Epithelioma of Malherbe: New ultrasound patterns

Abstract

Calcifying epithelioma of Malherbe, or Pilomatricoma, is considered an uncommon cutaneous neoplasia, normally occurring in children as a solitary, firm, asymptomatic, hard, subcutaneous, slowly growing nodule on the face, neck, or proximal upper extremity. In literature, two Pilomatricoma ultrasound patterns are described: the totally calcified nodule and the hypoechoic nodule with internal calcific foci. High frequency ultrasound has not yet been applied for routine diagnosis of Pilomatricoma. The aim of the study was to retrospectively identify specific ultrasound features.
We retrieved 124 histologically Pilomatricoma cases: 28 patients with 32 lesions were preoperatively evaluated with ultrasound.
22/32 have shown a solid formation, hypoechoic, with a sharp outline. Of these 22, 10 lesions were completely calcifying and 12 partially calcified. In 3/32 lesions with uncertain diagnosis, ultrasounds showed a complex/mixed pattern with pseudo-fluid areas and microspots. 7/32 lesions with US different diagnosis included 3 complex lesions, 2 cystic lesions and 2 solid nodular lesions.
In addition to well-known ultrasound patterns (completely calcified and partially calcified) we identified three new, not yet described, patterns that constitute the 31% of the cases: complex, pseudocystic and pseudotumoral.

Full text

Solivetti et al. Journal of Experimental & Clinical Cancer Research 2010, 29:42
http://www.jeccr.com/content/29/1/42
Open Access
RESEARCH
BioMed Central
© 2010 Solivetti et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons
Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in
any medium, provided the original work is properly cited.
Research
Epithelioma of Malherbe: new ultrasound patterns
Francesco M Solivetti*
1
, Fulvia Elia
1
, Alessandra Drusco
1
, Chiara Panetta
2
, Ada Amantea
2
and Aldo Di Carlo
3
Abstract
Backround: Calcifying epithelioma of Malherbe, or Pilomatricoma, is considered an uncommon cutaneous neoplasia,
normally occurring in children as a solitary, firm, asymptomatic, hard, subcutaneous, slowly growing nodule on the
face, neck, or proximal upper extremity. In literature, two Pilomatricoma ultrasound patterns are described: the totally
calcified nodule and the hypoechoic nodule with internal calcific foci. High frequency ultrasound has not yet been
applied for routine diagnosis of Pilomatricoma. The aim of the study was to retrospectively identify specific ultrasound
features.
Methods: We retrieved 124 histologically Pilomatricoma cases: 28 patients with 32 lesions were preoperatively
evaluated with ultrasound.
Results: 22/32 have shown a solid formation, hypoechoic, with a sharp outline. Of these 22, 10 lesions were completely
calcifying and 12 partially calcified. In 3/32 lesions with uncertain diagnosis, ultrasounds showed a complex/mixed
pattern with pseudo-fluid areas and microspots. 7/32 lesions with US different diagnosis included 3 complex lesions, 2
cystic lesions and 2 solid nodular lesions.
Conclusion: In addition to well-known ultrasound patterns (completely calcified and partially calcified) we identified
three new, not yet described, patterns that constitute the 31% of the cases: complex, pseudocistyc and
pseudotumoral.
Background
Calcifying Epithelioma of Malherbe - or Trichomatri-
coma, Pilomatricoma, Pilomatrixoma (PM) - is an
uncommon tumour [1], with an incidence of 1/800-1000
cutaneous tumours and about 20 new reports per year
[2,3], affecting predominantly women. It is more com-
mon at a young age, especially in the first two decades of
life, with an onset below 10 years in 40% of cases [4,5].
Although multiple localizations have been described in
literature [6,7], PM occurs as a solitary lesion on the face
(47% of cases), neck [8] and upper trunk and can be asso-
ciated to other diseases, e.g. Steinert's Myotonic Dystro-
phy and Gardner Syndrome [4,7,9,10].
Recent studies have shown that recurrent activating
mutations in the ss-catenina gene (CTNNB1), induce PM
tumourigenesis through activation of the WNT signalling
pathway [11,12]. Despite the benign biological behaviour
of the majority of cases, the treatment is still surgical.
However, in recent years, aggressive cases with local post-
surgery recurrences or metastasis have been described
[2,3,13,14], accounting for variable percentage rates in lit-
erature, with 6 cases out of 228 in the Forbis series [6].
According to some authors [13], local recurrences are
related to tumour aggressiveness, while for others, these
cases are only associated with an incomplete surgical
excision [15].
The tumour presents as a slow growing subcutaneous
mass, sometimes dark on the surface, with well-defined
borders and, often, with lobulated contours at ultrasound.
The size of the tumour is usually small, less than one cm,
but, in the Darwish series, 3 out 26 had more than 2 cm
lesions and 11 out of 26 had 11 - 20 mm lesions [16].
Histologically, the lesion appears as a well defined nod-
ule, often calcified and inflamed, sometimes reproducing
a granulomatous reaction. It originates from the matrix
cells of the hair follicle, having a basaloide appearance,
composed of anucleated eosinophilic cells (shadow or
ghost cells) which are typical of trichilemmal keratiniza-
tion [17].
* Correspondence: solivetti@tiscalinet.it
1 Struttura di Radiologia e Diagnostica per Immagini, Istituto Dermosifilopatico
di Santa Maria e San Gallicano-IFO-Roma, Italy
Full list of author information is available at the end of the article

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The clinical diagnosis is often difficult: in a recent
series, most of the cases were clinically confused with
sebaceous cysts [16] and, in the Pirouzmanesh series,
only 100 out 346 (28,9%) cases were correctly diagnosed
as PM [18].
In a survey where "soft rays" were employed, data did
not discriminate among the different pathologies [19].
Although the finding of a nodular calcified lesion in chil-
dren, should address the clinical diagnosis to PM [20],
classic X-ray, ultrasound and CT scan do not allow a dif-
ferential diagnosis with dermatofibroma, epidermoid
cyst, lipoma, sebaceous calcified cyst, fibrocalcified
lymphadenitis, foreign body granuloma, chronic abscess
or organized hematoma [18,21].
Moreover, FNAB has shown a significant number of
false positives and negatives [22] and MRI is considered
inconclusive [23]: in the Lim series [20], out of 5 cases
considered, only 60% were diagnosed correctly.
Therefore, it is necessary to identify a diagnostic imag-
ing technology to assure a correct diagnostic hypothesis.
High-frequency ultrasound [24] is a very simple, reli-
able imaging technique, yet poorly reported in literature
and in numerically limited series [19]. Hughes et al. [25]
presented a cohort of 28 clinically suspected PM cases,
diagnosed employing a relatively low frequency probe (7
MHz). 20 patients underwent surgery and were evaluated
histologically: 16 were confirmed as PM, 2 were epider-
moid cysts and, in 2, it was not possible to asses any diag-
nosis. Similar data have been reported by Ulrich et al.
[26], Lim el al. [20], Hwang el al. [27] and Whittle el al.
[28]; Buchwald et al. [29] diagnosed one case of PM using
ultrasound microscopy. In the Whittle series [28], typical
PM sonographic features were characterized by a
hypoechoic small superficial nodule (between epidermis
and dermis), with not always well-defined margins, with
some calcified areas (98% of this series) of variable
appearance, formed of central or peripheral single or
grouped foci of variable shapes [24]. The lesion was
sometimes surrounded by a hypoechoic halo and some-
times perilesional Doppler flow signals were present.
So far, two different PM sonographic patterns have
been described in literature: the totally calcified nodule
and the hypoechoic nodule with internal calcified foci.
Conducting a retrospective study of our cases, the
paper aims to identify high-frequency ultrasound pat-
terns of PM that should improve clinical diagnosis.
Methods
Images of 124 patients with a histological diagnosis of PM
were retrieved from the 1996-2008 archive of the Der-
matopathology Unit of our Institute. Pre-operatory ultra-
sound images of 28/124 patients were available. In order
to avoid the comparison of two inhomogeneous groups,
we only analyzed data of these 28 patients (with 32
lesions and 5 different locations on one patient), whose
clinical records were complete.
Fourteen females and 14 males, aged between 12 and 58
years, were considered in the study. Three different
Esaote ultrasound units (Genoa, Italy) were sequentially
used during the period 1996-2008: respectively, AU4
apparatus with 20-MHz Anular Array, single crystal
probe, an AU5 apparatus, with the same probe, and,
lastly, a My Lab 70, with linear probe having a maximum
rated frequency of 18 MHz, completed of colour, power
and pulsed Doppler.
Only in two cases, with unclear ultrasonographic fea-
tures, was the study also performed with contrast
medium (Sono Vue © Bracco, Milano, Italy), employing a
multi-frequency linear probe (7-12 MHz); in all cases,
retrospectively, the images were jointly discussed by
Radiologists of our group.
Finally, data were analyzed using a statistical package
IBM SPSS, limited by an obvious lack in the numbers of
the cohort and the control group. Statistical analysis of
data was performed by means of Mc Neman's test for
binomial data to assess differences in sensitivity and spec-
ificity.
Results
We reviewed 32 high-frequency ultrasound images of 28
patients (one patient had 5 lesions). Three different ultra-
sound units have been used sequentially during the
period 1996-2008. The first two types of equipment, AU4
and AU5, which had the same probe, did not show any
relevant image quality difference. Although using a
slightly lower frequency with respect to the previous ones
(18 MHz versus 20 MHz), the third apparatus, a My
Lab70, showed a better image quality when the lesion size
was compatible to the piezoelectric crystal resolution
power.
The size of the 32 lesions ranged from 3 to 22 mm. In
particular, 2 cases exceeded 20 mm, 6 were between 10
and 20 mm and the remaining 24 were smaller than 10
mm.
Table 1: Locations of pilomatricomas
Localization No. of lesions
Head 20
Upper extremity 8
Neck 2
Wrist 1
Trunk 1

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In 20 cases, the lesions were localized on the head, 2 on
the neck, 8 on the forearm, in 1 case on the wrists and
one on the back (Table 1 - Location of pilomatricoma).
We compared each clinical ultrasonographic diagnosis
to the respective definitive histopathological response of
the lesions. 22/32 cases (69%) were correctly diagnosed as
PM, 7/32 cases (22%) were misdiagnosed and in 3/32
cases (9%), it was not possible to assess any diagnostic
hypothesis with ultrasound.
In 4 cases, vascular signals were visible with colour and
power Doppler; this feature was usually peripheral and
only rarely intra-lesional, and was observed in lesions
larger than 10 mm. The apparatus setting was that gener-
ally used for superficial lesions at low flow speed. Tumour
locations were always superficial, between the dermis and
subcutaneous tissue. Our ultrasound images, obtained
with high-frequency probes, in all correctly diagnosed
cases, showed solid, hypoechoic, and sharp rimmed
lesions: 10 were fully calcified (Fig. 1) and 12 partially cal-
cified (Fig. 2); 5 of the latter had only calcified
microspots. In 4 cases, a perilesional peripheral
hypoechoic halo was also observed.
In 3 uncertain diagnosed cases, a complex ultrasound
lesion (mixed pattern) was found, with mixed fluid and
solid areas, scattered microcalcifications, and some sig-
nals to the colour Doppler (Fig. 3). The 7 misdiagnosed
cases included 3 mixed pattern lesion, 2 cystic-like (Fig.
4) and 2 solid, vascularised nodules with irregular con-
tours (Fig. 5) (Table. 2-US findings of pilomatricomas).
Figure 6 shows a detail of the histological pattern of these
tumor.
Finally, 2 lesions, with pseudo-neoplastic features, were
also studied with a second generation contrast medium
(SonoVue, Bracco, Milan, Italy), injected via a bolus in the
antecubital vein, and showed moderate enhancement of
the lesion and the presence of rather irregular internal
vessels. The most experienced radiologist (30 years of
general ultrasound and 11 of dermatological ultrasound),
Figure 1 Pattern type 1: nodulation fully calcified, no longer evaluable.

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assessed a correct diagnosis in 11/15 cases (74%), misdi-
agnosed in 2/15 cases (13%) and provided a non conclu-
sive response in the remaining 2/15 cases (13%). There
were no significant differences (p = ns) among experi-
enced and less experienced radiologists in diagnosing
PM.
Due to the small size of the lesions and to the need for
immediate surgical treatment, none of our patients were
studied by CT scan or MRI.
Only 1 case of multiple PM (5 lesions in the same
patient) was found, and the genetic examination excluded
the coexistence of myotonic dystrophy.
Discussion
PM is an uncommon cutaneous tumour affecting young
adults, especially women. It originates from the matrix
cells of the hair follicle.
Figure 2 Pattern type 2: partially calcified nodulation, mostly sol-
id, hypoechogenic, with well defined borders, and coarse calcifi-
cations.
Figure 3 Pattern type 3: complex nodulation, with undetectable contours, with fluid and macrocalcified areas. The lesion presents well de-
fined borders. B) Histologic section at low power. The proliferation is surrounded by connectival stroma, and is edged by a basaloid epithelia with
tricholemmal and shadow cells, associated to a moderate inflammatory reaction (E-E1, 25x).
Figure 4 Pattern type 4: A)Pseuso-cystic, Lesion borders and sizes
are not well evaluable. Fluid nodule with feature similar to a thick-
ened wall cyst, extending up to the derma.

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Despite their benign behaviour, very malignant forms
have been reported in literature. So far, most of the stud-
ies have revealed the difficulties encountered in diagnos-
ing PM clinically. Imaging techniques such as X-ray, CT
scan, MRI, and FNAB have failed to differentiate PM
from other pathologies. Ultrasounds have only been of
significant use in detecting bigger lesions, and most of the
authors evaluated images obtained from low-frequency
ultrasound (7.5-10 MHz). Since the probe resolution
power is a direct proportional function of the frequency
used, a very high frequency must be employed to charac-
terize small lesions such as PM. In particular, the follow-
ing data, provided from the Esaote Research Centre of
Genoa, concerning the real experimental resolution
power of their manufactured ultrasonographic probes:
7.5 MHz linear probe: axial resolution 0.2, lateral resolu-
tion 0.25; 10 MHz linear probe: axial resolution 0.154, lat-
eral 0.187; 13 MHz linear probe: axial resolution 0.188,
lateral resolution 0.144; 18 MHz linear probe: axial reso-
lution 0.085, lateral resolution 0.104; 20 MHz annular
array: axial resolution 0.077, lateral resolution 0.094.
In our study, we have reviewed 32 series of images
obtained from high-frequency ultrasound units and have
found 5 sonographic patterns to differentiate PM from
other subcutaneous tumours. In particular, Type 1 and 2
of our classification correspond to the two typical
hypoechoic solid nodules, fully calcified and partially cal-
cified respectively, already described in literature. These
lesions normally present a hypoechoic peripheral rim in a
significant number of cases, and rarely, vascular signals
with colour Doppler.
In our series, 22 lesions exhibited the solid and calcified
patterns of type 1 (10 cases) and 2 (12 cases), and diagno-
sis was confirmed at histopathology.
Eight cases (25%) of our series showed internal fluid
areas with a thick-wall: 6 complex lesions (type 3) and 2
pseudo-cystic (type 4). Type 4 fluid areas were larger than
type 3 and showed a good transmission of the ultrasound
wave, without enhancement of the posterior wall. Histo-
logically, the pseudo-cystic lesions showed huge groups
of ghost cells, without stroma, clearly correlated to the
sonographic features.
Lim et al. [20] described 2 cases out of 17 with little
endotumoural liquid-like areas, which the author, and,
more recently, Choo et al. [30], considered to be related
to degenerative phenomena. We are the first to report the
occurrence of real ultrasonographic cystic areas in PM.
As pointed out by some dermatopathologists [31], the
tumour originates from a cystic formation of the follicle
matrix, with more or less thick walls, depending on the
neoplasia evolvement, and with consequential formation
of an internal mass of shadow cells, with low vascularisa-
tion and almost absent stroma. Generally, calcifications
and signs of inflammation appear belatedly.
The homogeneity of pseudo-cystic fluid areas, the lack
of internal interfaces and of fibrous support structures,
the absence of internal signs with colour Doppler, but
without enhancement of the posterior wall, might
address the operator to an erroneous diagnosis. The
resemblance of sonographic features to so-called seba-
ceous cysts (epidermal or trichilemmal cysts), might
result from the very high frequency probes that we first
used in this particular type of dermopathology. Two
cases, with a tumour-like pattern (type 5), were indistin-
guishable from an aggressive neoplasia of the superficial
structures; in both patients, the lesions were significantly
old and, histologically, displayed chronic flogistic phe-
nomena and fibrosis.
Conclusion
Based on the above, some remarks can be drawn:
Figure 5 Pattern type 5: Pseudo-neoplastic, solid nodulation, hy-
poechogenic, not homogeneous, with irregular anterior contours,
with signal with Colour and Power-Doppler.
Figure 6 Shadow cell and thricholemmal keratinization details,
interspersed inflammatory cells (E-E 20×).

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1 -Using very high frequency probes, we have identified
five different ultrasound patterns of PM. Pattern type 3, 4
and 5 have never been described before, not even in the
recent paper of Choo et al. [30].
This finding constitutes a new important contribution
that deserves to be promptly shared with other specialists
working in the field:
• type 1, 31.5% of cases; nodule fully calcified, semi-
superficial with minimal solid hypoechoic peripheral
ring, with an average size of 11 mm (Fig. 1);
• type 2, 37.5% of cases; nodule partially calcified, with
internal calcareous formations, of variable size (average
diameter of 10 mm), with a solid hypoechoic peripheral
component, avascular (Fig. 2);
• type 3, complex formation; 19% of cases (Fig. 3);
• type 4, 6% of cases; pseudocystic formation, without
enhancement of the posterior wall, with semi thick walls
(Fig. 4)
• type 5, 6% of cases; pseudo-neoplastic nodules; the
inflammatory phenomena seemed to justify the pattern
(Fig. 5).
2-As described in literature, the diagnostic accuracy of
an experienced operator is very high for "classic" forms,
but it is lower for the three new patterns.
3-There were no differences in the evaluation of the
features of the images among less experienced and expert
radiologists. This evidence could be explained by the rel-
atively high incidence of lesions with non-classical pat-
terns encountered in our series.
4-We used higher resolution apparatus, that certainly
permitted good performances in the diagnosis of the
"classic" forms, but showed better results in discriminat-
ing the peculiar characteristics of pattern 3, 4 and 5.
However, more cases would be needed to evaluate the
real incidence of those new patterns.
5-Although our results showed only 69% of correct
diagnosis compared to 96% (50/52) of Whittle et al. [28]
and 82% of Lim et al. [20] (17/18), we reached 100% when
considering only the "classic" forms (pattern 1 and 2),
which are really easily diagnosable with ultrasounds.
6-In agreement with Choo et al. [30], and for the few
cases we studied, the colour-power Doppler and the sec-
ond generation contrast media did not seem to give sig-
nificant diagnostic advantages. In conclusion, we believe,
that the knowledge of these three new patterns, not pre-
viously described, could help in the clinical diagnosis of
pilomatricoma, and, consequently, in the diagnostic and
therapeutic management of this type of neoplasia.
Competing interests
The authors declare that they have no competing interests.
Authors' contributions
FE and AD carried out the research, participated in the sequence alignment
and drafted the manuscript text. CP and AA assessed the pathological diagno-
sis. ADC contributed with his professional experience to the revision of the
manuscript. FMS conceived the study, participated in its design, carried out the
research and coordinated the study. All authors read and approved the final
manuscript.
Author Details
1Struttura di Radiologia e Diagnostica per Immagini, Istituto Dermosifilopatico
di Santa Maria e San Gallicano-IFO-Roma, Italy, 2Struttura di Dermopatologia,
Istituto Dermosifilopatico di Santa Maria e San Gallicano-IFO-Roma, Italy and
3Direttore Scientifico, Istituto Dermosifilopatico di Santa Maria e San Gallicano -
IFO-Roma, Italy
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This article is available from: http://www.jeccr.com/content/29/1/42© 2010 Solivetti et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.Journal of Experiment al & Clini cal Cance r Research 2010, 29:42
Table 2: US findings of pilomatricomas
Type US features No. of lesions
Type 1 Fully calcified 10
Type 2 Partially calcified 12
Type 3 Complex lesion 6
Type 4 Pseudocystic lesion 2
Type 5 Pseudotumoural 2

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Cite this article as: Solivetti et al., Epithelioma of Malherbe: new ultrasound
patterns Journal of Experimental & Clinical Cancer Research 2010, 29:42