Signalment:  

Adult male crested-wood partridge, (Rollulus rollout).This bird was found dead on the floor of its enclosure. It had recently been the target of increased conspecific aggression.

Gross Description:  

The skull was crushed with loss of overlying skin and soft tissues. The dorsal aspects of the cerebral hemispheres and cerebellum were exposed, lacerated and hemorrhagic. Fragments of brain tissue were embedded in bone at the fracture sites. 

Histopathologic Description:

Lungs: Throughout the section, pulmonary arterioles are diffusely congested and filled by variably sized, fragmented sections of neuropil sparsely populated by neurons, supportive glial cells and capillaries (gray matter) while others contain sections of white matter, portions of the molecular layer and granular layer separated by large multipolar Purkinje cells (cerebellum). In some sections there is a focal aggregate of macrophages, multinucleated ciant cells and fewer lymphocytes and plasma cells that surround a central area of necrosis (granuloma). There are multifocal aggregates of macrophages that contain both fine black pigmented (carbon) and slightly larger, crystalline-like birefringent particulate debris associated with the parabronchi (anthracosis).

Morphologic Diagnosis:  

Lungs:
1) Brain tissue emboli, pulmonary arterioles, multifocal, peracute, moderate to severe with arteriolar congestion.
2) Pneumonia, granulomatous, multifocal, chronic, mild (not present in all sections).
3) Anthracosis, parabronchial, chronic, multifocal, mild.

Condition:  

Cerebral tissue pulmonary embolization due to trauma

Contributor Comment:  

This crested wood partridge died from severe head trauma that resulted in fracture of the skull and disruption of the dorsal venous sinus and subjacent cerebrum and cerebellum. This severe trauma resulted in embolization of fragments of brain tissue that are visible throughout the pulmonary arterioles. The small granuloma present in one of the lungs was fungal in origin. Anthracosis is an exceedingly common finding in animals that inhabit densely populated urban environments. In this case, fungal pneumonia and anthracosis were mild and incidental to the death of this bird.

Cerebral tissue pulmonary embolization (CTPE) is a possible sequel to severe penetrating or closed head trauma. CTPE is most commonly associated with high impact blunt force trauma (i.e. automobile collision) in adults and instrument-assisted delivery in neonates.(4,5) Though a rare occurrence, post-traumatic pulmonary emboli can cause significant mortality (up to 43%) in the absence of prophylactic treatment.(6) Massive CTPE is detectable at autopsy and is associated with disruption of the large dorsal cerebral venous sinus in addition to brain injury. Microscopic brain emboli, however, have been identified in pulmonary arterioles and systemic veins in cases with intact dura, suggesting embolic entry through smaller cerebral and meningeal veins.(8)

The behavior, physiology and anatomy of flighted birds may increase the likelihood of CTPE in avian species compared to terrestrial animals. Behaviorally, flighted birds are prone to severe brain trauma due to in-flight speed and prevalent collision injuries. Physiologically, avian veins, unlike mammalian veins, are compliance vessels, and they actively dilate during flight to increase cardiac output.(9) A larger venous diameter permits embolization of larger tissue fragments to the lungs. Anatomically, the avian brain and spinal cord are surrounded by a series of contiguous venous sinuses including the dorsal cerebral, occipital and vertebral sinuses and the ventral sinus cavernosus. These sinuses drain blood to the heart via the jugular or vertebral veins.(10) These extensive, superficial structures are prone to rupture with severe, closed or penetrating head trauma, presenting direct venous access to injured neural tissue.

This case illustrates dissemination of central nervous system (CNS) tissue to the venous system after head trauma. Consumption of meat products contaminated with CNS tissue from cattle with bovine spongiform encephalopathy is considered to be a significant route of transmission for mutant proteinase-resistant protein (PrPsc), the proposed etiologic agent of variant CreutzfeldtJakob disease (vCJD) in humans.(2,7) Air-injection penetrating captive bolt stunning prior to terminal exsanguination has been identified as a major risk factor in CNS contamination of meat products. This method allows dislodged CNS tissue to disseminate through the bloodstream during the brief period of sustained cardiac function, followed by contamination of skeletal muscle with jugular exsanguination. For this reason, this method of cattle slaughter is currently banned in the United States and the European Union.(1)

JPC Diagnosis:  

1. Lung, pulmonary arteries: Neural emboli, multiple.
2. Lung: Granulomas, parabronchiolar, multiple, with anthracosis.

Conference Comment:  

The contributor provides an outstanding review of cerebral tissue pulmonary embolization. Both cerebral and cerebellar tissue was identified in emboli. This particular case has significant slide variation; in several sections the neural emboli are not as striking; however, immunohistochemical staining with GFAP confirms the presence of cerebrum or cerebellum within numerous pulmonary arterioles. 

Conference participants conducted an abbreviated discussion of the anatomy and physiology of the normal avian lung. The avian mesobronchus (similar to the mammalian bronchus) is an airway lined with ciliated respiratory epithelium that has hyaline cartilage and smooth muscle within its walls; it has no direct function in gas exchange. The mesobronchus gives rise to the recurrent secondary bronchi, which are analagous to mammalian bronchioles and contain smooth muscle, but no cartilage within their walls. These further divide into tertiary bronchi (parabronchi) with walls that are "scalloped" by bay-like air vesicles, where gas exchange takes place. Air vesicles are composed of simple squamous epithelium with an underlying supporting connective tissue. Air passes through numerous air capillaries in the wall of each air vesicle; these are adjacent to the blood capillaries, an arrangement that results in the establishment of a countercurrent flow. Unlike mammalian ventilation, in which a part of the ventilator volume is "stale" air, and mammalian structure with its numerous blind alleys and abundant dead space, the avian lung is a continuous flow system. Thus, avian lungs are much more efficient than mammalian, which is not surprising, considering the high demand of flight muscles for oxygenation.(3)

Participants closed with a brief summary of other reported causes of pulmonary emboli, including trophoblastic emboli (especially in guinea pigs), fibrocartilaginous emboli, neoplastic cells (especially lymphocytes in mice with tumor lysis syndrome), bone marrow elements (subsequent to injury/fracture), and allantoic fluid (in humans).

References:

1. Bowling MB, Belk KE, Nightingale KK, Goodridge LD, Scanga JA, Sofos JN, et al. Central nervous system tissue in meat products: an evaluation of risk, prevention strategies, and testing procedures. Adv Food Nutr Res. 2007;53:39-64.

2. Brown P, Will RG, Bradley R, Asher DM, Detwiler L. Bovine spongiform encephalopathy and variant Cruetzfeldt-Jakob disease: background, evolution and current concerns. Emerg Infect Dis. 2001;7:6-16.

3. Caceci T. Virginia-Maryland Regional College of Veterinary Medicine, Blacksburg, VA. VM8054 Veterinary Histology website. Respiratory System II: Avians. http://www.vetmed.vt.edu/education/Curriculum/VM8054/Labs/Lab26/lab26.htm. Accessed February 22, 2014.

4. Cox P, Silvestri E, Lazda E, Nash R, Jeffrey I, Ostojic N et al. Embolism of brain tissue in intrapartum and early neonatal deaths: report of 9 cases. Pediatr Dev Pathol. 2009;12:464-468.

5. Echeverria RF, Baitello AL, Pereira de Godoy JM, Espada PC, Morioka RY. Prevalence of death due to pulmonary embolism after trauma. Lung India. 2010;27:72-74.

6. Geerts WH, Code KI, Jay RM, Chen E, Szalai JP. A prospective study of venous thromboembolism after major trauma. N Engl J Med. 1994;331:16011606. 

7. Jones M, Peden AH, Prowse CV, Gr+�-�ner A, Manson JC, Turner ML, et al. In vitro amplification and detection of variant CreutzfeldtJakob disease PrPSc. J Pathol. 2007;213:21-26.

8. Morentin B, Biritxinaga B. Massive pulmonary embolization by cerebral tissue after head trauma in an adult male. Am J Forensic Med Pathol. 2006;27:268-270.

9. Smith FM, West NH, Jones DR. The Cardiovascular system. In: Whittow GC, ed. Sturkies Avian Physiology. 5th ed. San Diego, CA: Academic Press; 2000:174.

10. West NH, Langille BL, Jones DR. Cardiovascular system. In: King AS, McLelland J, eds. Form and Function in Birds. Vol. 2. San Francisco, CA: Academic Press; 1981:278-283.

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