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Chondrosarcomas arising from soft tissues are rare. Two different varieties are described, myxoid and mesenchymal. We have collected nine cases of the ...
CHONDROSARCOMA

OF

TWO

R.

CASADEI,

M.

RICCI,

P.

DIFFERENT

RUGGIERI,

From

THE

R.

Rizzoli

of chondrosarcoma

and histological Extraskeleta!

seen

differences

between

BIAGINI,

S.

Orthopaedic

chondrosarcomas

are

between

1904

less

common

than those in bone. Tumours arising from the soft tissues are not attached to bone, periosteum or cartilage (Stout and Verner 1953 ; Go!denberg, Cohen and Steinlauf 1967; Amir et a! 1985). They can be divided into two histological varieties : myxoid and mesenchymal. The aim

of this

paper

is to define

PATIENTS

these

AND

two

entities.

METHODS

At the Bone Tumour Centre of Bologna, 5 1 3 cases ofchondrosarcoma 1904 and 1988 and have been

the

radiographical!y and histologically. was the diagnosis of soft-tissue firmed (1 7%). Of these, five were

Only in nine patients chondrosarcoma conmyxoid and four were

BENASSI,

Institute,

P.

PICCI,

M.

CAMPANACCI

Bologna

Two different varieties are described, five myxoid and four mesenchymal,

and 1988.

the two varieties

much

TISSUES

SUB-GROUPS

Chondrosarcomas arising from soft tissues are rare. mesenchymal. We have collected nine cases of the tumour, of 513 cases

SOFT

We report

and discuss

their

Clinical

findings.

the principal surgical

clinical,

treatment

Clinical

myxoid and from a review radiographical

and prognosis.

details

are

reported

in Table

toms.

ranged

from

months (average, 12 months : 1 7 for mesenchyma! chondrosarcoma). Imaging. In myxoid chondrosarcoma were normal (case 3) or showed only

The

duration

of symptoms

myxoid,

three

to 24

nine

Rizzoli Institute, were seen between reviewed clinically,

Correspondence

©

should

be sent

Centre,

and Via

Head Di

of the

Barbiano Fig.

1

to Dr P. Picci.

1991 British Editorial Society ofBone 0301-620X/91/l059 $2.00 JBoneJoint Surg[Br] 1991 ; 73-B:162-8.

162

of Bologna

and

Joint

Surgery

2. Plain radiograph sarcoma shows a roundish mass with some stippled the deltoid. Case

THE

JOURNAL

ofa myxoid chondroslightly radiopaque calcification within

OF BONE

for

the radiographs a soft-tissue mass

mesenchymal.

R. Casadei, MD, Fellow First Orthopaedic Clinic M. Ricci, MD, Fellow Bone Tumour Centre P. Ruggieri, MD, Orthopaedic Surgeon First Orthopaedic Clinic R. Biagini, MD, Orthopaedic Surgeon First Orthopaedic Clinic S. Benassi, ScD, Biologist Bone Tumour Centre P. Picci, MD, Oncologist Bone Tumour Centre M. Campanacci, MD, Director First Orthopaedic Clinic of the University Bone Tumour Centre Istituto Ortopedico Rizzoli, Bone Tumour 1/10, Bologna, 40136, Italy.

I

for the seven women and two men aged 32 to 62 years. Eight tumours were in a lower limb and only one in an upper limb. Pain and tenderness were the main symp-

AND

JOINT

SURGERY

CHONDROSARCOMA Table

I. Clinical

Age(yr) and sex

Case Myxoid 1

details

of nine

patients

Site

chondrosarcoma 62 F

IA

Vastus lateralis Triceps

IA

32 F

3

45

4

48

F

5

46

M

Mesenchyma/ 6

chondrosarcoma 28 F Leg

F

with

Stage

Vastus medialis Deltoid

2

OF THE SOFT soft-tissue

Wide excision Wide excision Wide excision Marginal

lB

surae

163

chondrosarcoma Time to metastasis (mth)

Treatment

IA

TISSUES

Follow-up (mdi)

-

19

-

36

-

60

-

108

-

132

excision*

Vastus medialis

IA

Marginal excisionS

IIB

Marginal

Result

Tumour free Tumour free Tumour free Tumour freet Tumour freet

21

33

Died

0

13

Has metastases

6

48

Died

15

87

Died

excision*

7

37 F

Buttock

IIIB

8

55

Leg

IIB

9

27 F

Buttock

IIB

Hindquarter amputation (wide)

* local

M

:see text

recurrence

t free of tumour

Marginal excision Chemotherapy Marginal excision

for details

after excision

oflocal

with no distinctive features (cases 1, 4 and patient (case 2) minute stippled calcifications

recurrence

5). In one were seen

CT scans were performed in six cases, showing a soft-tissue mass in the patient with normal radiographs and contributing to pre-operative staging by demonstrating different densities of tumour and surrounding soft

(Fig. 1). In mesenchyma!

chondrosarcoma

radiographic finding irregular calcifications the lesion

was

cobweb-like

the

most

ill-defined, calcification

with

blurred

(Fig.

3).

margins

Fig.

Case

73-B,

No.

1, JANUARY

1991

and

thin,

7

tissue and the relationship bundles. Usually the tumour but in two with bone,

patients without

showcalcifica-

to bone and was distant

(cases 6 and any erosion

Fig.

2

6. Mesenchymal chondrosarcoma ing a large ovoid mass with irregular tion between tibia and fibula.

VOL.

frequent

was an ovoid mass, with numerous (cases 6, 8 and 9, Fig. 2). In case

7) the mass was in contact or penetration (Fig. 4).

3

Case 7. Mesenchymal chondrosarcoma buttock showing net-like calcification a mass with ill-defined margins.

neurovascu!ar from the bone

of the within

R. CASADEI,

164

Bone-seeking

isotope

M. RICCI,

scans,

P. RUGGIERI.

available

showed uptake in all patients. activity within the lesions showing two cases where tumour extended

in seven

R. BIAGINI,

S. BENASSI,

P. P1CC!,

M. CAMPANACCI

cases,

There was increased calcification. In the to the periosteum,

isotope scans also showed a reactive uptake in the adjacent bone. Gross findings. The five cases of myxoid chondrosarcoma presented as ovoid, soft, nodular masses, well circumscribed by a distinct pseudocapsule. On section the surface appeared translucent, gelatinous, and grey to brown in colour with large haemorrhagic and sometimes necrotic areas. The size of the tumours ranged from 5 to 8cm. The mesenchymal chondrosarcomas, were multilobulated and circumscribed, firm in consistency with no well-defined pseudocapsule. Cut sections of specimens showed

a

pale

cartilaginous necrosis were

grey,

fleshy

surface

with

foci, which creaked on cutting. abundant while haemorrhagic

Fig.

scattered

4

CT scan of Case 6 (Fig. 2) shows a partially mass in contact with the bone without penetrating

Areas of zones were

sometimes eosinophi!ic In case

tive tissue capsule, which had resulted from the expansile growth of the tumour. Fibrous septae of variable thickness with a few small blood vessels extended in from

scanty myxoid ground substance. Anaplasia and pleomorphism were rare and mitotic figures were absent. We observed no differentiated chondrocytes within distinct lacunae. Mucoid material was abundant in three patients

narrow vacuolated chromatic

rim

round of

by variable was weakly

deeply

cytoplasm nucleus.

fine anastomosing tumour a lace-like

Within the or slightly

eosinophilic around

Typically strands appearance.

amounts basophilic

lobules, elongated. the

the and

the and

small, cells

cells There

and in two, the typical texture ofmyxoid was disturbed by large haemorrhagic

sometimes ovoid,

were

were was a

arranged

and occasional haphazardly argyrophilic

hyperin

small nests giving the These cells were separated

of mucoid ground with haematoxy!in

stain was of glycogen

substance which and eosin, but

chondrosarcoma

#{149}1

a

probably

homogeneous or whorls

with

chondrosarcoma and necrotic areas

calcification. Silver stains arranged reticulin fibres and material within the myxoid

always positive, in the cytoplasm.

Mesenchymal

of

it.

scanty. The tumour size ranged from 10 to 20 cm. Histological findings. Myxoid chondrosarcomas were multilobular and well circumscribed by a condensed connec-

the pseudocapsu!e. small, uniform,

contained small droplets material (Fig. 5). 2 there were cells in clusters

calcified

due showed

showed a few some granular matrix. PAS to the

presence

a characteris-

Case 2. Myxoid chondrosarcoma (Fig. 1) showing the characteristic alignment of tumour cells in strands and cords separated by large amounts of myxoid material. The vacuoles within the myxoid ground substance are extracellular and should not be confused with lipoblasts. Note the absence ofvessels (haematoxylin and eosin, x 200).

a

T*

Fig. 5

THE

JOURNAL

OF BONE

AND

JOINT

SURGERY

CHONDROSARCOMA

tic pattern oftwo basic round or spindle-shaped differentiated mesenchyma! of

cellular cells

tumour component

elements : undifferentiated and small nodules of well-

cartilage. showed

haemangiopericytoma

OF THE

(Fig.

7 showed

plasm. figures

nuclei

In all cases and dilated

Cartilaginous abundant

and

scanty,

poorly

outlined

there were numerous vascular clefts. foci

in only

were

two.

present

These

in

nodules

a

mitotic

a!!

tumours,

were

well

there were negative.

pattern

of

large Silver

reticu!in

undifferentiated

necrotic stains fibres

cells

and

zones. showed around

but defined

groups

of

vessels.

cases

of myxoid

chondrosarcoma

were

treated

by

wide excision. Al! these patients are alive and free of tumour after an average of 38 months (19 to 60). In case 4 a marginal excision had been performed elsewhere and at

12 months

a local

required amputation. free at nine years. The fifth patient with the diagnosis developed

a local

recurrence This

in the

patient

had a marginal of ‘myxoma’ recurrence

;

biopsy

popliteal

is alive excision and five then

and

fossa disease-

elsewhere, years later provided

the

again excised our care with

free

of tumour

No. 1, JANUARY

1991

marginally. a further

Of the four one

was

treated

surgical region, anterior there

A marginal therapy.

at 1 1 years from

margin. attached

the

a wide

In 1986 large local

the patient recurrence

vessels. A wide bypass. The

excision surgical

from

excision was performed, The patient is alive and the

first

operation

and

at

last.

cases of mesenchymal chondrosarcoma, by hindquarter amputation with a wide This patient to the iliac

portion of the thigh. was a single pulmonary

had a mass wing and At

in the g!utea! involving the

the time metastasis.

of diagnosis, This was

excised. Ten months later multiple pulmonary metastases developed ; the patient was treated with chemotherapy and radiotherapy. He is still alive at 1 3 months.

margins in two

other

three had

patients conservative

with mesenchyma! surgery. The

were ‘marginal’ and a local cases at three and 12 months

recurrence respectively.

chonsurgical developed In case

6 radiation

therapy was used in an unsuccessful attempt to control the local recurrence ; finally an amputation was performed. In case 9 the recurrence was adherent to the periosteum of the iliac wing without involvement of the bone : wide excision with a partial resection of the iliac wing

was

developed involvement

performed.

In

these

in lung, liver and of supraclavicu!ar

Fig.

73-B,

and

However, the excision was in 1984 a further recurrence

the femora! an arterial

Case 6. Mesenchymal chondrosarcoma (Fig. 2) showing, on the left, areas of welldifferentiated cartilage surrounded by undifferentiated cells in a highly cellular arrangement ; on the right, an alveolar and haemangiopericytoma-like pattern (haematoxylin and eosin, x 50).

VOL.

chondrosarcoma

margins of this specimen were confirmed to be wide, but three years later a further small recurrence developed

The drosarcoma

TREATMENT Three

of myxoid recommended. marginal and

in the thigh involving was attempted with

six months

PAS stain was a well-defined small

was than

close to the bypass. followed by radiation

in two cases while in another two they had ill-defined margins that blended with the mesenchymal areas. In three cases they followed lobules of!ow-grade malignancy (grade 1 to 2). Haemorrhagic areas were rare but in three cases always

165

diagnosis

developed, came under

cyto-

atypical

TISSUES

excision no more

many

areas ofdense cellularity reminiscent ofEwing’s sarcoma, and in case 6 there were round cells arranged like lymphoma. Mesenchyma! cells had ovoid or elongated hyperchromatic

correct

In cases 8 and 9, the the histological pattern 6). Case

SOFT

6

three bone

and lymph

cases

metastases

case 6 also had nodes. These

166

R. CASADEI,

patients

died

at

Chemotherapy when metastases

33,

has been appeared

M. RICCI,

48,

87

P. RUGGIERI,

months

used only in one in bone.

R. BIAGINI,

from

surgery.

patient

(case

Enneking 8)

is a quite a pre-existing

rare tumour chondroma

of the soft tissues (Enzinger and Weiss 1983). Recently Enzinger and Shiraki (1972), Hajdu (1979) and Campanacci, Bertoni and Bacchini (1981) have distinguished two typical sub-groups. Clinical findings. Myxoid chondrosarcoma occurs more frequently in lower limbs, deep to the fascia in muscular compartments ger and Weiss

(stage 1983).

A) (Campanacci Mesenchymal

arise in any mesenchymal Hajdu 1979), sometimes in and Garret 1963). When it usually arises in the soft tissues (stage B, Enneking

tissue (Guccion et a! 1973; an irradiated area (Brenner is found in the extremities, it areo!ar extracompartmental 1983). Myxoid chondrosar-

coma occurs more frequently (Uehara and Becker 1960; Angerva!l, Enerb#{228}ck and Ferenczy

1978

et a! 1981 ; Enzinchondrosarcoma may

in adult Enzinger Knutson

; Campanacci

and elderly males and Shiraki 1972; 1973 ; Mehio and

et a! 198 1 ; Amir

et a! 1985)

although in our series we observed a 4 to 1 female to male ratio. The mesenchyma! variety occurs more often in young adult females (Salvador, Beabout and Dahlin 1971 ; Guccion et a! 1973; Campanacci et a! 1981; Enzinger Pain

and and

Weiss 1983; Nakashima tenderness are the most

observed

in both

types

et a! 1986). frequent symptoms

of extraskeletal

chondrosarcoma

(Salvador et al 1971 ; Campanacci et a! 1981 ; Enzinger and Weiss 1983; Amir et a! 1985). In our patients the average duration of complaints was 1 7 months in myxoid and nine months in mesenchymal chondrosarcoma. Imaging. A well-defined soft-tissue neoplasm, often speckled with calcification, is more indicative of a mesenchyma! than a myxoid chondrosarcoma because in this second type there is no intratumora! calcification or only and

minor Shiraki

stippling 1972;

(Uehara Campanacci

1985). In mesenchymal floccules are different pattern typical (Campanacci

Becker 1960 ; Enzinger et a! 1981 ; Amir et a!

chondrosarcoma from the granular

the flecks and or ‘popcorn’

of the osseous type of chondrosarcoma et a! 1981 ; Bertoni et a! 1983; Enneking

1983). In myxoid chondrosarcoma radiographic features does diagnosis et a! 198!

and

from other Enzinger

;

not

soft-tissues and Weiss

the lack of distinctive allow a differential

sarcomas 1983).

(Campanacci

Intrinsic radiopacities may suggest lesions which contain amorphous calcification, either benign tumours, such as angioma, synovial chondromatosis, or chondroma (Goldenberg

et

al

1967;

Wi!ner

1982),

or

as

tumoral

ca!cinosis or soft-tissue calcification in secondary hyperparathyroidism (Bertoni et a! 1983), or malignant as in extraskeletal fibrosarcoma (Goldenberg et a! 1967;

P. PICCI,

1983),

M. CAMPANACCI

extraskeleta!

al 1983), or synovial Enzinger and Shiraki 1983; Enneking 1983; Isotope

DISCUSSION Extraskeleta! chondrosarcoma arising ‘de novo’, and not from

S. BENASSI,

scans

osteosarcoma

(Bertoni

et

sarcoma (Go!denberg et a! 1967; 1972; Wilner 1982; Bertoni et a! Nakashima et a! 1986).

show

uptake

in both

types

of tumour

but is more pronounced coma, sometimes with

in mesenchymal increased activity

chondrosarin the adjacent

bone because the tumour In myxoid chondrosarcoma

was extended angiography

to the periosteum. delineates the

mass

and

the reaction

in the surrounding

soft

tissues

and

shows the relationship neurovascular bundles. strongly because the comparison with its (Enneking 1983). In ma! chondrosarcoma

of the tumour with the adjacent The tumour itself does not inject interior of the mass is avascular in peripheral reactive vascularisation contrast, angiography in mesenchyshows a hypervascu!arisation of the

neoplasm

broadened

with

many

capillaries

(Campanacci

eta!

1981). CT scans are necessary for surgical planning demonstrate differences in density in comparison the adjacent soft tissues and with other soft sarcomas (Enneking very low fluid density whereas density

they with tissue ;

1983). The myxoid variety has due to the richly mucinous material,

mesenchymal due to calcification.

chondrosarcoma Only in a few

shows reported

a

a high cases

is there evidence of erosion of the adjacent bone (Stout and Verner 1953; Go!denberg et a! 1967; Steiner, Mirra and Bullough 1973; Amir et a! 1985). Differential diagnosis. Myxoid chondrosarcoma may be mistaken

for

other

myxoid liposarcoma, liposarcoma has

richly

mucinous

myxoma a plexiform

tumours

such

and chordoma. vascular pattern,

as

Myxoid many

lipoblasts and no stainable mucin after previous treatment of the sections with hya!uronidase (Campanacci et al 1981). Histologically, chordoma is very similar to myxoid chondrosarcoma because it also contains mucoid material with the same staining characteristics. However, the usual site (skull, spine and sacrum) and the presence of physaliferous cells, are useful for the differential diagnosis (Mehio and Ferenczy 1978). A myxoma can also be confused with a myxoid chondrosarcoma, but it has more scattered and less defined cells not arranged in cords, and the mucoid material has the same staining characteristics Shiraki

as

1972; Hajdu The differential

sarcoma sarcoma,

myxoid

!iposarcoma

is made from haemangiopericytoma, !ymphoma, rhabdomyosarcoma,

coma, and high-grade liposarcoma. drosarcoma may often be haemangiopericytoma because of pattern (Goldman 1967; Salvador et a! 1973; Campanacci et a! 1981 ; Enzinger

(Enzinger

and

Weiss

1983;

differs in its well-defined poor intercellular reticulum. (Steiner et a! 1973 ; Fu THE

and

1979; Campanacci et a! 1981). diagnosis of mesenchymal chondro-

Nakashima cartilaginous Electron and Kay

JOURNAL

OF BONE

Ewing’s synovial sar-

Mesenchymal chonmistaken for a its similar cellular a! 1971 ; Guccion et Bertoni et a! 1983; et a! 1986), islands microscope 1974) show AND

JOINT

but

it

and the studies that in SURGERY

CHONDROSARCOMA Table tissues

II.

Differences

between

OF THE the two

SOFT

sub-groups

Small

mass

Large

Radiograph

Little

or no calcification

Irregular

CT scan

Low homogenous

Bone

Faint

Histology

Strands and cords round cells within amount of mucoid

Local

Radiotherapy

mesenchymal cells and islets of well-differentiated cartilage with central calcification Quick invasive growth

Probably

Useless

Metastases

Rare

and

Prognosis

Good

vascular

cells have the

hypervascularity

Radical excision amputation

after

the

density uptake

Undifferentiated

of large matrix

growth

Rare

undifferentiated ; they do not

calcification

Diffuse

Wide

recurrence

chondrosarcoma

the result of vascular spaces

High

Hypervascular margin Avascular centre

mass

Irregular

uptake

Slow

mesenchymal

density

Angiography

Chemo/

soft

35

scan

167

ofchondrosarcoma

Myxoid

(yr)

Age

TISSUES

wide

excision

small

or

useful

Frequent

late

Common

and

early

Bad

features

are

growing around characteristics of

often be treated by limb salvage surgery. of extraskeleta! chondrosarcoma often putation (Salvador et a! 1971 ; Enneking

Local recurrence requires an am1983).

pericytes. Other malignant round cell tumours lack the foci of cartilaginous differentiation (Salvador et a! 1971; Steiner et a! 1973 ; Bertoni et a! 1983 ; Nakashima et a! 1986). An alveolar and haemangiopericytoma-like texture may also be observed in synovial sarcoma, but there

There are no definitive data about the role of chemotherapy or radiotherapy in addition to an adequate surgical excision. Campanacci et al (1981), Bertoni et a! (1983), and Enzinger and Weiss (1983) suggest the use of

is often appearance

In myxoid chondrosarcoma the rate of metastasis is lower (20%, Enzinger and Shiraki 1972) than in the mesenchymal variety (50%, Salvador et al 1971). We found a more striking difference : no metastasis compared

a

biphasic pattern, and proliferating

with a pseudoglandular spindle-shaped cells (Gold-

man 1967 ; Guccion et a! 1973 ; Enzinger and Bertoni et a! 1983 ; Nakashima et a! 1986). Treatment and prognosis. Staging studies omitted lesional

and tumours are excision (Salvador

treated by marginal et a! 1971 ; Smith

adjuvant

therapy

Weiss

1983;

are

often

with

100%

or intraet a! 1976;

we!!

localised,

Enneking 1983 ; Amir et a! 1985). The reported rate of local recurrence and metastasis, therefore, varies from 20% to 60% in soft-tissue chondrosarcomas (Stout and Verner 1953 ; Kauffman and Stout 1963 ; Goldenberg et

in mesenchymal

respectively. the

When patient

may

chondrosarcoma.

a metastasis be treated

is unique

and

by pulmonary

lobectomy or local excision, because of the slow growth ofthe tumour cells (Wu et a! 1980). The patients must be followed up for a long time to evaluate correctly the survival and recovery, because coma may develop a recurrence after surgical al 1981).

percentage

coma of bone is equally aggressive (31% of recurrences) as myxoid chondrosarcoma of soft tissue (40% of recurrences) but has a worse prognosis (39% of metastases as against no metastases). According to Enzinger and

coma series)

of recurrence

either

(30%, Enzinger and or in the mesenchymal

a! 1971 ; 40%, Wide surgical myxoid sub-type acci et al 1981),

Guccion resection

in myxoid

chondrosar-

Shiraki 1972 ; 100%, in our variety (33%, Salvador et

et al 1973 ; 66%, in our is the treatment of choice

(Enzinger whereas

series). for the

and Shiraki 1972 ; Campanfor the mesenchymal variety

radical excision is preferable (Salvador et a! 1971; Campanacci et a! 1981 ; Bertoni et a! 1983 ; Enneking 1983 ; Enzinger and Weiss 1983 ; Nakashima et al 1986), because the tumour is frequently extracompartmenta!. For this reason, mesenchymal chondrosarcomas cannot VOL.

73-B, No.

1, JANUARY

1991

a

From

(Wu

et a! 1980;

chondrosarmany years

a! 1967 ; Guccion et a! 1973 ; Wu, Collon and Guise 1980). In our series it occurred in 44% and was closely related to tissue margins at the first surgical treatment. A marginal or intralesiona! excision has a high

tumour

treatment

soft-tissue or metastasis

a study of all chondrosarcomas centre (Mercuri et a! 1988) central

Campanacci

et

treated in our chondrosar-

Shiraki (1972), Smith et a! (1976), and Amir et al (1985), mesenchymal chondrosarcoma has a higher malignancy when it is localised in soft tissues : 14% recurrence and 7 1% metastasis in mesenchyma! chondrosarcoma of bone as against 50% and 100% in the soft-tissue type. In our series, mesenchymal chondrosarcoma has a worse prognosis than both the myxoid variety and osseous chondrosarcomas.

168

R. CASADEI,

M. RICCI,

Chondrosarcoma logically well defined

of soft tissues and distinct

chondrosarcoma (Table II). They

mesenchymal in both clinical

features

and

and differ

P. RUGGIERI,

includes sub-types,

two

R. BIAGINI,

histomyxoid

chondrosarcoma and radiographic

in prognosis.

special project ‘Oncology’ was supported by grant number 124.44 from the Italian National Council of Research. No benefits in any form have been received or will be received from a commercial party related directly or indirectly to the subject of this article.

Hajdu

Angervall origin. Bertoni bone

L, Enerb#{228}ck L, Knutson Cancer 1973; 32:507-13.

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M, Bertoni Vol 3. Bologna:

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KK, Colon Joint Surg

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