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The

Veterinary Journal
The Veterinary Journal 174 (2007) 344–350
www.elsevier.com/locate/tvjl

Cattle with thymic lymphoma and haematoma of the ventral neck:


A comparison of findings
a,*
U. Braun , B. Hauser b, S. Meyer a, B. Feller a

a
Department of Farm Animals, University of Zürich, Winterthurerstrasse 260, CH-8057 Zürich, Switzerland
b
Institute of Veterinary Pathology, University of Zürich, Winterthurerstrasse 260, CH-8057 Zürich, Switzerland

Abstract

The goal of the present paper was to establish criteria for the differentiation of thymic lymphoma and haematoma of the ventral neck
in cattle. Four cattle with thymic lymphoma and seven with haematoma of the ventral neck underwent physical, haematological, bio-
chemical and ultrasonographic examinations as well as histological evaluation of a biopsy specimen. All of the animals had firm non-
painful swellings, which were no warmer than normal and extended from the pharyngeal region to the thoracic inlet. A diagnosis could
not be established based on the results of physical examination and palpation of the swellings. Animals with a haematoma had a shorter
history of being ill compared to those with thymic lymphoma. In patients with a haematoma, anaemia was present, the heart rate was
elevated and the haematocrit was decreased, but not in cattle with thymic lymphoma. A tentative diagnosis was made on the basis of a
macroscopic evaluation of the biopsy samples, which were dark red and firm in cattle with a haematoma. All cases of malignant thymic
lymphoma were confirmed by histological examination of a biopsy sample. Ultrasonography did not help to differentiate between
haematoma and thymic lymphoma. All animals with thymic lymphoma and three of those with a haematoma were euthanased. The four
remaining animals with a haematoma were treated successfully.
 2006 Elsevier Ltd. All rights reserved.

Keywords: Cattle; Thymus; Malignant lymphoma; Lymphosarcoma; Haematoma

1. Introduction tumours on the ventral aspect of the neck cannot be accu-


rately differentiated by physical examination and palpation
There are various causes of diffuse swelling in the ventral alone. Moreover, the prognosis varies: that for thymic lym-
neck region in cattle. A differential diagnosis would include phoma is grave, whereas for a haematoma the prognosis is
phlegmon (an acute suppurative inflammation affecting the good. The goal of the present paper was to provide criteria
subcutaneous connective tissue), abscessation, oedema, that would aid in the differentiation of the two disorders.
haematoma and neoplasia (Radostits et al., 2000a; Stöber,
2002). Examination and palpation of the swelling are often 2. Materials and methods
helpful: a warm painful swelling is usually phlegmon
(Gründer, 1990); a circumscribed fluctuating swelling could 2.1. Animals
well be an abscess; and a swelling that pits with pressure
indicates oedema (Radostits et al., 2000b). From 1st January 1985 to 31st March 2005, 11 cattle
In many cases, a definitive diagnosis cannot be made were referred to the Department of Farm Animals, Univer-
based on clinical examination alone because certain diseases sity of Zürich, for further diagnostic work-up. All of the
have similar findings. In our experience, haematomas and animals had a firm non-painful swelling on the ventral sur-
face of the neck. The swelling was no warmer than normal
*
Corresponding author. Tel.: +41 44 6358241; fax: +41 44 6358904. and extended from the pharyngeal area to the thoracic
E-mail address: ubraun@vetclinics.unizh.ch (U. Braun). inlet. Based on our findings, a diagnosis of malignant

1090-0233/$ - see front matter  2006 Elsevier Ltd. All rights reserved.
doi:10.1016/j.tvjl.2006.07.024
U. Braun et al. / The Veterinary Journal 174 (2007) 344–350 345

thymic lymphoma was made in four animals (Nos. 1–4). A 3.5 MHz linear transducer (Hitachi Medical Systems)
These ranged in age from six months to three years and was used for the examinations.
of the Swiss Braunvieh, Holstein–Friesian, Simmental
and Jersey breeds. The remaining animals (Nos. 5–11), 2.5. Histological examination
which were diagnosed with a haematoma, ranged in age
from 3–16 months and were of the Swiss Braunvieh (5), With one exception (No. 6), a biopsy sample of the
Simmental (1) and Limousin (1) breeds. swelling was collected from each of the animals. The swell-
ing was scanned ultrasonographically to choose a biopsy
2.2. History site with no blood vessels. The skin over the site was anaes-
thetised using 2% lidocaine containing hyaluronidase (Stre-
The animals with thymic lymphoma were referred uli, Uznach). A Bard magnum core high speed biopsy
because of swelling in the ventral neck region, which punch with an appropriate size needle (Bard Truguide
according to the owners had been present for one day, Coaxial, 14G · 16 cm; Bard Media S.A.) was used to col-
two, six or 14 weeks. In all of the animals, the swellings lect the biopsy sample, which was immediately placed in
progressively increased in size. Two of these cattle also 10% formalin solution for 24–48 h. Histological sections
had ruminal tympany. All animals had been treated with were prepared, stained with haematoxylin and eosin stain
various topical medications, two had also received antihis- and examined microscopically.
tamines, and one had been given procaine penicillin and
dexamethasone. 2.6. Treatment, euthanasia and post-mortem examination
Six of the seven animals with a haematoma had been
referred because of a swelling on the ventral neck which Animals with thymic lymphoma were euthanased and
had been present for 1–2 days. One other animal was underwent a post-mortem examination. Of the seven ani-
referred with a tentative diagnosis of cardiac disease mals with a haematoma, three (Nos. 5–7) were also euthan-
because of marked distension of the jugular veins but no ased at the owners’ request and underwent post-mortem
swelling had been seen. In five animals, the main sign examination but the remainder (Nos. 8–11) were success-
was ruminal tympany with a dorsal gas cap that recurred fully treated and discharged.
after passing a stomach tube. Five animals were anorexic.
All of the animals had been treated with various medica- 2.7. Statistics
tions such as antibiotics, corticosteroids, metamizole, ami-
nophenazone, antihistamines and topical creams. Statistical calculations were carried out by means of the
calculation program SPSS/PC+ 4.0, according to the meth-
2.3. Clinical, haematological and biochemical examinations ods of Norusis (1990). Frequencies, mean and SD were cal-
culated. The heart rate, respiratory rate, rectal temperature
Each animal underwent a thorough clinical examination and all haematological values were compared with
as described by Rosenberger (1979). In addition, the hae- ANOVA.
matocrit and leukocyte count, and the serum concentra-
tions of total protein, fibrinogen, bilirubin, urea, sodium, 3. Results
chloride and calcium, and the activities of the enzymes c-
glutamyl transferase (c-GT), aspartate aminotransferase 3.1. Clinical findings
(AST), glutamate dehydrogenase (GLDH) and sorbitol
dehydrogenase (SDH) were measured. The haematocrit, The general condition was normal or mildly abnormal in
total leucocyte count and concentrations of total protein, six animals (Nos. 1, 3, 5, 9, 10 and 11) and moderately to
and fibrinogen were determined in EDTA blood (Braun severely abnormal in five (Nos. 2, 4, 6, 7 and 8; Table 1).
et al., 1989). The concentrations of bilirubin, urea, calcium, The body condition was good in six animals (Nos. 1, 5,
inorganic phosphorus, magnesium, sodium, chloride and 7, 8, 9 and 11) and moderate in four (Nos. 3, 4, 6 and
potassium, and the activities of c-GT, AST, SDH and 10). One animal (No. 2) was emaciated and milk yield
GLDH were determined in serum using a Cobas Integra was severely decreased to a few litres per day.
700 Analyzer (Roche Diagnostics) and Roche reagents All animals had a firm non-painful swelling on the ven-
under conditions defined by the International Federation tral surface of the neck, which was no warmer than normal
of Clinical Chemists at 37 C. Blood gas analysis was car- and extended from the pharyngeal region to the thoracic
ried out on a jugular venous blood sample. Cow 2 was inlet. Thymic lymphoma and haematoma could not be dif-
examined for enzootic bovine leucosis (ELISA). ferentiated based on the results of physical examination
and palpation (Figs. 1 and 2). There was marked distension
2.4. Ultrasonographic examination of both jugular veins in two animals (Nos. 10 and 11) and
one jugular vein in one (No. 7). Ruminal tympany and
Ultrasonography of the swelling was carried out in two atony were seen in all the animals with thymic lymphoma
cattle with thymic lymphoma and four with a haematoma. (Fig. 3), whereas only five with a haematoma (Nos. 5, 7,
346 U. Braun et al. / The Veterinary Journal 174 (2007) 344–350

Table 1
Clinical findings in four cattle with thymic lymphoma (Nos. 1–4) and seven cattle with a haematoma on the ventral neck (Nos. 5–11)
Animal Breed/age Clinical findings
1 Swiss Braunvieh/11 months RT = 39.7 C, HR = 84, RR = 20, reduced ruminal motility, ruminal tympany with dorsal
gas cap, positive withers’ pinch, both iliac lymph nodes markedly enlarged on transrectal
palpation
2 Holstein Friesian/3 years Moderately abnormal general condition, bruxism, thin body condition, dull coat,
enlargement of both prescapular lymph nodes, RT = 39.3 C, HR = 60, RR = 24,
distension of jugular veins, ruminal atony and tympany, reduced intestinal motility,
distension of rumen on transrectal palpation
3 Jersey/6 months Moderate body condition, RT = 38.9 C, HR = 80, RR = 24, stenosis sound on inspiration,
ruminal atony and tympany, distension of jugular veins
4 Simmental/1.5 years Moderately abnormal general condition and moderate body condition, RT = 39.2 C,
HR = 68, RR = 44, increased breath sounds and crackles, enlarged left prescapular lymph
node, distension of jugular veins, ruminal atony and tympany, regurgitation of ingested hay
5 Swiss Braunvieh/3 months Mildly abnormal general condition, RT = 39.0 C, HR = 120, RR = 20, injected scleral
vessels, left popliteal lymph node enlarged, ruminal atony and tympany
6 Swiss Braunvieh/3.5 months Severely abnormal general condition, moderate body condition, shaking, enophthalmus,
RT = 40.0 C, HR = 136, RR = 28, abdominal lift during respiration, dyspnoea, very pale
mucous membranes, wheezes, ruminal atony
7 Swiss Braunvieh/10 months Severely disturbed general condition, dry muzzle, uraemic breath, RT = 38.6 C, HR = 112,
RR = 32, very pale mucous membranes, distension of left jugular vein, left prescapular
lymph node enlarged, ruminal atony and tympany, positive tests for reticular foreign body
8 Limousin, 3 months Moderately abnormal general condition, stenotic sounds on inspiration, RT = 39.6 C,
HR = 120, RR = 28, pale mucous membranes, normal ruminal motility
9 Swiss Braunvieh/7 months Mildly abnormal general condition, arched back, RT = 39.7 C, HR = 84, RR = 28,
ruminal atony and tympany
10 Swiss Braunvieh/16 months Mildly abnormal general condition, moderate body condition, mild enophthalmus, reduced
skin turgor, RT = 39.2 C, HR = 88, RR = 20, ruminal atony and tympany, positive
withers’ pinch test, distension of both jugular veins
11 Simmental/3 months Mildly abnormal general condition, RT = 39.2 C, HR = 88, RR = 32, strong ruminal
contractions, ruminal tympany, distension of both jugular veins
Only those findings that deviate from physiological conditions are presented.
RT = Rectal temperature, HR = Heart rate, RR = Respiratory rate.

Fig. 1. A 1.5-year-old Simmental heifer (No. 4) with swelling of the


ventral neck due to thymic lymphoma. A metal clip was used to close the
biopsy site.

9, 10 and 11) had ruminal tympany with normal or no


ruminal motility. In three animals with thymic lymphoma
and two with a haematoma, there was enlargement of cer-
tain lymph nodes, which included both iliac lymph nodes Fig. 2. A three-month-old Limousin calf (No. 8) with swelling of the
(No. 1), one popliteal lymph node (Nos. 5 and 7) and ventral neck due to a haematoma. The left jugular vein is markedly
one (No. 4) and both prescapular lymph nodes (No. 2). distended.
U. Braun et al. / The Veterinary Journal 174 (2007) 344–350 347

patients with thymic lymphoma. In the fourth animal


(No. 4), there was a leukocytosis (15 100 leukocytes/lL)
with absolute neutrophilia (11 250 segmented neutro-
phils/lL) and a left shift. Of the animals with a haema-
toma, five (No. 5, 6, 7, 8 and 11) had a neutrophilia
and left shift. In these, the total leukocyte count ranged
from 18 800 to 43 500 leukocytes/lL with 12 784–
39 585 segmented neutrophils/lL. The remaining blood
variables did not differ significantly between the groups
and were in the normal ranges with the exception of
one animal with thymic lymphoma (No. 4). That animal
had increased activities of c-GT, GLDH (234 U/L; nor-
Fig. 3. An 11-month-old Swiss Braunvieh calf (No. 1) with swelling of the
mal range, 15–25 U/L) and SDH (164 U/L; normal range,
ventral neck due to thymic lymphoma, and ruminal tympany. 3.0–7.5 U/L). In one animal with a haematoma (No. 6),
the total protein was slightly reduced (58 g/L; normal
range 60–80 g/L). Serological testing for enzootic bovine
The heart rate in animals with a haematoma was signif- leucosis was negative in cow No. 2.
icantly higher (mean [SD] 107 [20.2] bpm) than in animals
with thymic lymphoma (73 [11.0] bpm; difference 3.3. Ultrasonographic findings
P < 0.05, ANOVA). Of the animals with thymic lym-
phoma, only one (No. 1) had a mild increase in heart rate In the two patients with thymic lymphoma (Nos. 3 and
(84 bpm), whereas all the animals with a haematoma had a 4) that underwent ultrasonography, the swelling appeared
mild to marked elevation in heart rate (84–136 bpm). The as a heterogeneous hypoechogenic mass with irregular
respiratory rate was normal or mildly increased in all ani- echogenic focal lesions (Fig. 4). There were no pockets of
mals, and did not differ significantly between the two fluid within the mass. In all animals with a haematoma
groups. There was no significant difference in rectal tem- (Nos. 4–11) that were examined ultrasonographically, there
perature between groups. The rectal temperature was was at least a trace of a capsule around the swelling. The
increased in three animals with thymic lymphoma (Nos. swelling appeared heterogeneous with hypoechogenic and
1, 2 and 4; range, 39.2–39.7 C) and in five with a haema- echogenic areas. In three of the animals (Nos. 9, 10 and
toma (Nos. 6, 8, 9, 10 and 11; range, 39.2–40.0 C). Other 11), there were a number of anechogenic foci of varying
signs included pale mucous membranes in three animals diameter (Fig. 5).
with a haematoma (Nos. 6, 7 and 8) and regurgitation in
one patient with thymic lymphoma (No. 4). The faeces
were normal in all the animals. Urine samples assessed
using a test strip (Combur9-Test, Roche) were also normal.

3.2. Haematological and biochemical findings

With the exception of two animals with thymic lymphoma


(Nos. 3 and 4), the haematocrit was decreased in all patients
and ranged from 0.20–0.31 L/L (normal range, 0.30–0.33 L/
L). Animals with a haematoma had a significantly lower hae-
matocrit (23.1 [2.73]%) than those with thymic lymphoma
(29.3 [1.71]%; P < 0.01). The serum concentration of fibrin-
ogen in animals with a haematoma was significantly higher
(7.3 [1.50] g/L) than those with thymic lymphoma
(5.0 [1.15] g/L; P < 0.05). The activity of c-GT was higher
in animals with thymic lymphoma (51.3 [36.69] U/L) than
those with a haematoma (13.7 [2.87] U/L; P < 0.05). Three
animals with thymic lymphoma (Nos. 1, 2 and 4) had higher
than normal c-GT values, which ranged from 28 to 97 U/L
(normal range, 10–25 U/L), whereas all the patients with a
haematoma had normal values.
There were no significant differences in the total leuko-
cyte count and differential cell count between the two Fig. 4. Ultrasonogram of a thymic lymphoma in a 1.5-year-old Simmental
groups. The total leukocyte count (5000–10 000 leuko- heifer (No. 4). The tumour is hypoechogenic with echogenic foci. 1 – Skin,
cytes/lL) and differential cell count were normal in three 2 – Lymphoma, 3 – Echogenic foci. Left is cranial, right is caudal.
348 U. Braun et al. / The Veterinary Journal 174 (2007) 344–350

large nuclei. The nuclei were round or slightly notched


and had fine, sometimes clumped, chromatin usually with-
out visible nucleoli. The mitotic rate was low in two
patients and high in two others. The biopsy samples from
the animals with a haematoma were dark red and firm
and were macroscopically indicative of a haematoma. His-
tologically, massive numbers of erythrocytes were seen
within a net of contracting fibrin. Neutrophils had an irreg-
ular distribution and sometimes pyknotic nuclei (Fig. 7).

3.5. Euthanasia and post-mortem examination of animals


Nos. 1–7

In all animals with thymic lymphoma, the thymus had


white nodular lesions with a greasy appearance (Fig. 8).
Similar lesions were also seen in the mediastinal and iliac

Fig. 5. Ultrasonogram of a haematoma on the ventral neck of a seven-


month-old Swiss Braunvieh calf (No. 9). The haematoma is well delineated
from the surrounding tissue and appears heterogeneous; the haematoma is
hypoechogenic with anechogenic areas. 1 – Skin, 2 – Haematoma, 3 –
Anechogenic cavity. Left is cranial, right is caudal.

3.4. Biopsy findings

A diagnosis of malignant thymic lymphoma was con-


firmed by the histological examination of a biopsy sample Fig. 7. Histological section of a haematoma: there is a dense accumulation
of erythrocytes and scattered neutrophils with slightly pyknotic nuclei. In
in all the animals with thymic lymphoma. Histologically, the upper left of the photomicrograph are bands of retracting and
there was a diffuse homogeneous uniform population of intensely eosinophilic fibrin (400· magnification, haematoxylin and eosin
lymphocytes with relatively small (Fig. 6) or, in one case, staining, No. 7).

Fig. 8. Thymus, lungs, heart and liver of an 11-month-old Swiss


Fig. 6. Histological section of thymic lymphoma: there is diffuse infiltra- Braunvieh heifer (No. 1) with thymic lymphoma. The thymus (to the
tion of small lymphocytes, and the nuclei have dense fine chromatin (400· right) is markedly enlarged and has neoplastic changes. The liver contains
magnification, haematoxylin and eosin staining, No. 3). a few round white neoplastic nodules.
U. Braun et al. / The Veterinary Journal 174 (2007) 344–350 349

lymph nodes and liver of patient No. 1. Neoplastic lesions in our patients and was interpreted by one of the referring
were seen in the mediastinal lymph nodes of patient No. 3 veterinarians as a sign of right-sided cardiac insufficiency.
and in the spleen, mesenteric lymph nodes and intestinal A haematoma is the accumulation of blood perivascu-
wall of patient No. 4. larly in the subcutaneous, subserosal, intermuscular or
In the three animals euthanased with a haematoma intramuscular connective tissue due to a lesion in a blood
(Nos. 5, 6 and 7) a massive amount of blood was seen in vessel (Gründer, 2002). Subcutaneous haematomas, which
the ventral neck region. There was no evidence of thymic occurred in patients Nos. 5–11, are usually the result of
neoplasia in any of these patients. blunt trauma resulting from fighting, falls, running into
obstacles or entrapment in a neck chain or head gate
3.6. Treatment of patients with a haematoma (No. 8–11) (Gründer, 2002). All but one cow with a haematoma were
housed in free stalls, which provide many opportunities for
Animal No. 8 was treated with a warm linseed poultice blunt trauma. However, it is not usually possible to identify
placed onto the neck for 11 days. After this, the haema- the injured blood vessel.
toma was lanced surgically, and the patient received There were no differences between the two groups with
7 mg/kg amoxicillin (Clamoxyl, Pfizer) IM once daily for respect to the age and breed of the animals and the physical
five days before being discharged from our clinic. Animal appearance of the swelling. All animals with thymic lym-
No. 9 received 7 mg/kg amoxicillin IM once daily for five phoma were between four months and four years of age.
days because infection of the haematoma was suspected. Four of the seven cattle with a haematoma were only 3–
In addition, the swelling was treated topically with a hepa- 3.5 months old, an age that is not typical for thymic
rin-containing cream (Hirudoid forte, Sankyo Pharma) lymphoma. With the exception of a three-month-old calf
every 12 h for nine days after which the patient was dis- (Hatfield et al., 1986), thymic lymphoma has not been
charged. In animals Nos. 10 and 11, the swelling was also reported in cattle <4 months old. Three of our four
treated topically with the same heparin-containing cream, patients with thymic lymphoma had been ill for >2 weeks,
and the cows were discharged after six and seven days, whereas all those with a haematoma had been sick for only
respectively. Treatment of animals Nos. 9, 10 and 11 1–2 days. Whereas signs of a haematoma occur rapidly,
resulted in a marked reduction in the size of the swelling those of thymic lymphoma are more insidious. Because
and normalisation of appetite and general condition during of the acute anaemia in patients with haematoma, the heart
hospitalisation. A follow-up via telephone revealed that all rate was significantly higher compared with patients with
the animals had an uncomplicated recovery with complete thymic lymphoma. In the latter, the heart rate was
cure. <85 bpm, whereas in 6/7 cattle with a haematoma, it
exceeded 85 bpm; in four, it was >100 bpm.
4. Discussion An increase in metabolic activity associated with neopla-
sia was most likely the cause of an increase in rectal tem-
Bovine lymphoproliferative diseases include enzootic perature in three animals with thymic lymphoma.
leukosis, caused by bovine leukemia virus, and three spo- Resorptive processes after haemorrhage may have been
radic forms, namely juvenile multicentric lymphoma, cuta- the cause of an increase in rectal temperature in five ani-
neous lymphoma and thymic lymphoma (Radostits et al., mals with a haematoma. In three patients with thymic lym-
2000a; Stöber, 2002). Recently, bovine leukaemia virus phoma, but in only two of those with haematoma, one or
was also detected in tissues from a heifer diagnosed with two peripheral lymph nodes were enlarged.
sporadic thymic lymphosarcoma by in situ polymerase All of the animals were anaemic; however, the anaemia
chain reaction (Duncan et al., 2005). Thymic lymphoma was more severe in patients with a haematoma. Five of
has been described repeatedly in the past 20 years (Hatfield seven animals with a haematoma had a haematocrit of
et al., 1986; Holmes et al., 1990; Angel et al., 1991; Mat- <25%, whereas none of the patients with thymic lymphoma
thews et al., 1992; Thorp et al., 1994; Alexander et al., had a haematocrit this low. Interestingly, in three animals
1996; De Vliegher et al., 2000). with thymic lymphoma, the activity of c-GT was higher
Thymic lymphoma occurs in cattle four months to four than normal; the activity of this enzyme was within normal
years of age (Stöber, 2002), although it is most common ranges in the animals with a haematoma. This was possibly
between the ages of six months and two years, and studies due to impaired blood flow not only from the cranial but
in France have determined a hereditary predisposition for also from the caudal vena cava to the heart, which resulted
this disease (Parodi et al., 1989; Dacosta et al., 1991). Malig- in chronic congestion of the liver (Stöber, 2002) and an
nant lymphoma affects the thymus and adjacent lymph increase in c-GT activity. Surprisingly, there was no signif-
nodes. The main clinical sign is a firm swelling along the ven- icant difference in the total leukocyte count and differential
tral aspect of the neck, which was also seen in our patients. cell count between the two groups. None of the animals
Compression of the oesophagus by the tumour may result in with thymic lymphoma had haematological results indica-
ruminal tympany, which is often the first sign. When the tive of leukaemia (Stöber, 2002). The five animals with a
tumour impinges on the cranial vena cava, distension of haematoma had a neutrophilia and left shift, which was
the jugular veins may occur. Jugular distension was seen due to stress as well as resorptive processes.
350 U. Braun et al. / The Veterinary Journal 174 (2007) 344–350

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phoma and haematoma based on the results of ultrasonog- ical findings in cattle with dilatation and torsion of the caecum.
Veterinary Record 125, 396–398.
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appearance. The only difference was that the haematomas A.L., 1991. Epidemiological and pathological studies of a familial
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respect to length of illness, heart rate, haematocrit and paresis in a heifer. British Veterinary Journal 146, 91–92.
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