PRINCIPLES OF ONCOLOGIC SURGERY
Laurent Findji DMV, MS, MRCVS, Diplomate ECVS
VRCC Veterinary Referrals, Essex, United Kingdom
“Tumours belong in formalin jars” – William Stewart Halsted (1852-1922)
Surgery has been and remains the mainstay of treatment of solid cancers and most cancer cures in humans today
still result from surgery alone.
Historically, surgeons were first limited in the extension of surgical excisions by their own technical
insufficiencies and shortcomings of supporting disciplines such as anaesthesia and intensive care medicine. As
progress was made in these other fields came the era of large resections. Initially, it appeared that wider
resections improved the prognosis. However, this was only true to a certain point and, although local disease
control was more often achieved, metastatic disease remained an obstacle to cure. Surgery as sole treatment of
cancer was obviously not the panacea.
The most efficient treatment of cancer is today multimodal. It is now clear that surgeons should be members of a
team including radiographers, anaesthetists, criticalists, pathologists, and medical and radiation oncologists. In
addition to surgical skills, surgeons need to have a good knowledge of tumour biology to determine the role and
contribution of surgery, for each case, to the whole treatment. They also need to understand how other therapies
work, in order to adapt their surgical technique to previous or later treatments.
These are exciting perspectives for oncologic surgeons. Their role is constantly evolving as they are increasingly
working in close cooperation with other specialists in fields such as chemotherapy, radiotherapy and
immunotherapy. Whilst the times of extensive, technically challenging resections are not over, the oncologic
surgeon has evolved from a technician to a more complete clinician, whose deep knowledge in cancer biology
allows more concerted and tailored procedures.
Every surgeon treating cancer should not only be an oncologic surgeon but rather a surgical oncologist. Like in
the other fields of surgery, thinking in terms of biology is the most important concept of oncologic surgery. It
means that above all, the surgeon needs to know what type of tumour they are dealing with, and what its
characteristics (expected behaviour, response to treatment, possible paraneoplastic syndromes, etc.) are.
Roles of surgery in oncology
Diagnostic surgery
Biopsies
Biopsies are crucial in the diagnosis process of tumours. They can be incisional or excisional. They are
performed percutaneously (core-needle biopsies), or by minimally-invasive or conventional surgery.
Staging surgery
Surgery can be involved in tumour staging. Lymph node biopsies (incisional or excisional) provide helpful
information on locoregional spreading of a tumour. Exploration of body cavities for signs of metastatic disease
can also be performed, either when operating the main tumour (e.g. inspection of the abdomen when resecting an
abdominal tumour) or separately. Minimally-invasive surgery (laparoscopy, thoracoscopy) is increasingly used
in such indications.
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Curative-intent surgery
Surgery is most often performed with an intention to cure, whether it be through surgery alone or combined with
other therapies. Depending on the “dose” of surgery administered, several types of tumour resections are
possible: cytoreductive or intracapsular, marginal, wide and radical.
Cytoreductive surgery consists of removing as much of the tumour as possible but leaving macroscopic disease
behind. It is only considerable in a view of potentiating a planned adjuvant therapy is planned. However,
adjuvant treatments are less effective in presence of macroscopic disease, which makes cytoreductive
(debulking) surgery very rarely acceptable1.
Marginal resections consist of excision of the tumour with minimal amounts of surrounding tissues. The
likelihood of leaving microscopic residual disease is high and this type of resection should be avoided as much
as possible. However, in certain cases, it is preferable to more extensive resections, either because of difficulties
in wound reconstruction (e.g. tumours of extremities) or vicinity of non-expandable structures (e.g. brain
tumours). In such cases, surgery should be followed by adjuvant therapy, radiotherapy especially.
Wide resections consist of excision of the tumour with enough surrounding tissues to expect complete excision
including microscopic disease. This is the type of resection to seek as often as possible. Its main limitation
comes from the fact that precise guidelines as to what appropriate margins should be for each tumour type are
lacking. Therefore, in some cases, microscopic disease remains, leading to recurrence. Good communication
with the pathologist is essential to have as precise an assessment of the excision margins as possible.
Radical resections consist in even wider resections. Often, it consists of the excision of body parts
(amputations). A good definition is that after radical excision, there is no need to await the pathology results to
know that the surgical margins are free of tumour.
Palliative surgery
Palliative surgery is performed to improve the patient’s quality of life, without extending its life expectancy.
Amputation for an appendicular osteosarcoma and splenectomy on a haemangiosarcoma are two examples of
palliative surgeries, as they do not improve survival times per se.
The difference between curative and palliative surgeries mainly lies in the intent2: whenever the surgeon is
seeking a cure, the surgery is considered curative although in many cases a cure will not be obtained and the
surgery will at best be providing palliation. The goal of palliative surgery is to improve the patient’s quality of
life by relieving as much as possible the clinical signs resulting from its cancer. Palliative surgery may also
increase life expectancy, as a result of this improvement of the quality of life, but also through its direct action
against the tumour development when possible. Overall, the line between curative and palliative surgeries can be
very fine: with many tumours, the surgeon knows that the tumour is unlikely to ever be cured even though a
curative-intent procedure will be performed. In every case, the surgeon aims at getting the longest disease-free
interval and his means are similar, whether the procedure be performed with an intent to cure or merely to
palliate.
When opting for a palliative surgical intervention, it is most important to balance the expected benefits and
improvement of quality of life against the risks and morbidity associated with the procedure. The less likely a
tumour is to be curable, the smaller the operative risk and the shorter the expected recovery from the procedure
must be. In deciding the “dose” of surgery to apply to an animal with cancer, the discussion with its owners is
critical: it is most important for them to be well informed of the prognosis and of the results which can be
reasonably expected after surgery in terms of disease-free interval and potential postoperative complications.
Preventive surgery
Some cancers, such as hormone-dependant cancers, can be prevented by surgical procedures: prepubertal
ovariectomy in dogs dramatically reduces the risk of mammary tumour; castration of dogs prevents the
occurrence of testicular tumours and perianal adenomas; etc.
In human surgery, preventive or prophylactic surgery, defined as the pre-emptive operative of an organ prior to
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malignant transformation or while the cancer is in situ3, is used increasingly as the increasing knowledge of
genetics increases the ability to determine the individual risk of patients to develop cancer of some organs in
their lifetime. Common applications include preventive surgery for hereditary forms of ovarian, breast, colon or
thyroid tumours.
Ancillary surgery
Surgery for medical support
Placement of feeding tubes can be necessary to support nutrition of cancer patients. Cachexia is a major concern
in some cancer patients. Nutritional support is known to decrease associated morbidity in humans.
Surgery for treatment device implantation
Surgeons can play a part in non-surgical treatments by placing several types of implants such as vascular access
ports, intracavitary catheters, brachytherapy catheters, etc.
Before surgery
Before surgery, the patient’s general health status must be evaluated as it may have consequences of the
treatments to pursue, in type and extent. In addition, the findings of the general health profile may indicate
further tests which may reveal extension of the malignancy in distant systems (metastatic disease).
In addition, the tumour type and extension (staging) must be determined. The local staging of the tumour,
obtained through imaging, will allow the precise planning of surgery.
Evaluation of the patient
The cancer patient is often an older animal. As such, it can be affected by concurrent diseases. However, age is
not a disease in itself, and it should not be considered a negative prognostic factor4-6 as tumour biology and
response to treatment are not influenced by advanced age. In fact, malignant tumours in young animals tend to
have a more aggressive behaviour than in older animals. For instance, dogs of less than 2 years of age with
osteosarcoma are reported to do worse than older dogs when treated with amputation alone 7. The concomitancy
of systemic diseases may nonetheless influence treatment options. It is therefore essential to obtain a general
health profile in all cancer patients.
In addition to diseases associated with age, a proportion of cancer patients will suffer from one or several
paraneoplastic syndromes (PNS), which are diseases caused by substances, produced by the tumour, having a
systemic effect. The PNS of greatest relevance for the surgeon in veterinary medicine are hypercalcaemia,
hypoglycaemia, anaemia, thrombocytopaenia / coagulopathies, hypo / hypertension, and cancer cachexia /
anorexia (Table 1).
Hypercalcaemia as a paraneoplastic syndrome is referred to as hypercalcaemia of malignancy (HM).
Hypercalcaemia has pathophysiological effects on renal, cardiovascular, neuromuscular and gastrointestinal
functions, but its primary clinical manifestations are usually due to impairment of renal function. Severe HM
(i.e. calcium > 180 mg/L) should be considered a medical emergency: treatment is initiated in proportion with
the severity of HM and associated clinical signs, and the cause of HM is investigated. Management of HM is
beyond the scope of this text and is widely detailed elsewhere 8-10. Briefly, it is treated with a combination of
fluid therapy (0.9% NaCl), loop-diuretics (furosemide) once dehydration is corrected, steroids when the cause of
HM has been diagnosed and, for extreme or refractory cases, calcitonin and bisphosphonates. Concurrently, the
tumour responsible for HM is searched. Lymphoma is the most common cause and its presence must be
investigated. A careful rectal examination is also important to detect an anal sac carcinoma, for which the
primary tumour can be of very small size. Beyond these, a thorough physical examination, imaging and tests are
used to localise the malignancy. With some tumours, such as anal sac carcinomas or parathyroid tumours, after
an initial period of medical support and patient optimisation, surgery is rapidly necessary to treat HM.
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Hypoglycaemia as a PNS most commonly results from beta-islet cell pancreatic tumours (insulinomas)8, 10.
However, extra-pancreatic tumours can also be responsible for paraneoplastic hypoglycaemia. Such tumours
include lymphoma, hepatocellular carcinoma, leiomyoma and leiomyosarcoma, haemangiosarcoma, salivary
gland carcinoma and oral melanoma. Clinical signs depend on the severity, rate of onset, duration and cause of
the hypoglycaemia. Similarly to HM, paraneoplastic hypoglycaemia is treated symptomatically as its origin is
investigated. When a tumour is found which could explain it, the best treatment is excision of the tumour
whenever possible. When surgery is not an option, a medical treatment (prednisolone, diazoxide, etc.) can help
control the paraneoplastic hypoglycaemia with more or less lasting effects. When no tumour can be found by
diagnostic imaging but insulin levels are high in the face of hypoglycaemia, an exploratory coeliotomy may be
indicated as some insulinomas are too small to be detected by imaging techniques.
Anaemia is a common finding in animals with cancer. Numerous mechanisms can lead to anaemia as a PNS: the
lack of red blood cells results either from loss (i.e. haemorrhage), destruction (e.g. haemolysis) or decreased
production (e.g. anaemia of chronic disease, myelophthisis). Most frequently, the paraneoplastic anaemia results
from chronic disease, immune-mediated haemolysis, blood loss or microangiopathic haemolysis. For all these
mechanisms of paraneoplastic anaemia, excision of the tumour responsible is the treatment of choice. However,
in some cases, both specific (e.g. immunosuppressive drugs) and non-specific (e.g. blood product administration)
treatments for the anaemia, can be necessary. Non-specifically, before embarking on surgery, the patient must be
optimised and have sufficient oxygen-carrying capacity. Blood products or haemoglobin-based oxygen-carrying
solutions (Oxyglobin®) must therefore be administered whenever haemoglobin levels are inadequate. As a rough
guide, the oxygen-carrying capacity should be considered insufficient for surgery when packed-cell volume
(PCV) is below 25% and the PCV should at least be maintained above 20% during and after surgery. However,
the need for blood product administration depends on the clinical condition of the animal rather than on absolute
values of its PCV.
Ideally, when fresh blood products are to be transfused from one animal to another, the donor and recipient
should be blood typed prior to administration. If blood typing is unavailable, a crossmatch should be performed.
If time is lacking, using a donor negative for dog erythrocyte antigens (DEA) 1.1 and 1.2 greatly limits the risks
of hazardous reaction. Furthermore, transfusion reactions are limited in dogs which have never received blood
products previously because of the absence of native alloantibodies. To the contrary, in cats, donors and
recipients should be typed, given the presence of natural alloantibodies and severity of blood transfusions in this
species.
The amount of blood to be administered depends on the PCV of the recipient, on the PCV of the donor and on
the desired PCV of the recipient after transfusion. It can be calculated as follows:
Volume of blood to transfuse = V x (recipient desired PCV – recipient current PCV) / donor PCV,
where V=90 in dogs and V=70 in cats.
Alternatively, it can be considered that whole fresh blood administered at a rate of 2.2 ml/kg will raise the
recipient’s PCV by approximately 1%.
Thrombocytopaenia is another PNS of great relevance for the surgeon. Like for anaemia, the lack of platelets
can result from their excessive consumption (e.g. haemorrhage, disseminated intravascular coagulation),
destruction (e.g. immune-mediated) or decreased production (e.g. myelophthisis). Thrombocytopaenia as a PNS
is most frequently associated with vascular tumours or tumours infiltrating the bone marrow. Similar tumours
and mast cell tumours can in addition cause coagulopathies. Any tumour can cause acute or chronic
disseminated intravascular coagulation (DIC), which in turn can lead to thrombocytopaenia by excessive
consumption of platelets. However, DIC is most frequently clinically relevant in cases of haemangiosarcoma.
Excessive bleeding can also be observed in patients with mast cell tumours. It is likely the consequence of the
release of heparin as mast cells degranulate.
Most coagulopathies will be best treated by excision of the tumour. However, as sufficient haemostasis is
required for surgery, symptomatic treatments may be necessary before surgery. To bring coagulation factors to
the patient, plasma (fresh, fresh-frozen, cryoprecipitate) can be administered. To bring functional platelets, fresh
whole blood should be administered as platelets are rapidly destroyed when blood is stored (within 2 to 4 hours).
When thrombocytopaenia results from haemorrhage (e.g. bleeding splenic haemangiosarcoma) and the patient is
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stable enough to undergo surgery without transfusion, the administration of blood products is sometimes
withheld until the bleeding is controlled.
Hypertension and cardiac arrhythmias can be life-threatening consequences of the presence of certain tumours
such as pheochromocytomas. These tumours can produce catecholamines which can be massively released in the
blood stream when they are manipulated.
On the contrary, perioperative hypotension, secondary to the release of histamine and other vasoactive
substances, can be encountered when mast cell tumours are manipulated and degranulate.
In both cases, these possibilities need to be anticipated. When operating on pheochromocytomas, premedication
favouring hypertension and arrhythmias are avoided and emergency treatments (phentolamine, lidocaine,
propranolol, etc.) are kept at hand. If hypotension is feared when operating on a mast cell tumour, anti-histamine
drugs (e.g. diphenylhydramine) and steroids are administered preoperatively.
Cancer cachexia consists of weight loss in the face of adequate nutritional intake. Cancer anorexia consists of
weight loss associated with insufficient nutritional intake. Their cumulative incidence in veterinary oncology is
unknown. In humans, it clearly is a negative prognostic factor for a variety of malignancies. Severe malnutrition
may have deleterious effects on wound healing and postoperative infection rates. The effects of cancer cachexia
and anorexia often last for some time after the tumour has been excised. For this reason, the surgeon must
anticipate the need for forced enteral feeding postoperatively and be ready to place feeding tubes at the time of
surgery.
Hypercalcaemia
Lymphoma
Anal sac carcinoma
Multiple myeloma
Thymoma
Parathyroid tumours, …
Hypoglycaemia
Insulinoma
Hepatocellular carcinoma
Smooth muscle tumours (leiomyoma, leiomyosarcoma)
Anaemia
Haemangiosarcoma
Digestive tumours
Mast cell tumour, …
Bleeding disorders
Haemangiosarcoma
Mast cell tumour
Thyroid carcinoma, …
Hypertension
Pheochromocytoma
Adrenocortical adenoma / adenocarcinoma
Hypotension
Mast cell tumour
Table 1: Common paraneoplastic syndromes and associated tumours
Ideally, the work-up of any cancer patient undergoing surgery should at least include a complete blood count, a
biochemistry panel, electrolytes and urinalysis. When the tumour to operate may be associated with
coagulopathies or when the procedure carries a risk of significant blood loss (e.g. maxillectomy, liver lobectomy,
thyroidectomy), a coagulation profile should also be run.
Tumour diagnosis
Knowledge of the tumour type is essential to determine the best course of treatment. No mass should ever be
excised without knowing its nature. This diagnosis is generally made on the basis of cytological (fine-needle
aspirates) or histopathological (biopsies) examination of the primary tumour.
Fine-needle aspirates are an extremely useful tool for the surgical oncologist, who should have a good
knowledge of basic cytology. They can be performed directly or under imaging (ultrasound or CT) guidance for
deeper lesions. It is however important to acknowledge the limitations of cytology and not base decisions
involving major surgeries (e.g. large resections, amputations) only on it. Cytology appears to be most reliable for
diagnosis of cutaneous and subcutaneous masses (70%-91% of agreement between cytology and
histopathology)11-13. It appears much less reliable for examination of hepatic and splenic masses 12, 13. Diagnostic
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cytology is also more sensitive round cell and epithelial tumours then mesenchymal tumours, whose cells tend to
exfoliate less12, 14. A more detailed review of the data of literature regarding the accuracy of diagnostic cytology
system by system is available elsewhere15. Some tumour types can be fairly easily determined by cytology (e.g.
lymphoma, mast cell tumour, melanoma), but cytology does not provide much information on the grade of the
tumour (i.e. aggressiveness, invasion, etc.). Whenever knowing the precise nature and grade of a tumour will
affect the treatment (type and extent) to pursue, a biopsy is indicated (Figure 1). The principles of surgical
biopsy techniques are discussed below in this text.
In addition to cases for which a properly performed excisional biopsy is appropriate, there are a few situations in
which a biopsy is not necessary before definitive treatment. When the precise knowledge of the tumour type and
grade will not change the treatment options and when the risk associated with the biopsy is not worth the
potential information it may yield. For instance, percutaneous splenic biopsies are often unrewarding, as a result
of blood contamination, and carry a significant risk of haemorrhage and seeding of neoplastic cell in the
abdominal cavity. Furthermore, should it lead to a diagnosis, it is unlikely that the appropriate treatment
(splenectomy) will differ significantly depending on it. The same is true for primary lung tumours, whose
treatment is lung lobectomy, regardless of their type and grade. In addition, percutaneous lung biopsies carry a
risk of haemorrhage, iatrogenic pneumothorax or pyothorax, and tumour cell seeding in the pleural space.
Another example is thyroid tumours. Percutaneous biopsies of thyroid tumours carry a significant risk of severe
haemorrhage, which can prove difficult to control. In this case, the risk associated with preoperative biopsy is a
great as the intraoperative risk. For thyroid tumours, the invasive versus non-invasive (adherent versus nonadherent) nature of the mass is a more important criterion to choose between treatment options.
A particular case is bone tumours. If signalment, history, and clinical and imaging findings support the
hypothesis of primary bone tumour, many experienced surgeons will be confident enough to amputate (or
perform limb-sparing surgery on) the patient without performing a biopsy beforehand. The rationale for this
attitude is that the degree of suspicion is often very strong and other differential diagnoses rather few, and that
the biopsy carries a risk of pathological fracture and misdiagnosis if only reactive bone is sampled, and will
delay definitive treatment. However, the risk is then to amputate a patient and find out that the lesion was not a
tumour.
Figure 1: Surgical decisions facing a surgically resectable solid mass
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Tumour staging
When the general health profile has been obtained and the nature of the tumour is known or suspected on the
basis of its cytological examination, the tumour is staged. Staging follows the TNM classification: a score is
given to 3 categories describing the presence and extension of the primary tumour (T), locoregional lymph nodes
(N) and distant metastasis (M). Schemes adapted to various tumour types have been developed which correlate
more accurately with prognosis, but the principle remains the same (Table 2).
Primary Tumour
No evidence of neoplasia
T0
Tumour <1 cm diameter, not invasive
T1
Tumour 1–3 cm diameter, locally invasive
T2
Tumour >3 cm diameter or evidence of ulceration or local invasion
T3
Node
No evidence of nodal involvement
N0
Node firm, enlarged
N1
Node firm, enlarged, and fixed to surrounding tissues
N2
Nodal involvement beyond the first station
N3
Metastasis
No evidence of metastasis
M0
Metastasis to one organ system (e.g., pulmonary metastasis)
M1
Metastasis to more than one organ system (e.g., pulmonary and hepatic metastases)
M2
Table 2: TNM Classification scheme for tumours in animals16
The primary tumour (T) is staged by means of palpation and diagnostic imaging.
Conventional x-rays are useful to detect bone involvement or reaction, but is somewhat insensitive: loss of 30 to
40% of bone mineral density is required to induce radiographic changes 17. Conventional radiography therefore
tends to underestimate the extent on bone involvement.
Ultrasound is most valuable for the evaluation of abdominal tumours and lymph nodes. It is also superior to
conventional radiography in presence of cavitary effusions. It is sensitive but not very specific: it cannot
accurately differentiate benign from malignant lesions18, but can guide the performance of fine-needle aspirates
or core-needle biopsies. It may also help determine the nature and invasion of tumours within soft tissues (e.g. in
the neck and limbs). In addition, Doppler techniques can provide information on the tumour vascularity. The
amount and accuracy of the information provided by ultrasound are, however, very dependent on the skills of the
operator.
Advanced imaging techniques, such as computed tomography (CT) or magnetic resonance imaging (MRI), are
much more reliable for determination of tumour extension and relationships. CT and MRI allow precise
assessment of tumour extension within soft tissues. They are extremely valuable for planning surgical resection
as they provide 3D images, either after reconstruction (CT) or direct acquisition (MRI). CT is generally better for
evaluation of the thorax and it is indispensable for proper radiotherapy planning. On the other hand, MRI offers
better tissue differentiation and is the imaging modality of choice of the nervous system.
Locoregional lymph nodes (N) are evaluated through palpation, fine-needle aspiration and biopsy. Lymph node
enlargement is screened by palpation and imaging (ultrasound, CT, MRI). Fine-needle aspiration and cytological
examination of the locoregional lymph nodes should however ideally be performed regardless of their size: a
study evaluating 100 dogs with oral malignant melanoma showed that lymph node palpation and size are not
reliable indicators of lymph node metastasis and that cytology or histology was required for accurate staging 19.
In another study involving 37 dogs and 7 cats, clinical examination of the lymph node also appeared poorly
correlated with their metastatic status20. In that same study, cytological examination of lymph nodes for tumour
invasion appeared 100% sensitive and 96% specific, showing that fine-needle aspiration is an accurate diagnostic
tool for lymph node metastasis evaluation. However, tumours do not necessarily drain to the closest lymph node
and may even drain controlaterally. Limiting fine-needle aspirations to the mandibular lymph nodes because they
are superficial thus decreases staging accuracy. Ideally, individual mapping of the tumour drainage should be
obtained to determine the position of the sentinel lymph nodes, which are the first to which the tumour drains
and whose aspiration therefore is the most sensitive for detection of metastasis 21. This is seldom performed in a
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clinical setting. In the absence of sentinel lymph node mapping, it can only be recommended to sample as many
regional lymph nodes as possible, regardless of their size, in order to increase staging sensitivity. However, there
is considerable variation in the number and consistency of lymph nodes, and some are not normally palpable.
Staging accuracy is therefore limited by the impossibility of targeted or exhaustive lymph node sampling.
The presence and extension of metastatic disease (M) is evaluated by ultrasound, radiography and advanced
imaging (CT, MRI). The pulmonary parenchyma is the most common site of metastasis of tumours, especially
sarcomas. Thoracic x-rays are therefore most often indicated when screening for metastases. Two incidences,
preferably 3, are required to increase the sensitivity of chest x-rays. As a result of the difference in the perfusion
/ ventilation ratio between the dependent and nondependent lungs, lesions of soft tissue density will appear more
clearly when the lung they sit in is nondependent. Radiographs are not very sensitive (65% to 97%22) for
detection of pulmonary metastases and lesions need to be at least 4 to 8 mm in diameter to be visible on
conventional x-rays4, 22, 23. On the anaesthetised animal, manual lung inflation can be applied to improve contrast.
However, CT is more sensitive than conventional radiographs for detection of thoracic metastatic disease24.
Scintigraphy is another means of detecting metastatic disease. It can be used to evaluate the bones, kidneys,
thyroids, lungs and liver, using different radionuclides. It is very sensitive but poorly specific: benign (e.g.
inflammatory) and malignant lesions have a similar aspect. It is therefore useful to signal distant lesions which
must subsequently be investigated by other means (i.e. imaging, cytology, histopathology). The availability of
appropriate facilities and equipment greatly limits the use of scintigraphy in a clinical setting.
The choice of the imaging modality depends on the nature of the tumour to stage. For tumours preferentially
spreading by lymphatic route (e.g. mast cell tumours), imaging is targeted at locoregional lymph nodes (e.g.
abdominal ultrasound rather than chest x-rays) and fine-needle aspirates of these locoregional lymph nodes are
more systematically obtained. Conversely, when staging sarcomas, imaging of the lymph nodes is of lesser
interest, whereas chest x-rays are essential for evaluation of the pulmonary parenchyma. Similarly, the extent of
the staging is dictated by the expected malignancy of the primary tumour to some degree: it may be decided not
to stage a small mast cell tumour appearing well differentiated on cytology or histopathology before receiving
the definitive histopathology results. Should the mass appear more aggressive (higher grade) than expected,
more exhaustive staging may be pursued.
Planning surgery
Once the tumour type and stage are known, treatment can be considered. This is where the surgeon needs to have
a good knowledge of non-surgical therapies, to determine whether surgery is the best course of action and, if so,
if it will be the sole treatment or merely part of a multimodal treatment. When in doubt, the surgeon must consult
medical and radiation oncologists to discuss what treatment modality, if any, will be optimal for the patient.
Similarly, if surgery is required, it needs to account for the treatments administered before (neoadjuvant
treatments) and those administered after (adjuvant).
In every case, surgery must be planned. No masses should ever be excised without any knowledge of their
nature, expected behaviour and recommended margins of excision. Unplanned marginal resections are associated
with a higher risk of incomplete resection compared to well-planned excisions, and can significantly impair the
chances of local disease control after revision surgery1.
The most important point, when planning surgery for tumour resection, is to balance the consequences of surgery
and potential complications against the expected benefits. In other words, the treatment should never be worse
than the disease! It is easy for surgeons to be tempted to perform technically challenging procedures, which turn
out to be of no significant benefit for the patient. Inversely, surgeons should not deter owners to proceed with
some apparently extensive, but well tolerated, surgeries (amputations, extensive mandibulectomies /
maxillectomies, etc.) because they personally feel uncomfortable with them. Referral should then be offered.
It is crucial that surgeons place the patient’s welfare first, before owners’ wishes. In-depth discussion with the
owners will allow understanding what their expectations are and whether they can be met by possible treatments.
This will avoid misunderstandings and later issues.
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Knowledge of the tumour type and biology is paramount in appropriate surgical planning. The surgical “dose”
depends on it. The first surgery is the best chance to cure, it should not be wasted.
Surgery is planned on the basis of physical examination and diagnostic imaging (cf. local tumour staging). The
recommended margins are determined around the tumour in 3 dimensions and anatomic structures included in
this volume are considered. Structures which can be resected without significant morbidity usually are included
in the resection plan and those which are not expendable (e.g. spinal cord, heart, brain) are preserved. Decisions
have to be made regarding structures which can be resected at the cost of significant functional consequences.
The benefit of their resection en-bloc with the tumour has to be weighed against the functional consequences and
this must be well discussed with the owners.
When surgery has been planned, pain management must be anticipated. Some cancer patients are presented with
pre-existing pain associated with their disease. It has been estimated that at least 30% of tumours of dogs and
cats are associated with significant pain at the time of diagnosis 25. Tumours themselves are not painful as they
are not innervated. However, when tumours grow at the expense of surrounding structures, either compressive or
invading them, pain is to be expected. Metastatic cancers are almost always painful.
In addition, oncologic surgery is often aggressive and destructive. It is therefore expected to be associated with
moderate to severe pain, depending on the procedures. The description of techniques and protocols of analgesia
is beyond the scope of this text, but for optimal efficacy, systemic analgesia is often combined with local
analgesia (e.g. epidural injections, nerve blocks, wound diffusion catheters, etc.).
Techniques in oncologic surgery
Biopsies
Performing a biopsy consists of obtaining tissues for analysis (often histopathological) in view of getting of a
better understanding of their nature. Properly performed, biopsies do not seem to negatively affect the course of
the disease: there is no evidence of increases in the frequency of metastatic disease after biopsies, but seeding of
cancer cells and subsequent tumour local spreading along the biopsy tract is possible 26. It is therefore extremely
important to plan biopsies keeping in mind that, should surgical excision of the tumour be later contemplated, the
entire biopsy tract or surgical approach will need to be excised en-bloc with the tumour.
Many biopsy techniques exist and the choice of one of them depends on the organ involved, on the patient’s
condition, on the clinician’s preference, on the tests to be performed, as well as on the most expected diagnosis.
When histopathology is contemplated, the larger the samples obtained the better, as the accuracy of the
histopathological diagnosis is largely proportional to the size of the sample(s) 27. However, the larger the sample,
the more traumatic the procedure. Therefore, the choice of a biopsy technique is a compromise between
obtaining a sample which is large enough whilst remaining as little traumatic as possible. In addition, the
procedure must be as safe as possible and the patient’s general condition and concurrent diseases are to be
considered when making this choice.
In uncommon selected cases, lesions thought to be tumours can be excised without obtaining a pre-treatment
biopsy. Primary lung tumours, bleeding splenic tumours and bone tumours classically serve as examples of such
tumours as regardless of their precise nature, their treatment will invariably consist of lung lobectomy,
splenectomy and amputation / limb-sparing procedure respectively. In such cases, tumours are only examined by
the anatomopathologist after their excision, which is referred to as a post-treatment biopsy.
In most cases, however, a biopsy should be performed prior to treatment (pre-treatment biopsy) as the
knowledge of the nature of a lesion has often significant implications on its treatment. It also allows defining the
prognosis more precisely, which is important to inform owners and help them make decision. From the
surgeon’s point of view, a biopsy is useful for determining whether there is an indication for surgery and, if so,
how aggressive it should be. For lesions which can easily be excised widely due to their size and location, fine-
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needle aspirates may be sufficient obtain a crude diagnosis prior to excision. However, whenever the surgical
treatment is challenging or questionable, obtaining a precise diagnosis before embarking on it is essential.
Biopsy types
 Fine-needle aspirates
Fine-needle aspirates (FNAs) are not universally considered as biopsies as they do not preserve the structure of
tissues but only provide information on their cell population. Therefore, a precise tumour grading cannot be
obtained from FNAs, as grading partly relies on the examination of the structural relationship of the tumour and
surrounding structures. However, for several types of tumour, determination of the cellular type and changes can
provide enough information to guide treatment. Cytology is most useful in making the difference between a nonneoplastic lesion and a tumour, as well as in classifying a tumour as round-cell, epithelial or mesenchymal. A
crude estimation of the tumour’s likely aggressiveness may also be possible.
Fine-needle aspirates can be used for deep and superficial lesions. For deep and intracavitary lesions,
ultrasonographic guidance is useful to ascertain proper sampling of the relevant area.
The sensitivity of FNAs is better for round-cell (70%-100%) and epithelial (67%-98%) than for mesenchymal
(50%-61%) tumours, which do not easily exfoliate. For cutaneous and subcutaneous lesions, the cytological and
histopathological diagnoses were found to be in agreement in 91% of cases11.
 Needle-core biopsies
Needle-core biopsies are obtained with special needles (e.g. TruCut, Jamshidi) which can be manually or
automatically operated. Here again, the larger the diameter of the needle, the larger the biopsy sample and the
more accurate the histopathological diagnosis. The choice of the needle gauge therefore depends on the
characteristics of the mass to sample (organ involved, cavitary or not, etc.) as well as on the estimated risk for
inducing complications (haemorrhage, pneumothorax for pulmonary lesions for instance).
Needle-core biopsies can be taken percutaneously, either blindly for large, superficial and rather homogeneous
masses, or under ultrasonographic or laparoscopic guidance in all other cases. They can also be a rapid means of
obtaining a biopsy at surgery (e.g. kidney biopsies). When used percutaneously, these biopsy techniques give
little control on potential complications, especially haemorrhage.
Samples obtained with this technique are fragile and should be collected with care not to compromise their
diagnostic value. Gentle removal of the obtained tissues with the tip of a needle or small scalpel blade, or by
directly dipping the open biopsy needle in the formalin are two ways to collect tissue samples from the coreneedle. If dipped in formalin, the core-needle is flushed with sterile saline prior to be used again for another
biopsy on the same patient.
 Surgical biopsies
Surgical biopsies can be incisional or excisional. Incisional biopsies consist of sampling a portion of the tumour
to allow histopathological determination of its nature. Excisional (or post-treatment) biopsies consist of the
complete excision of the tumour prior to any histopathological diagnosis.
Excisional biopsies should only be chosen when knowledge of the tumour type or grade would not alter the
surgical dose required for resection, or when wide excision of the biopsy tract will easily be possible if
insufficient margins were to be obtained (Figure 1). Excessive and inappropriate use of marginal excisional
biopsies is a major cause for cancer treatment failure. If in doubt, perform fine-needle aspirates or an incisional
biopsy to ascertain that the subsequent resection plan is appropriate.
In general, it is best to biopsy at the junction between healthy and tumoral tissues, so that the pathologist can
study the characteristics of the tumour invasion in surrounding tissues. Also, many tumours are necrotic,
inflammatory or infected in their centre, which may lead to misdiagnosis. However, some tumours, such as
osteosarcoma, should be biopsied in their centre as they induce a strong reaction within surrounding tissues,
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which may lead to misdiagnosis is biopsied in periphery. In addition, if the surrounding tissues are essential for
later reconstruction, they should not be included in the biopsy. Overall, it is crucial not to jeopardise later
treatments by performing biopsies in a way that the biopsy tract can be later excised en-bloc with the tumour.
Therefore, when sufficient margins may be difficult to achieve, it is best to limit the incisional biopsies to the
tumour itself and not extend it to normal tissues, so that the required subsequent surgical resection is not made
larger.
When performing biopsies, incisions should not be made with electrocautery as it can create polarisation
artefacts which can hinder pathological evaluation of the tissues. This is especially important when the biopsies
taken are small. If cautery is needed for haemostasis, it should only be used once the biopsies have been
collected. Similarly, biopsies of friable tissues must be handled carefully and not crushed with the surgical
instruments, as it creates a crushing artefact with can also complicate or prevent pathological interpretation.
Once samples have been collected, they must be handled appropriately. If they are large, they must be incised
prior to be fixated, as formalin only penetrates the tissues 1 cm deep. The mass should therefore be sliced as
required, but only partially so that it remains cohesive and the pathologist can still have a clear understanding of
the orientation of the slices28 (Figure 2).
Figure 2: Large biopsy prepared for formalin fixation (d’après Henry28).
Tumour resection
As often as possible, tumours should be resected widely. Fear of not being able to close the resulting defect
should not limit the resection extension. It is better to leave a wound partially open but free of cancer than be
able to close it over residual tumour as a result of a more timid resection6.
Depending on the tumour type and size, 1 to 3-cm lateral margins are generally recommended. Tumour type and
grade are probably the most important factors for determination of the required surgical margins. Benign and
little aggressive malignant tumours can be resected with narrower margins than aggressive malignant tumours.
For instance, some surgeons advocate very wide (5-cm) lateral margins for excision of feline soft tissue
sarcomas29, which are extremely infiltrative tumours. In depth, depending on tumour type and size, one or two
fascial planes should be excised en-bloc with the tumour.
However, it seems that tumour size also influences the width of required margins: for a same tumour type, larger
tumours are associated with greater microscopic extension in surrounding tissues and therefore require wider
surgical margins than smaller tumours1.
If an adjuvant treatment is planned (radiotherapy especially), the surgical excision can be sometimes be more
conservative. Taking intraoperative pictures and leaving metallic vascular clips at the margins of excision can
then help the radiation oncologist plan subsequent treatments.
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Tumours should be manipulated as little and as gently as possible to prevent seeding of tumour cells. Ideally, the
tumour should not be approached or visualised and only healthy surrounding tissues be manipulated. Similarly,
the pseudocapsule of tumours must not be approached, as it is not only reactive tissue but mostly composed of
compressed tumour cells6, 30. Previous biopsy and drain tracts are excised en-bloc with the tumour. Whenever
possible, major arteriovenous pedicles should be ligated as early as possible in the procedure and veins be ligated
before arteries to limit the risk of macroscopic embolisation of tumour cells when the tumour is manipulated.
Tumours located in body cavities can usually not be excised en-bloc with surrounding tissues. They are therefore
directly exposed during surgery and should be wrapped in laparotomy swabs to limit the risk of coelomic
seeding as a result of capsule rupture of the affected organ during its manipulation31. Such tumours may be found
to be adherent to other organs or to the omentum for abdominal tumours. The portions of other organs being
adherent to the tumour should be excised en-bloc with it (e.g. omentum with splenic or digestive tumours, lung
with rib tumours, etc.).
Tumour should be considered and treated as infected tissues would: any instruments, gloves and drapes which
may have been contaminated by tumour cells should be changed. Likewise, any tissues having been in contact
with the tumour are treated as if they were part of the tumour itself: they should be resected with similar margins
whenever possible. The same instruments should not be used to excise, or biopsy, two separate masses.
Similarly, when closing the surgical wound, it is important to remember that any distant tissues used (skin flaps
for instance) will be considered contaminated if any subsequent treatment is required. For reconstruction, the use
of multifilament sutures is not recommended as it has been associated with higher tumour recurrence rates 1.
Using large skin flaps after tumour excision should also be avoided if the tumour margins are not known to be
clear. It could lead to tumour seeding and recurrence away from the initial site and prevent adjuvant radiotherapy
as the irradiation field would become too large. An option allowing skin flaps to be used in the face of uncertain
margins is to harvest the flap before starting the tumour resection. I regularly use this approach, which requires
careful surgical planning.
Similarly, drains should be used a rarely as possible as they provide a route for tumour seeding, should any
residual disease be left in the wound. All tissues along the draining tract would later need to be considered as
contaminated, which will increase the size of any revision surgery or radiotherapy field, should these be
necessary. If the use of drains are absolutely necessary, they should be placed wisely, keeping in mind the
potential future treatments, and as closely as possible from the surgical field. If a postoperative complication
requiring placement of a drain occurs once the margins are known to be free of tumour, drains can then be used.
Postoperative care should be anticipated. Enteral feeding tubes should be placed as appropriate. Similarly,
wound catheters can be left in surgical wounds, allowing regular instillation of local anaesthetics in the wound.
Even if the tumour has previously been biopsied, the entire piece of excision is fixed in 10 volumes of 10%
formalin for each volume of tissue5, 27, 28, 32 and submitted for pathology. Prior to fixation, margins can be marked
with India ink and the piece of excision be oriented using sutures, with appropriate explanations provided to the
pathologist. It is important to remember that the formalin will not penetrate tissues on more than 1 cm in depth.
Therefore, thicker samples must be sliced in 1-cm, similarly to a loaf of bread, leaving the deep (inked) margin
intact so that the sample remains in one piece and can still be orientated by the pathologist 1, 27, 28 (Figure 2).
After surgery
Postoperative care
Non-specifically, postoperative care of cancer patients include wound care, analgesia, nutritional support, and
medical care as appropriate. Depending on the tumour type, specific treatments of paraneoplastic treatments can
be required (e.g. blood levels monitoring and management of calcium in patients with hyperparathyroidism or of
glucose in patients with insulinomas, etc.). Depending on the procedure performed, specific management may be
required (chest drain for thoracic tumours, nursing on animals with spinal tumours, rehabilitation for amputees,
etc.).
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Adjuvant therapies: should the surgeon care?
Basic understanding of the principles of adjuvant therapies is essential for the surgeon working in cooperation
with medical and radiation oncologists. Non-surgical therapies of cancer are an extremely wide and deep field of
medicine, which can obviously not be covered here. Only a very brief presentation of the principles of
radiotherapy and chemotherapy, orientated towards their relevance for the surgeon, will be attempted.
Radiotherapy
Radiotherapy consists of using ionizing radiation to kill neoplastic cells. Different sources of radiation are
currently used: orthovoltage units, cobalt 60 units, linear accelerators, brachytherapy (implantation of a
radioactive source) and systemic radiation therapy (radioisotope injections). The SI unit for absorbed dose of
radiation is expressed is the gray (Gy). Radiotherapy is mostly a local (or loco-regional) treatment. As such it is
used to help in controlling local disease.
When the tumour and normal tissues are exposed to radiation, both free radical production and damage to the
cell DNA ensues. A third of the radiotherapy effect is mediated by damage to DNA, the rest being a result of free
radical production33. The majority of the DNA damage is mediated by oxygen free radicals, the production of
which is dependent on the oxygenation of tissues. Therefore, hypoxic tumours will tend to be less radiosensitive
than well-oxygenated tumours.
Cells with damaged DNA do not die immediately, but when attempting division. Some may even be able to
divide a few times before dying. Therefore, the effect of radiotherapy is not immediate and depends to a certain
extent on the division rate of tumour cells and growth rate of the tumour. Slow-growing tumours may take
months to show clinical response. This is also true for normal tissues: rapidly proliferating tissues rapidly show a
response to radiotherapy (acutely-, or early-, responding tissues), whereas slow-proliferating tissues show more
delayed reactions (late-responding tissues)34. The goal of radiotherapy is to destroy the reproductive capacity of
a tumour without excessive damage to surrounding normal tissues 34. Most adverse side-effects from radiotherapy
are caused by exposition of normal tissues to radiotherapy, which is currently unavoidable. These adverse sideeffects are however minimised by fractionating the dose of radiotherapy to administer into several smaller doses.
This is called fractionation. As a rule, potential complications of radiotherapy are more likely as the total
radiation dose, the dose per fraction and the size of the radiation field increase 6.
Different protocols, in terms of total dose and fractionation, can be used for administration of radiotherapy.
Briefly, the choice depends on the type and location of the tumour and on the aim of radiotherapy (palliative
versus definitive, i.e. with intent to cure). Hypofractionated and hyperfractionated protocols have different
indications and side-effects.
For the surgeon, radiotherapy is a powerful ally. Radiotherapy and surgery can be synergistic35, 36. Surgery is
most efficacious are eliminating the bulk of a tumour, but most often fails at detecting and removing microscopic
or small satellite nests of tumour cells around the tumour. On the contrary, radiotherapy is most efficient on
microscopic or small size disease, as the centre of bulky tumours is often hypoxic, and therefore radioresistant.
The combination of both treatments is therefore logical.
Radiotherapy can be administered either before surgery (neoadjuvant radiotherapy) or after surgery (adjuvant
radiotherapy). Each option has advantages and disadvantages1, 33.
A surgical scar is relatively hypoxic because of the vascular damage induced by surgery. As such, it is relatively
radioresistant. When radiotherapy is administered before surgery, no surgical scar is present and tissue hypoxia
is kept to a minimum, making tissues more radiosensitive. Also, the irradiated volume may be smaller for
preoperative radiotherapy than when surgery has been performed, as it may have required manipulation of more
distant tissues for reconstruction. Preoperative radiotherapy also potentially decreases viable tumour cell seeding
at surgery and it can in some instances reduce the size of the tumour which will facilitate surgical excision.
However, preoperative surgery can make tissues more fibrotic and more difficult to dissect. It can also make
intraoperative differentiation between tissues more difficult. Lastly, radiotherapy is detrimental to wound
healing, which it delays, and complications such as wound dehiscence are more likely when surgery is
performed on irradiated tissues. However, all these detrimental effects are mostly significant when
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hypofractionated protocols are used. When neoadjuvant radiotherapy is properly and carefully planned in view
of being followed by surgery, the effects on tissues are hardly perceptible at surgery and wound complication
rates are not significantly increased. The only potential exception may be oral tumours, which seems to be
associated with a higher rate of wound complications when surgery is performed after radiotherapy.
Conversely, postoperative radiotherapy decreases the risk of wound complication, but may have to be
administered to a larger field and to more hypoxic, and therefore more radioresistant tissues. In addition,
radiotherapy needs to be delayed by several weeks after surgery and potential residual tumour may have time to
proliferate.
Chemotherapy
In oncology, chemotherapy refers to the use of antineoplastic drugs. Unlike radiotherapy, chemotherapy is
mostly a systemic treatment. When chemotherapy is used in combination with surgery, it can be administered
before (neoadjuvant, or primary, chemotherapy) or after (adjuvant chemotherapy) surgery.
In veterinary oncology, a common indication for neoadjuvant chemotherapy is feline injection-site sarcomas.
The rationale for neoadjuvant chemotherapy is that, like radiotherapy, chemotherapy is most efficacious against
microscopic or small-size neoplastic disease. When administering neoadjuvant chemotherapy, it is hoped that
satellite nests of tumour will be killed, resulting in sterilisation of the main tumour margins. In addition, the main
bulk of tumour may shrink as a result of chemotherapy, which can facilitate its surgical excision.
Nonetheless, chemotherapy is most often used in veterinary oncology as an adjuvant treatment to control the
possible spreading of tumours with significant metastatic potential after the primary tumour has been addressed
by other treatments such as surgery and radiotherapy. Usually, in this indication, chemotherapy is started early
after surgery (most often 7 to 10 days postoperatively).
Although most chemotherapeutic agents experimentally impair wound healing6, 37, it is of little, if any, clinical
relevance and should not be a concern for the surgeon.
The main implication of chemotherapy for the surgeon is that patients on chemotherapy have an increased risk of
developing infections. Therefore, any procedure increasing the risk of postoperative infection in patients destined
to have chemotherapy must be performed cautiously. For instance, the use of massive implants, such as large
prosthetic meshes for extensive wound reconstruction, should only be resorted to when no other option is
available.
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