942393 JFM Journal of Feline Medicine and SurgeryDobromylskyj et al

Original Article

Journal of Feline Medicine and Surgery

Prognostic factors and proposed 1­–7

© The Author(s) 2020
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DOI: 10.1177/1098612X20942393
https://doi.org/10.1177/1098612X20942393

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in cats, based on a retrospective by the European Editorial Office (ISFM)

for publication in JFMS

study

Melanie J Dobromylskyj1 , Victoria Richards2 and Ken C Smith2

Abstract
Objectives  The objectives of this study included utilising a large database from a diagnostic laboratory to identify
any breed, sex or age predilections for cutaneous and subcutaneous soft tissue sarcomas (STSs), and the most
common anatomical locations. The second aim was to obtain clinical outcomes and to assess histological features
of those tumours to identify any potentially useful prognostic indicators and propose a grading system.
Methods  Records from the laboratory were searched for feline submissions received from January 2012 to
December 2013 diagnosed with STSs; the breed, age, sex and neuter status of the cat and anatomical location
of the tumour were recorded. Clinical outcomes were acquired using a questionnaire to submitting practices, and
histological features of tumours from patients with known outcomes were assessed.
Results  No sex, neuter status or breed predispositions were found. Most STSs arise in middle-aged and older cats,
and the most common anatomical location was the trunk. Forty-seven cases had a known clinical outcome and
archived tissues allowing for histological assessment of the tumour. Significant differences in median survival time
(MST), mitotic index and histological score were detected between those cats that died of tumour-related disease
and those that did not. A novel grading system applied to these tumours produced significant differences in MST
between cats with low (MST = 900.5 days), intermediate (MST = 514 days) and high grade tumours (MST = 283
days).
Conclusions and relevance  This is the first study applying a histological grading system to these common tumours.
Local recurrence is often the cause of a poor outcome, with metastatic disease apparently rare. The proposed
grading system incorporates features that can be assessed on routine haematoxylin and eosin-stained sections; in
this small study, the histological grade of the tumour appears to be associated with survival time.

Keywords: Neoplasia; sarcoma; grade; soft tissue

Accepted: 18 June 2020

Introduction
Soft tissue sarcomas (STSs) are neoplasms arising from
mesenchymal cells within the soft connective tissues of
1Finn Pathologists, Diss, Norfolk, UK
the body. While such tumours may potentially arise at 2Pathobiology and Population Sciences, Royal Veterinary College,
any anatomical location, those arising from the cutane- Hatfield, UK
ous and subcutaneous tissues are most common. The
STS group incorporates a number of neoplasms with dif- Corresponding author:
ferent cell origins, but which are generally considered Melanie J Dobromylskyj BSc Vet Path (Hons), BVSc, PhD,
FRCPath, MRCVS, Finn Pathologists, Histopathology Department,
together due to their similar histological features and The Old School House, One Eyed Lane, Weybread, Diss, Norfolk
biological behaviours; these typically include fibrosar- IP21 5TT, UK
coma, myxosarcoma, peripheral nerve sheath tumours Email: [email protected]
2 Journal of Feline Medicine and Surgery 

(non-brachial plexus), perivascular wall tumours, undif- pedigree, with 12 different breeds represented. The breed
ferentiated sarcomas and sometimes also liposarcomas.1 of cats in the study population was compared with the
The existence of feline injection site sarcomas (FISSs) fur- breed prevalence of a sample from the background popu-
ther complicates the clinical picture for cats; these are lation (n = 3771); this sample from the background popu-
tumours that commonly arise at previous sites of vacci- lation was based on the stated breed on submission forms
nation (historically known as vaccine-associated fibro- accompanying fixed tissue samples received by the labo-
sarcoma) or other focal trauma.2,3 ratory throughout the period April 2006 to May 2011 and
STSs tend to be locally infiltrative, often extending with any diagnosis.14 Anatomical location was catego-
along fascial planes, demonstrating a ‘pseudocapsule’ rised into seven anatomical sites including the head, pin-
and a relatively slow growth rate, but a low to moderate nae, neck, trunk, limbs, digits or tail. Ambiguous locations
incidence of metastasis.2 However their clinical behav- such as ‘dermis’ or ‘injection site’ were excluded from this
iour can vary and post-surgical recurrence is a relatively part of the study.
common occurrence, due to their often poorly-defined Further information was sought from these cases and
peritumoural margins.4 The tumours can be superficial was acquired for 51 cases using a questionnaire to the
and mobile, or may infiltrate deeper tissues, and may submitting practices, approved by the Royal Veterinary
persist for weeks to months with only minor changes College Clinical Research Ethical Review Board. Data
before undergoing rapid growth.5 requested included whether the cat had succumbed to
STSs are one of the most common forms of cutaneous STS-related disease, non STS-related disease or was still
neoplasia diagnosed in the UK cat population, with one alive, together with the date of death where relevant, as
retrospective study6 identifying fibrosarcomas as the well as questions regarding the site and appearance of
most common malignant neoplasm, a finding consistent the mass, and whether there had been any evidence of
with previous studies.7–10 One study has identified local recurrence at the sample site and/or of metastatic
potential prognostic factors specifically for FISS,11 but disease. Forty-nine of these cases had archived tissues
otherwise there are currently no published grading sys- available for histological assessment, and haematoxylin
tems for feline STSs. In dogs, there is a well-established and eosin (HE)-stained sections of each tumour were
grading system and the prognostic factors, including blindly reviewed by a pathologist (MJD), with some
completeness of surgical margins, have been studied.1,12 cases additionally reviewed by a second pathologist
This canine grading system, originally a human grading (KCS). Two of these cases were excluded on assessment
scheme,13 is based on the mitotic rate, presence and of the HE-stained sections as the tissue affected was not
extent of tumour necrosis and a subjective score for haired skin and/or subcutis.
tumour differentiation and, together with completeness None of the cats in this part of the study had concur-
of surgical margins, has been shown in canine STSs to be rent tumours of other histological types. The cats typi-
predictive for local recurrence.1,12 cally presented owing to the mass itself or associated
The aim of this study was to utilise the large number clinical signs (eg, lameness), or rarely for other reasons
of feline STSs submitted to a commercial diagnostic lab- including vaccination (n  =  3), flea-allergic dermatitis
oratory to examine the signalment of affected cats and (n = 1) or a corneal ulcer (n = 1).
the anatomical location of their tumours. A retrospective Each of the remaining 47 individual tumours was
study of the histological features of tumours with known assessed for mitotic index (calculated as the number of
clinical outcomes was then undertaken to identify poten- mitotic figures per 10 high power fields [x400; field area
tially useful prognostic indicators. of 0.237 mm2]), degree of inflammation, presence and
extent of necrosis (none; equal to or less than 50%; more
Material and methods than 50% of tumour present in the section), presence of
Records from a large commercial diagnostic laboratory, multinucleate cells, ulceration and presence or absence
Finn Pathologists (Diss, UK), were searched for all feline of material resembling adjuvant within macrophages.
STSs diagnosed based on fixed tissue samples submitted Margins, where present in the HE-stained sections, were
to the laboratory during the period of January 2012 to also measured to the closest 0.5 mm, and the size of the
December 2013. These dates were selected based on the tumour (excisional biopsy samples only) to the nearest
availability of archived material and to allow for a period 1 mm. Margins were considered ‘incomplete’ if neoplas-
of up to 6 years’ clinical follow-up for any given case. tic cells were contiguous with at least one margin, ‘close’
Clinical details including sex and neuter status, age, if neoplastic cells were closer than 3 mm from the margin
breed and anatomical location were recorded for all or if only a pseudocapsule was present and ‘complete’ if
submissions diagnosed with STSs (n = 723 tumours). neoplastic cells were at least 3 mm from the margin
Domestic shorthair (DSH), domestic longhair (DLH), (including amputations of limbs and tails). The number
‘domestic cat’ and ‘cross-breed’ were amalgamated under of inflammatory cells were subjectively categorised as
the term ‘non-pedigree’; all others were considered none, mild, moderate or severe, while multinucleate cells
Dobromylskyj et al 3

Table 1  Grading system for feline cutaneous and submitted from cats classified as non-pedigree breeds
subcutaneous soft tissue sarcomas (DSH, DLH, ‘domestic cat’ and ‘cross-breed’). Pedigree
breeds accounted for 38 cases (5.3%), with eight tumours
Mitotic score Number of mitoses per 10 submitted from Maine Coon cats (1.1%), six each from
HPFs; x400
British Shorthair and Persian cats (0.8%), four each from
1 0–9 Burmese and Bengal cats (0.6%), three from Norwegian
2 10–19 Forest Cats (0.4%), two cases from Ragdoll cats (0.3%)
3 >19 and one each from Siamese, Sphynx, Russian Blue,
Tumour necrosis score Necrosis as % of tumour area Scottish Fold and British Silver Tabby breeds (0.1%).
When compared with the background population, no sig-
0 No necrosis nificant differences were found between pedigree and
1 Equal to or less than 50%
non-pedigree cats, and no breed predispositions were
2 More than 50%
observed.
Inflammation score   Of the 723 cases, 697 had the gender specified on the
1 None, minimal or very mild
submission form. Of these, 356 were male (51.1%; 282
2 Mild to moderate neutered, 74 entire) and 341 were female (48.9%; 272
3 Severe neutered, 69 entire). The age of 663 cats was specified on
the submission form, giving a median age of 11 years
Histological grade Total score* (range 1–21 years). For non-pedigree breeds (n = 630),
I (low grade) Equal to or less than 3 the median age was 11 years (range 1–21 years), whereas
II (intermediate grade) 4 or 5 pedigree cats (n = 33) had a median age of 10 years
III (high grade) 6 or more (range 2–16 years); this difference did not reach statisti-
cal significance.
HPF = high power field (x400; field area of 0.237 mm2)
The anatomical location of the sample submitted was
*Combined mitotic, tumour necrosis and inflammation scores
recorded on the submission form for 686 cases. The most
common anatomical region affected was the trunk
were subjectively categorised as none, rare, occasional or
(34.5%), followed by the limbs (excluding digits; 28.3%),
prominent. A score for each of the following was
head (17.8%) and the neck (8.9%).
assigned; mitotic index, tumour necrosis and degree of
Forty-seven cases with known clinical outcome and
inflammation present within the tumour. The sum of
tissue available for histopathological assessment were
these scores provides the histological grade for the
included in the second part of the study. Of these, 22
tumour (Table 1). Survival time was assessed as time
were from cases where the cat had died of tumour-
from first diagnosis until either the date the question-
related disease (TRD), although for one case the date of
naire was returned by the submitting practice or the date
death was not recorded. Of the remaining 21 cases in this
that death/euthanasia occurred, whether due to STS-
group, the median survival time (MST) was 205 days.
related disease or other causes.
There were 25 cats that either died of non-tumour related
Data were analysed using IBM SPSS Statistics for
disease (NTRD) or were still alive at the time of the
Windows v19.0 and GraphPad Prism 8.3.0. Categorical
study, with an MST of 854 days (four were lost to follow-
variables were analysed using a χ2 or Fisher’s exact test
up; those still alive at the time of the study were given an
if two binary variables were to be tested. The Shapiro–
arbitrary date of 01/01/2018). The difference between
Wilk’s test was used to identify any normal distribu-
these two MSTs is statistically significant (Mann–
tions (P >0.05). The t-test was used to test association
Whitney U test, U = 70; P <0.00001). For the 22 cases
between two groups. For more than two groups, a one-
that died from TRD, the median mitotic index (MI) was
way ANOVA was used. For non-normally distributed
21 per 10 high power fields (x400; range 5–52), while for
data, the Mann–Whitney U was used for testing of two
the 25 cases that died of NTRD or were still alive at the
groups or Kruskal–Wallis for three or more groups.
time of the study, the median MI was 9 per 10 high
Kaplan–Meier survival plots and corresponding non-
power fields (x400; range 1–70); this difference is statisti-
parametric log-rank tests were examined for the three
cally significant (Mann–Whitney U test, U value = 138;
histological grades. A P value <0.05 was considered
P = 0.00362).
significant.
Grading was applied to 47 cases (22 with death from
TRD, 25 that died of NTRD or that were still alive at the
Results time of the study). Of these, 16 cases were considered
The total number of feline STSs submitted to the labora- grade I (low grade), of which three died from TRD. Of
tory over the time period of this study (January 2012 to those three, in two cases treatment was not attempted,
December 2013) was 723; of these, 685 (94.7%) were while in the third there was local recurrence with a
4 Journal of Feline Medicine and Surgery 

study. Ten of the 17 tumours with MNGCs present were

grade III (high grade), six were grade II (intermediate
grade) and one was grade I (low grade). The presence of
adjuvant within macrophages was noted in eight cases
(17.0%), with only three of those cases from cats that
died of TRD. Of those eight cases, six were grade III
(high grade), two were grade II (intermediate grade) and
none were grade I (low grade).
In 22 cases, margins were available for histological
assessment (excisional biopsy or amputation) from those
cases with a known clinical outcome; of these, four cases
reported local recurrence. Of those four cases, one had
incomplete margins, two had close margins and one had
Figure 1  Kaplan–Meier survival curve for histological grade. histologically complete margins (suspected to be FISS).
The black line represents cats with grade I (low grade) soft
The remaining 18 cases reported no local recurrence; six
tissue sarcomas (STSs) the blue line represents cats with
grade II (intermediate grade) STSs, and the red line represent had incomplete margins, 11 had close margins and one
cats with grade III (high grade) STSs. Tick lines represent had complete margins on histological assessment.
censored cases (lost to follow-up, or died of non-tumour
related causes)
Discussion
A recent study showed that neoplasia arising at any ana-
survival time of 802 days. The MST for cats with grade I tomical site is the fourth most common cause of death in
tumours was 900.5 days. Fifteen cases were considered cats presenting to primary care veterinary practices in
grade II (intermediate grade), and of these eight were the UK.15 Other studies have demonstrated that tumours
reported to have died of TRD. Of those eight, six had arising in the skin and subcutis are the most common
reported local recurrence, one developed further soft form of neoplasia in cats,7,8 and of those, more than half
tissue masses elsewhere suspected to be metastatic dis- are malignant.6,16 Fibrosarcomas, a common subtype of
ease (although histopathological confirmation was not STS in cats, are reported to be the second most common
attempted) and in one case the reason was not reported skin tumour diagnosed in the UK cat population.6
other than ‘tumour-related’. The MST for cats with grade The current study found no significant sex, neuter
II tumours was 514 days. The remaining 16 cases were status or breed predispositions in cats to developing
considered grade III (high grade), and of these 11 had STSs, despite the large study size. There was also no
died of TRD; in four cases there was local recurrence, for significant difference noted when pedigree breed cats
four cases treatment was not attempted and in three were compared with non-pedigree. Previous studies7,8
cases the primary veterinarian reported suspected meta- also found no apparent breed predispositions, although
static disease, although histopathological confirmation Graf et al reported females to be at increased risk com-
was not attempted (two intrathoracic, one renal). The pared with males.8 The large-scale study by Ho et  al
MST for cats with grade III tumours was 283 days. found certain breeds were at decreased risk of develop-
Kaplan–Meier analysis (Figure 1) showed that differ- ing fibrosarcoma of the skin and soft tissues, including
ences between the three survival curves was significant Persian, Siamese, Burmese and British Blue cats, and
(Log-rank [Mantel–Cox] P = 0.0274). also reported no gender difference.6 Ho et al utilised the
The total score given as part of the grading process same database as the present study, although their
was compared between those cases with TRD (n = 22; study spanned a greater time period (2006–2013) and
median score = 5.5; range 3–8) with those with NTRD or encompassed all skin masses submitted for histopatho-
that were still alive (n = 25; median score = 3; range 2–6); logical assessment.6
the difference was statistically significant (Mann–Whitney The median age of the cats in this present study was
U test, U = 130; P = 0.00208). 11 years, with a range from 1 to 21 years. This is largely
Other histological features assessed included the in agreement with previous studies, with such tumours
degree of inflammation and the presence of multinucle- mostly arising in middle-aged to older cats, although
ate giant cells (MNGCs) and potential adjuvant within with a wide age range represented.6–8 Two studies look-
macrophages. There was a statistically significant asso- ing at FISS in particular reported median ages of 9.5
ciation between the degree of inflammation and survival years3 and 11 years.11
time (P =  0.015). Seventeen of the 47 tumours had In the current study, the most commonly reported
MNGCs present (36%); of those, 10 were tumours from anatomical locations for STSs to arise were the trunk, fol-
cats that died of TRD, and seven were from those that lowed by the limbs, the head and the neck. Miller et al
died of NTRD or that were still alive at the time of the reported the most common sites as the limb and head,
Dobromylskyj et al 5

followed by the trunk and with none reported on the the tumours with MNGCs were grade II or III, and mac-
neck; this study specified fibrosarcomas, however, and rophages containing adjuvant were noted in grade II
was based on a North American feline population.7 (n = 2) and grade III (n = 6) tumours only. Both MNGCs
There may also have been differences in the way head, and suspected adjuvant within macrophages are fea-
neck, trunk and limb were defined between the two tures noted in FISS,17 although they may not always be
studies, as anatomical regions such as ‘limb’ do not present, meaning that differentiation of FISS from other
necessarily have clear boundaries. forms of STSs can be challenging from a histological per-
Clinical outcome and archived tissues were available spective. In human tumours, the presence of MNGCs is
for 47 cases in the present study. The outcome for 22 of generally regarded as an expression of anaplasia and is
those cases was death related to the tumour; this included assumed to indicate a more aggressive phenotype. Couto
six cases where further treatment was not attempted et al3 reported that MNGCs were a common finding in
after the diagnosis of STS was made (via incisional FISS and were most often seen in higher grade tumours,
biopsy). Eleven cases reported local recurrence, and four consistent with the findings in the present study.
cases had suspected metastatic disease, including to the Very few studies have applied the canine STS grading
kidneys, lungs and other soft tissue sites (although no system to feline STSs. Two such studies3,11 focused solely
attempt was made to confirm metastatic disease [or local on FISS, and neither found grading to be of prognostic
recurrence] histologically in these cases). Poor quality of merit in these tumours. Porcellato et al reported that the
life was commonly reported as forming an important STS grade, depth of infiltration, surgical margin and
part of the decision to euthanase in these cases. Twenty- Ki67 score of these tumours bore no relation to the likeli-
five cats did not succumb to TRD; some of these cats hood of local recurrence, while the size of the tumour
died from other non-tumour related causes, a reflection and the mitotic count were more useful (a cut-off of 20
of the generally older age of affected cats and the long mitotic figures per 10 high power fields was used).11 The
follow-up period of this study. Two of these cases also grading system used in the present study is a modified
reported local recurrence, not resulting in euthanasia but version of the one applied in these two FISS studies.
in repeat surgery. Some of these cats were still alive at the Having evaluated potential factors individually, those
time of the study, up to 6 years following treatment by which were found to be significantly associated with
excisional biopsy or amputation of the affected limb (or survival time were then incorporated into two different
tail). When comparing the group of cats that succumbed grading systems (the second system was not as strongly
to TRD with the group of those that did not, there were associated with outcome and was therefore not included
statistically significant differences in MST, the mitotic here).
count of their STSs and in the total score of the tumour The canine STS grading system is based on a human
(as calculated as part of the grading process). The study scheme.13 Some sarcomas that are not typically included
was designed to allow a prolonged period from time of within the canine STS group were included in the origi-
diagnosis to the time the questionnaire was returned, nal human study,13 which found that histological grade
with the presumption that given sufficient time cats was predictive of survival and also disease-free inter-
could also potentially succumb to non-tumour related vals. Interestingly, the histological grading of adult
causes as well as to TRD. These cases were included in human STSs is predictive of metastatic disease (rather
the survival analysis, on the assumption that this was a than local recurrence).13,18 Metastatic disease is consid-
sufficiently long time period to have lapsed without any ered uncommon in canine STSs; it is reported to be rare
obvious sign of local recurrence/metastatic disease lead- in canine grade I STSs, of uncertain frequency in grade II
ing to death owing to TRD. STSs and to be most frequent in grade III tumours.
Histological assessment of these 47 tumours followed Published studies do not generally verify metastatic dis-
by grading revealed that there was a statistically signifi- ease histologically, and are further hampered by the rela-
cant difference in the MST between tumours of differing tively rare occurrence of metastatic disease and the small
grades; for grade I (low grade) tumours, the MST was numbers of grade III STSs diagnosed in dogs; thus it is
900.5 days, compared with 514 days for grade II (inter- difficult to be certain of the true metastatic rate of these
mediate grade) and 283 days for grade III (high grade) tumours.1 Metastatic disease has been reported affecting
tumours. A greater degree of inflammation was also lymph nodes and the lungs.19–21 In the current study, four
found to be associated with shorter survival times and of the 22 cats that died of TRD were suspected to have
was thus incorporated into the grading system, replac- metastatic disease (out of the 51 cases with clinical fol-
ing the subjective ‘degree of tumour cell differentiation’ low-up available); however, this was not confirmed his-
component of the traditional canine STS grading scheme. tologically. Those with suspected metastatic disease had
MNGCs and suspected adjuvant within macrophages grade II (n = 1) and grade III (n = 3) tumours; these num-
were also more frequently noted within higher grade bers are too small to draw any conclusions but would
tumours, but not necessarily with TRD. All except one of appear to be consistent with the previous understanding
6 Journal of Feline Medicine and Surgery 

that these tumours are unlikely to metastasise. This may can be assessed on routine HE-stained sections. In this
also reflect that metastatic disease is slow to occur and/ small scale study, the histological grade of the tumour
or metastatic lesions are slow to grow to a size likely to appears to be associated with survival time, although
be clinically detectable or to pose a significant threat to larger scale studies are required to confirm this finding.
life, particularly in older patients that often have
comorbidities. Acknowledgements  The authors would like to thank all of
There is no clear consensus as to whether the histo- the staff at Finn Pathologists for their assistance with accessing
logical grade of canine STSs is associated with overall the database and producing the tissue sections. This research
survival;1 in one study, the grade was prognostic for sur- was performed as part of a final year research project (VR)
supported by the Royal Veterinary College.
vival19 but in several others it was not.12,21–23 McSporran
demonstrated that histological grade was a predictor of
Conflict of interest The authors declared no potential
local recurrence after excisional biopsy, but not sur-
conflicts of interest with respect to the research, authorship,
vival.12 Canine STSs were most often grade I or II, with and/or publication of this article.
relatively few grade III tumours,1 whereas in the current
study feline STSs were evenly spread across the three Funding  The authors received no financial support for the
grades. This may reflect the differences between the two research, authorship, and/or publication of this article.
grading systems used, differences between the two spe-
cies and/or may be impacted by the presence of FISS Ethical approval This work involved the use of non-
within the feline population, which themselves appear experimental animals only (including owned or unowned
to be typically of higher grade than other feline STSs. animals and data from prospective or retrospective studies).
In the present study, there were relatively few cases Established internationally recognised high standards (‘best
with both clinical follow-up and margins available for practice’) of individual veterinary clinical patient care were
followed. Ethical approval from a committee was therefore not
assessment, meaning that it is difficult to determine the
necessarily required.
effect of margin completeness on the likelihood of local
recurrence and survival time. Margins could only be Informed consent  Informed consent (either verbal or writ-
measured for those cases with excisional biopsies (or ten) was obtained from the owner or legal custodian of all
amputations). Furthermore, the mass was not available animal(s) described in this work (either experimental or non-
for gross assessment, meaning that measurement of mar- experimental animals) for the procedure(s) undertaken (either
gins had to be performed on the tumour represented in prospective or retrospective studies). No animals or humans
the histological sections. Other limitations of the study are identifiable within this publication, and therefore addi-
include the small number of cases with clinical follow- tional informed consent for publication was not required.
up available, for what is undoubtedly a common but het-
erogeneous group of tumours with a range of potential ORCID iD Melanie J Dobromylskyj https://orcid.org/
0000-0002-0781-5726
biological behaviours. The FISS phenomenon further
complicates the picture for our feline patients; if FISS
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