmetic mutilation follow-
ing incomplete excision. Can J Dermatol
1991;3:168–9.
6. Breuninger H, Dietz K. Prediction of
subclinical tumor infiltration in basal cell
carcinoma. J Dermatol Surg Oncol
1991;17:574–8.
7. Lang PG Jr, Osguthorpe JD. Indications
and limitations of Mohs micrographic
surgery. Dermatol Clin 1989;7:
627–44.
8. Calhoun KH, Wagner RF. Multidiscipli-
nary treatment of facial skin cancer. Tex
Med 1991;87:64–9.
9. Bricca GM, Brodland DG, Ren D, Zitelli
JA. Cutaneous head and neck melanoma
treated with Mohs micrographic surgery.
J Am Acad Dermatol 2005;52:92–100.
10. Chilukuri S, Peterson SR, Goldberg LH.
Granular cell tumor of the heel treated
with Mohs technique. 2004;30:1046–9.
11. Kimyai-Asadi A, Goldberg LH, Jih MH.
Accuracy of serial transverse cross-sec-
tions in detecting residual basal cell
carcinoma at the surgical margins of an
elliptical excision specimen. J Am Acad
Dermatol 2005;53:469–74.
12. Nerad JA, Folberg R. Multiple cylindro-
mas. The ‘‘turban tumor’’. Arch Op-
hthalmol 1987;105:1137.
13. Koay JL, Ledbetter LS, Page RN, Hsu S.
Asymptomatic annular plaque of the
chin: desmoplastic trichoepithelioma.
Arch Dermatol 2002;138:1091–6.
14. Brownstein MH, Shapiro L. Desmoplas-
tic trichoepithelioma. Cancer 1977;40:
2979–86.
15. Sajben FP, Ross EV. The use of the
1.0 mm handpiece in high energy, pulsed
CO2 laser destruction of facial adnexal
tumors. Dermatol Surg 1999;25:41–4.
16. Shaffelburg M, Miller R. Treatment of
multiple trichoepithelioma with electro-
surgery. Dermatol Surg 1998;24:1154–6.
17. Finkelstein MS, Klaus MV. Granular cell
tumor of the heel. J Am Podiatr Med
Assoc 1990;80:608–10.
18. Guenther L, Shum D. Granular cell
tumor of the vulva. Pediatr Dermatol
1993;10:153–5.
19. Mentzel T, Wadden C, Fletcher CD.
Granular cell change in smooth muscle
tumors of skin and soft tissue. Histopa-
thology 1994;24:223–31.
20. Fanburg-Smith JC, Meis-Kindblom JM,
Fante R, Kindblom LG. Malignant gran-
ular cell tumor of soft tissue: diagnostic
criteria and clinicopathologic correlation.
Am J Surg Pathol 1998;22:779–94.
21. Paskin DL, Hull JD, Cookson PJ. Gran-
ular cell myoblastoma: a comprehensive
review of 15 years experience. Ann Surg
1972;175:501–4.
22. Usui M, Ishii S, Yamawaki S, et al. Ma-
lignant granular cell tumor of the radial
nerve: an autopsy observation with elec-
tron microscopic and tissue culture stu-
dies. Cancer 1977;39:1547–55.
23. Lan MY, Lan MC, Ho CY, et al. Pi-
lomatricoma of the head and neck: a
retrospective review of 179 cases. Arch
Otolaryngol Head Neck Surg
2003;129:1327–30.
24. Pirouzmanesh A, Reinisch JF, Gonzalez-
Gomez I, et al. Pilomatrixoma: a review
of 346 cases. Plast Reconstr Surg
2003;7:1784–9.
25. Punia RP, Palta A, Kanwar AJ, et al. Pi-
lomatricomaFa retrospective analysis of
18 cases. Indian J Pathol Microbiol
2001;44:321–4.
26. Danielson-Cohen A, Lin SJ, Hughes CA,
et al. Head and neck pilomatrixoma in
children. Arch Otolaryngol Head Neck
Surg 2001;127:1481–3.
27. Brownstein MH, Arluk DJ. Proliferating
trichilemmal cyst: a simulant of squa-
mous cell carcinoma. Cancer
1981;48:1207–14.
28. Sethi S, Singh UR. Proliferating tricho-
lemmal cyst: a simulant of squamous cell
carcinoma. Cancer 1981;48:1207–14.
29. Lopez-Rios F, Rodriguez-Peralto JL,
Aguilar A, et al. Proliferating trichilem-
mal cyst with focal invasion: report of a
case and a review of the lite-
rature. Am J Dermatopathol 2000;22:
183–7.
30. Tierney E, Ochoa MT, Rudkin G, So-
riano TT. Mohs’ micrographic surgery of
a proliferating trichilemmal tumor in a
young black man. Dermatol Surg
2005;31:359–63.
Address correspondence and reprintrequests to: Leonard H. Goldberg,MD, DermSurgery Associates, 7515Main Street, Suite 240, Houston,TX 77030, or e-mail: [email protected].
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