ttp://www.bsava.

com CASE REPORT

Pneumopericardium,
pneumomediastinum, pneumothorax
and pneumoretroperitoneum
complicating pulmonary metastatic
carcinoma in a cat
V. Greci*, A. Baio*, L. Bibbiani*, E. Caggiano*, S. Borgonovo†, D. Olivero‡, P. M. Rocchi* and V. Raiano*

*Ospedale Veterinario Gregorio VII, Piazza di Villa Carpegna 52, 00165 Roma, Italia
†Alzaia Naviglio Grande, 40, 20144, Milano, Italia
‡BiEsseA s.r.l., 20129 Milano, Italia

This report describes a case of severe spontaneous tension pneumopericardium with concurrent
pneumomediastinum, pneumothorax and retropneumoperitoneum in a cat presenting with dyspnoea
and signs of cardiac tamponade secondary to metastatic pulmonary carcinoma. Spontaneous
pneumopericardium is an extremely uncommon condition consisting of pericardial gas in the absence
of iatrogenic/traumatic causes. In humans, it has been described secondary to pneumonia or lung
abscess and very rarely secondary to pulmonary neoplasia.

Journal of Small Animal Practice (2015) 56, 679–683

DOI: 10.1111/jsap.12366
Accepted: 16 March 2015; Published online: 11 May 2015

INTRODUCTION had bronchopulmonary diseases (Brown & Holt 1995, Parent

Pneumopericardium is defined as the collection of air within the
pericardial cavity that usually indicates an abnormal communica-
tion between the pericardial sac and the adjacent air-containing
structure (Maki et al. 1999, Barquero-Romero et al. 2005).
In humans, the main causes of pneumopericardium are alveolar
rupture, baro-traumas and blunt chest trauma; cardiac surgery and
oesophageal or gastric perforation represent other potential causes.
Spontaneous pneumopericardium is extremely uncommon and
consists of pericardial gas in the absence of iatrogenic or traumatic
causes. Spontaneous pneumopericardium can be caused by direct
extension from adjacent inflammatory, infectious or neoplastic pro-
cesses or very rarely by pericardial infection by gas-forming organ-
ism (Maki et al. 1999, Luthi et al. 2003, Taniyama et al. 2013).
Spontaneous pneumopericardium secondary to pulmonary
neoplasia is an extremely rare condition (Harris & Kostiner 1975,
Baydur & Gottlieb 1976, Rongé et al. 1983, Kim et al. 2000).
Only seven cases of pneumopericardium have been previ-
ously described including two cases in cats that were secondary
to positive-pressure ventilation, two cases in dogs hit by a car
and three cases of spontaneous pneumopericardium in dogs that
& Rozanski 1998, Lecrerc et al. 2004, Johnson-Neitman et al.
2006, Orlando 2009, Agut et al. 2010, Borgonovo et al. 2014).
Carcinomas are the most common neoplasm of the feline
mammary gland, representing 80–90% of cases; mammary
gland carcinomas frequently metastasize to the lungs (Madewell
& Theilen 1987, Forrest & Graybush 1998).
To the best of the authors’ knowledge, this is the first report of
spontaneous tension pneumopericardium with concurrent pneu-
momediastinum, pneumothorax and pneumoretroperitoneum
secondary to bronchopulmonary metastatic mammary gland
carcinoma in a cat.
CASE HISTORY
An 11-year-old female spayed domestic shorthaired cat was
referred for bronchoscopy because of bronchopneumopathy
of 2 weeks duration that was unresponsive to antibiotics. The
cat was an indoor cat, had no previous medical history and had
tested negative for feline immunodeficiency virus (FIV) and
feline leukaemia virus (FeLV). Thoracic radiographs undertaken
2 weeks before presentation were not available.

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 V. Greci et al.

On presentation, the cat was severely dyspnoeic with an ele-
vated respiratory rate (>80 breaths/minute), weak femoral pulses
with decreased heart rate (140 bpm), tacky but pink mucous
membranes and normal rectal temperature (38°C). The heart
and lung sounds were muffled.
The cat was administered flow-by oxygen (1 L/min) and sedated
with 0·2 mg/kg butorphanol (Nargesic ACME); 10 minutes later
an intravenous catheter was placed and a venous gas analysis
revealed respiratory acidosis [pH: 7·15 (7·351–7·463), pCO2 55
(30·8–42·8) mmHg and HCO3 25·6 (14–22) mmol/L]. The cat
was started on an intravenous crystalloid solution (Normosol®;
HOSPIRA) infusion at 30 mL/hour. An electrocardiograph
showed sinus bradycardia with flattened T waves.
A right lateral and a dorsoventral thoracic radiograph were
taken which showed severe pneumopericardium, pneumomedi-
astinum, minimum pneumothorax, increased alveolar-interstitial
pattern of the caudal lung lobes and pneumoretroperitoneum
(Fig 1A, B).
Cardiac ultrasound revealed a large amount of air in the peri-
cardial sac impairing visualisation of the right chambers; how-
ever, the left ventricle looked underloaded likely because of
reduced right output from the pneumopericardium suggesting
cardiac tamponade.
Given the clinical status, the radiographic and cardiac ultra-
sound findings, a diagnosis of cardiac tamponade secondary
to tension pneumopericardium was made. Pericardiocentesis
yielded more than 500 mL of air. The femoral pulses improved
but the cat remained dyspnoeic. A subsequent dorsoventral chest
radiograph showed reduction of the pneumopericardium and
increased pneumothorax.
The owner was informed of the guarded prognosis and opted
for further diagnostic work-up. The cat was anaesthetised and a
chest drain tube with Heimlich valve (BD and Company) was
placed.
Computed tomography was subsequently undertaken and imag-
ing findings were consistent with severe/end-stage degenerative
bronchopulmonary or infiltrative neoplastic disease (Fig 2A–F).
The owner elected for euthanasia but agreed to necropsy.
On gross examination, a 2-mm mammary nodule was detected
on the right inguinal mammary gland. Abdominal examination
was unremarkable. At the opening of the thorax, free air was lib-
erated and several air blebs (1–5 mm) were found in the thoracic
wall layers and pleurae; the lungs appeared decreased in volume,
thickened and of marbled appearance. Moderate pneumoperi-
cardium was still present and the pericardium showed foci of
recent haemorrhages likely secondary to the pericardiocentesis
(Fig 3A–D). No bronchial-pericardial or bronchial-pleural com-
munications were disclosed.
Samples from each affected and normal organs were fixed
in 10% buffered formalin and submitted for histopathological
examination.
Microscopy of the mammary nodule was characterised by a
proliferation of atypical epithelial cells of the intralobular duct-
ules with scant and clear cytoplasm, dysmetric and vesicular
nuclei with prominent nucleoli; these elements appeared irregu-
larly arranged in rows superimposed to form pseudotubuli with
1 to 2 mitoses per field (40×). Minimal surrounding reactive des-
moplasia, blood vessel congestion and mixed inflammatory cell
infiltration were noted.
Microscopy of the lungs was characterised by a multifocal
proliferation of cuboidal to columnar epithelial cells with scant
eosinophilic cytoplasm and hypochromic nuclei with 1 to 2
prominent nucleoli; normal ciliated epithelial cells were not dis-
closed. These cells were irregularly arranged in overlapping rows
resembling a honeycomb-like pattern, often with thin papillary
projections; two mitoses per field (40×) were evident. Numer-
ous neoplastic thromboemboli, new vascularisation and diffuse
micro-haemorrhages were also evident. The bronchi were filled
with amorphous content.
Microscopy of the pericardium showed irregularly hyperplastic
mesothelial cells lining the serosa layer and multiple areas of ero-
sion. The stromal fibroblasts were slightly reactive because of
the presence of a moderate lymphoplasmacellular inflammatory
infiltration. The vessels were hyperaemic and congested.
Histopathological diagnosis was consistent with a well-
differentiated simple tubular mammary gland carcinoma,

(A) (B)

FIG 1. (A) Right lateral view of the chest: note the elevated cardiac silhouette and the pericardium highlighted by free air within the pericardial
sac (black arrows), the evidence of the brachial venous plexus, the alveolar interstitial pattern in the caudal and accessory lung lobes and the
focal increased radiolucency caudally and dorsally; note the presence of pneumoretroperitoneum in the visible portion of the abdominal cavity;
(B) Dorsoventral view of the chest: note the severe pneumopericardium (black arrows), the minimal pneumothorax (white arrow) on the right caudal
aspect of the thorax and the increase in the alveolar-interstitial pattern of the right lung lobes

680 Journal of Small Animal Practice • Vol 56 • November 2015 • © 2015 British Small Animal Veterinary Association
 Pneumopericardium and lung tumour

(A) (B)

(E)
(C) (D)

(F)

FIG 2. Computed tomography findings: (A) Transverse scan at T7 level (bone algorithm, lung window): note the severe pneumopericardium, the moder-
ate bilateral pneumothorax (white arrow) and medial pneumomediastinum; the lungs show bilateral increased alveolar-interstitial pattern and radioden-
sity especially on the right side; a chest drain tube is detectable on the left and right side; (B) Transverse scan at the level of T10 (bone algorithm,
lung window): note the severe and diffuse atelectasis and consolidation of the right caudal lung lobe because of the presence of multiple disseminated
and confluent radiopacities; pneumothorax and pneumomediastinum are evident; a chest drain tube is detectable on the left and right side; (C) dorsal
multi-planar reconstruction (MPR) at thoracic level (bone algorithm, lung window): note the severe atelectasis of the right lung lobe, the presence of
pneumothorax and pneumomediastinum and the presence of the chest drain tubes; (D) dorsal MPR at thorax level (bone algorithm, lung window): note
the severe pneumopericardium and the minimal pneumomediastinum; (E) transverse scan of the abdomen at the level of the right kidney (soft tissue
algorithm, abdomen window): note the pneumoretroperitoneum; (F) sagittal MPR at the level of the thorax and abdomen (soft tissue algorithm, abdo-
men window): note the pneumopericardium, pneumothorax, pneumomediastinum and retropneumoperitoneum

moderately differentiated broncho-alveolar papillary adenocarci- DISCUSSION

noma and erosive pericarditis.
Immunostaining with thyroid transcription factor-1 (TTF-1;
clone 8G7G3/1; dilution 1/200; Dako) of multiple lung sections
was negative suggesting a mammary metastatic origin of the
bronchopulmonary tumour.
Pneumopericardium is an uncommon condition in small ani-
mals and only seven cases have been so far described. Three
cases developed spontaneous pneumopericardium secondary to
bronchopulmonary diseases but none had pulmonary neoplasia.

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 V. Greci et al.

(A) (B)

(C) (D)

FIG 3. (A) Different sized blebs (1–3 mm) in the thoracic muscular wall; (B) different sized blebs (3–6 mm) on the pleurae and marble aspect of the
lung lobes; (C) marble aspect of the lungs; (D) note the residual pneumopericardium and the foci of haemorrhages

To the best of the authors’ knowledge, this is the first case of
pneumopericardium described in association with pulmonary
neoplasia in cats or dogs (Brown & Holt 1995, Parent & Rozanski
1998, Lecrerc et al. 2004, Johnson-Neitman et al. 2006, Orlando
2009, Agut et al. 2010, Borgonovo et al. 2014).
The case reported here had imaging findings consistent with
severe bronchopneumopathy or infiltrative neoplastic disease
that was complicated by severe spontaneous tension pneumo-
pericardium, pneumomediastinum, pneumothorax and pneu-
moretroperitoneum. Histopathology diagnosed the neoplastic
origin of the bronchopulmonary alterations. The immunostain-
ing of multiple lung sections with TTF-1 confirmed the nonpul-
monary origin of the lung carcinoma that was indeed considered
secondary to the mammary gland tumour (Ramos-Vara et al.
2005, Matoso et al. 2010, Kujawa et al. 2014).
Feline mammary gland tumours are highly aggressive and
lung metastasis is frequently encountered (Madewell & Theilen
1987, Forrest & Graybush 1998). Pneumothorax has been rarely
reported secondary to pulmonary neoplasia in both humans and
small animals (Kim et al. 2000, Pawloski & Broaddus 2010, Liu
& Silverstein 2014). Pneumopericardium and/or pneumome-
diastinum secondary to pulmonary neoplasia is extremely rare
in humans but has never been described in the feline species
(Baydur & Gottlieb 1976, Brown & Holt 1995, Kim et al. 2000,
Leclerc et al. 2004, Johnson-Neitman et al. 2006; Barquero-
Romero & Redondo-Moralo 2009, Zahid et al. 2011, Thomas
& Syring 2013).
Three ways have been suggested in which pulmonary neoplasia
can lead to spontaneous pneumopericardium: through the forma-
tion of a bronchopericardial fistula by a necrotic tumour, which
invades the pericardium directly; through trauma caused by an
artificial procedure such as bronchoscopy or thoracocentesis; and
through the rupture of a bulla into the pericardium through a
necrotic focus (Baydur & Gottlieb 1976, Kim et al. 2000).
Spontaneous pneumothorax usually results from the rupture
of a cyst, bleb or bulla into the visceral pleura, migrant foreign
body, lung abscess or pneumonia and neoplasia (Baydur & Got-
tlieb 1976, Kim et al. 2000, Pawloski & Broaddus 2010). In
patients with bronchogenic carcinoma, four pathogenetic mech-
anisms of spontaneous pneumothorax have been suggested: the
creation of a bronchopleural fistula; the rupture of a subpleural
bleb or of an emphysematous bulla; direct pleural invasion by the
tumour; and an indirect effect caused by underlying emphysema
(Baydur & Gottlieb 1976, Kim et al. 2000, Mansella et al. 2014).
Spontaneous pneumomediastinum is a relatively rare benign
condition. It may be associated with one or combination of
pneumothorax, pneumopericardium, pneumoretroperitoneum
or subcutaneous emphysema. Pneumomediastinum can be sec-
ondary to bronchopulmonary diseases, bulla or bleb rupture or
secondary to baro and blunt traumas to the chest or neck (Kim
& Kim 2012, Thomas & Syring 2013, Bilir et al. 2014, Mansella
et al. 2014).
Retropneumoperitoneum is usually caused by a perforated
retroperitoneal hollow viscus or diagnostic procedures; air pas-
sage from the mediastinum through the diaphragmatic hiatus or
along the tissue planes has also been reported (Kim & Kim 2012,
Kim et al. 2013, Fosi et al. 2014); in cats it is frequently associ-
ated with pneumomediastinum (Thomas & Syring 2013).
In the cat reported here the most likely cause for spontaneous
pneumopericardium, pneumomediastinum and pneumothorax
was the rupture of bullae and blebs. During necropsy, a bron-
chopleural and/or a bronchopericardial fistula were not detected
but several blebs were noted on the pleural and visceral pleura
and in the thoracic wall layer (Fig 3). Migration of air into the

682 Journal of Small Animal Practice • Vol 56 • November 2015 • © 2015 British Small Animal Veterinary Association
 Pneumopericardium and lung tumour
pericardium was likely secondary to rupture of blebs into the
pericardium through foci of necrosis because several areas of ero-
sion were detected by histopathology on the pericardium; how-
ever, migration of air through damaged airway walls cannot be
completely ruled out. Retropneumoperitoneum was likely sec-
ondary to air passage through the diaphragmatic hiatus or along
the tissue planes as abdominal necropsy was unremarkable.
In conclusion, based on clinical, imaging findings and
immunohistopathology, the cause of spontaneous pneumoperi-
cardium, pneumomediastinum, pneumothorax and retropneu-
moperitoneum in this cat was metastatic pulmonary carcinoma;
the mechanism by which air reached the pericardium was most
likely secondary to bleb rupture and/or air migration through
impaired air walls.
Spontaneous pneumopericardium can develop in cats with
pulmonary carcinoma and can be associated with pneumothorax,
pneumomediastinum and retropneumoperitoneum as reported
in humans.
Cases presenting with pneumopericardium, pneumothorax
and pneumomediastinum should be strictly monitored and
treated when signs of tension pneumothorax and pneumomedi-
astinum or of cardiac tamponade develop as occurred in this cat.
Conflict of interest
None of the authors of this article has a financial or personal
relationship with other people or organisations that could inap-
propriately influence or bias the content of the paper.
References
Agut, A., Costa-Teixeira, M. A., Cardoso, L., et al. (2010) What is your diagnosis?
Pneumopericardium. Journal of the American Veterinary Medical Association
237, 363-364
Barquero-Romero, J. & Redondo-Moralo, M. J. (2009) Spontaneous pneumome-
diastinum and subcutaenous emphysema: an uncommon complication of lung
cancer. Archivos de Bronconeumologìa 45, 310-311
Barquero Romero, J., Izquierdo Hidalgo, J., Maciá Botejara, E., et al. (2005)
Spontaneous pneumopericardium in a patient with community-acquired pneu-
monia. Revista Española de Cardiologìa (English edition) 58, 227-229
Baydur, A. & Gottlieb, L. S. (1976) Pneumopericardium and pneumothorax compli-
cating bronchogenic carcinoma. The Western Journal of Medicine 124, 144-146
Bilir, O., Yavasi, O. & Ersunan, G., et al. (2014) Pneumomediastinum associ-
ated with pneumopericardium and epidural pneumatosis. Case Reports in
Emergency Medicine 2014, 275490
Borgonovo, S., Rocchi, P. M., Raiano, V., et al. (2014) Spontaneous pneumoperi-
cardium in a dog with bronchopulmonary disease complicated by pyothorax and
pneumothorax. Canadian Veterinary Journal 55, 1186-1191
Brown, D. C. & Holt, D. (1995) Subcutaneous emphysema, pneumothorax, pneu-
momediastinum, and pneumopericardium associated with positive-pressure
ventilation in a cat. Journal of the American Veterinary Medical Association
206, 997-999
Journal of Small Animal Practice • Vol 56 • November 2015 • © 2015 British Small Animal Veterinary Association
Forrest, L. J. & Graybush, C. A. (1998) Radiographic patterns of pulmonary metas-
tasis in 25 cats. Veterinary Radiolology & Ultrasound 39, 4-8
Fosi, S., Giuricin, V., Girardi, V., et al. (2014) Subcutaneous emphysema, pneu-
momediastinum, pneumoretroperitoneum, and pneumoscrotum: unusual com-
plications of acute perforated diverticulitis. Case Reports in Radiology 2014,
431563
Harris, R. D. & Kostiner, A. I. (1975) Pneumopericardium associated with broncho-
genic carcinoma. Chest 67, 115-116
Leclerc, A., Brisson, B. A. & Dobson, H. (2004) Pneumopericardium associated
with a pulmonary-pericardial communication in a dog. Journal of the American
Veterinary Medical Association 224, 710-712
Johnson-Neitman, J. L., Huber, M. L. & Amann, J. F. (2006) What is your diagno-
sis? Pneumomediastinum and pneumopericardium. Journal of the American
Veterinary Medical Association 229, 359-360
Kim, W. H. & Kim, B. H. (2012) Bilateral pneumothoraces, pneumomediastinum,
pneumoperitoneum, pneumoretroperitoneum, and subcutaneous emphy-
sema after percutaneous tracheostomy – a case report. Korean Journal of
Anesthesiology 62, 488-492
Kim, Y. I., Goo, J. M. & Im, J. G. (2000) Concurrent pneumopericardium and pneu-
mothorax complicating lung cancer: a case report. Korean Journal of Radiology
1, 118-120
Kim, B. H., Yoon, S. J., Lee, J. Y., et al. (2013) Subcutaneous emphysema, pneu-
momediastinum, pneumoretroperitoneum, and pneumoperitoneum secondary
to colonic perforation during colonoscopy. Korean Journal of Anesthesiology
65, S103-S104
Kujawa, A., Olias, P., Böttcher, A., et al. (2014) Thyroid transcription factor-1 is a
specific marker of benign but not malignant feline lung tumours. Journal of
Comparative Pathology 151, 19-24
Liu, D. T. & Silverstein, D. C. (2014) Feline secondary spontaneous pneumo-
thorax: a retrospective study of 16 cases (2000-2012). Journal of Veterinary
Emergency and Critical Care 24, 316-325
Luthi, F., Groebli, Y., Newton, A., et al. (2003) Cardiac and pericardial fistulae asso-
ciated with esophageal or gastric neoplasms: a literature review. International
Surgery 88, 188-193
Madewell, B. R. & Theilen, G. H. (1987) Tumors of the mammary gland. In:
Veterinary Cancer Medicine. 2nd edn. Eds G. H. Theilen and B. R. Madewell.
Lea & Febiger, Philadelphia, PA, USA. pp 327-340
Maki, D. D., Sehgal, M., Kricun, M. E., et al. (1999) Spontaneous tension pneu-
mopericardium complicating staphylococcal pneumonia. Journal of Thoracic
Imaging 14, 215-217
Mansella, G., Bingisser, R. & Nickel, C. H. (2014) Pneumomediastinum in blunt
chest trauma: a case report and review of the literature. Case Reports in
Emergency Medicine 2014, 685381
Matoso, A., Singh, K., Jacob, R., et al. (2010) Comparison of thyroid transcription
factor-1 expression by 2 monoclonal antibodies in pulmonary and nonpulmo-
nary primary tumors. Applied Immunohistochemistry & Molecular Morphology
18, 142-149
Orlando, J. M. (2009) What is your diagnosis? Pneumopericardium and bilateral
pneumothorax in a Labrador Retriever. Journal of the American Veterinary
Medical Association 235, 1145-1146
Parent, C. & Rozanski, E. (1998) What is your diagnosis? Pneumopericardium and
pulmonary alveolar disease (consistent with pulmonary contusions). Journal of
the American Veterinary Medical Association 212, 1377-1378
Pawloski, D. R. & Broaddus, K. D. (2010) Pneumothorax: a review. Journal of the
American Animal Hospital Association 46, 385-397
Ramos-Vara, J. A., Miller, M. A. & Johnson, G. C. (2005) Usefulness of thyroid tran-
scription factor-1 immunohistochemical staining in the differential diagnosis of
primary pulmonary tumors of dogs. Veterinary Pathology 42, 315-320
Rongé, R., Roels, P., De Meirleir, K., et al. (1983) Bronchogenic carcinoma: a rare
cause of nontraumatic pneumopericardium. Acta Cardiologica 38, 565-569
Thomas, E. K. & Syring, R. S. (2013) Pneumomediastinum in cats: 45 cases
(2000-2010). Journal of Veterinary Emergency and Critical Care 23, 429-435
Zahid, M., Shafiq, I. Albon, L., et al. (2011) Typical bronchial carcinoid tumour
presenting as pneumomediastinum. BMJ Case Reports 2011. doi: 10.1136/
bcr.01.2011.3744
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