Eur J Wildl Res (2013) 59:441–444 DOI 10.1007/s10344-013-0700-4
SHORT COMMUNICATION
First indication of gas embolism in a harbour porpoise (Phocoena phocoena) from German waters U. Siebert & P. D. Jepson & P. Wohlsein
Received: 28 September 2012 / Revised: 14 January 2013 / Accepted: 23 January 2013 / Published online: 24 February 2013 # Springer-Verlag Berlin Heidelberg 2013
Abstract In the last decade, a number of cetacean strandings have gas embolic pathology analogous to decompression sickness in man and experimental animals. Acute gas and fat embolic lesions have also been found in massstranded beaked whales causally linked to high-intensity anthropogenic mid-frequency sonar activities. Sporadic chronic gas embolic lesions have also been described. This communication describes a first case of numerous gas-filled fibrous cavities in the markedly enlarged liver of a dead adult male harbour porpoise stranded at the North Sea coast of Schleswig-Holstein, Germany. Additional pathological findings consisted of chronic parasitic granulomatous cholangiohepatitis, hepatic vein thrombosis, parasitic infestations of the bronchial tree and pulmonary blood vessels associated with bronchopneumonia and severe parasitic burden in both ear sinuses. The hepatic cavernous lesions are similar to those described in chronic gas bubble disease in other cetaceans, most likely resulting from decompression-related tissue supersaturation with nitrogen.
Communicated by H. Kierdorf U. Siebert Institute for Terrestrial and Aquatic Wildlife Research (ITAW), University of Veterinary Medicine Hannover, Foundation, Werftstr. 6, 25761 Büsum, Germany P. D. Jepson Institute of Zoology, Zoological Society of London, Regent’s Park, London NW1 4RY, UK
Keywords Harbour porpoise . Phocoena phocoena . German waters . Liver . Gas embolism
Introduction An increasing number of beaked whale mass strandings have been observed in different areas over the last decades including the Mediterranean Sea, Canary Islands and Bahamas (Frantzis 1998; Jepson et al. 2003; Fernández et al. 2005; Cox et al. 2006, Filadelfo et al. 2009). It was suspected that beaked whales, particularly, can develop acute gas and fat embolism similar to decompression sickness (DCS) in man caused by strong behavioural reaction as response to some sonar frequencies (Jepson et al. 2003; Fernández et al. 2005; Hooker et al. 2012). Cases of acute and chronic gas embolism have occasionally been found in marine mammals stranded in SW England (Jepson et al. 2005). Systematic pathological investigations have been performed on harbour porpoises (Phocoena phocoena) from different areas of European waters (Baker and Martin 1992; Siebert et al. 2001; Jauniaux et al. 2002; Jepson et al. 2005; Siebert et al. 2006). Effects of anthropogenic activities have been associated with an increased occurrence of infectious diseases as well as a reduced function of the immune and endocrine systems (Siebert et al. 1999; Beineke et al. 2005; Jepson et al. 2005; Das et al. 2006). This communication describes the first case suspicious for gas embolism in a harbour porpoise from German waters.
Material and methods P. Wohlsein (*) Department of Pathology, University of Veterinary Medicine Hannover, Foundation, Bünteweg 17, 30559 Hannover, Germany e-mail:
[email protected]
An adult male harbour porpoise, measuring 134 cm in length, was stranded at the western shore of the North Sea island of Sylt, Germany. Until post-mortem examination,
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the carcass was stored at −20 °C. The necropsy was performed according to standardised European necropsy protocol for cetaceans (Siebert et al. 2001). Samples from the liver were fixed in 10 % buffered formalin and were processed routinely into paraffin wax, sectioned and stained with haematoxylin and eosin, azan and Masson’s trichrome stains. In addition, the liver was submitted for bacteriological examination (Siebert et al. 2009). Parasites were fixed in 70 % ethanol prior to identification (Lehnert et al. 2005).
Results The emaciated harbour porpoise was in a state of starting decomposition, limiting the number of examinations possible. The liver was severely enlarged, and most of the parenchyma was almost completely replaced by gas-filled cavities of 1 to 5 cm in diameter filled with colourless gas (Fig. 1). The cavities were encapsulated, and the thickness of the capsule ranged from 2 to 4 mm. In addition, thrombosis of few hepatic veins was observed. Histologically, the lesions were identified as optically empty cavities with demarcating connective tissue (Figs. 2a and 3a) which stained intensely with Masson’s trichrome and azan stains (Figs. 2b and 3a). In addition, focally extensive granulomatous cholangiohepatitis with trematode eggs, multifocal lymphangiectasia and a mild bile duct hyperplasia were observed. The digestive tract was empty. Additional lesions included severe parasitic infection of the bronchial tree and blood vessels with Pseudalius inflexus and Torynurus convolutus associated with a moderate chronic diffuse granulomatous bronchopneumonia. Heavy infection of Stenurus minor was found in both ear sinuses. Microbiological examination of liver tissue revealed an unspecific mixed flora in low concentrations.
Fig. 2 a Liver with multiple large optically empty cavities (letters x) surrounded by a fibrous capsule (arrows). Haematoxylin and eosin; bar, 500 μm. b Liver with multiple large optically empty cavities (letters x) surrounded by a fibrous capsule (arrows). Azan; bar, 500 μm
Discussion
Fig. 1 Slice of the formalin-fixed liver with numerous cavities (arrows) ranging from 0.5 to 5 cm and thrombosed hepatic veins (arrows). Bar, 1 cm
The harbour porpoise showed chronic gas embolic lesions in the liver characterised by gas-containing cavities surrounded by fibrous tissue. The lesions are identical to those described in UK-stranded cetaceans of several species, including harbour porpoise, single-stranded common dolphins (Delphinus
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Fig. 3 a Fibrous capsule composed of collagen fibres (asterisks) and fibrocytes (arrowheads). Haematoxylin and eosin; bar, 25 μm. b Fibrous capsule composed of collagen fibres (asterisks) and fibrocytes (arrowheads). Azan; bar, 25 μm
delphis), Risso’s dolphins (Grampus griseus), Blainville’s beaked whale (Mesoplodon densirostris) (Jepson et al. 2003, 2005). The pathogenesis of the acute gas and fat embolic lesions that were mainly observed in beaked whales during naval exercises using high-powered mid-frequency sonars is thought to be analogous to DCS in human breath-hold divers where behavioural changes to dive profiles may lead to excessive nitrogen supersaturation on surfacing and driving symptomatic in vivo bubble formation (Jepson et al. 2003; Fernández et al. 2005; Hooker et al. 2012). In whales, lesions may result from behaviourally induced excessive nitrogen supersaturation on ascent leading to in vivo bubble formation followed by bubble persistence and growth (Jepson et al. 2005). Alternatively, mechanisms of bubble formation initiated by a direct physical effect of high-intensity sound energy (e.g. rectified diffusion) on bubble precursors (gas nuclei) have been proposed that may then further expand and grow by static diffusion in nitrogen-supersaturated tissues, including both shallow- and deep-diving cetaceans (Jepson et al. 2003, 2005; Cox et al. 2006). Once in vivo gas bubbles are sufficiently large (irrespective of how they initially formed), they may not easily or fully reabsorb but, instead, be subjected to further cycles of tissue supersaturation and growth by static diffusion on ascent (Jepson et al. 2005; Cox et al. 2006). The recent analysis of the gaseous contents in a gas-cavitated
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spleen of a UK-stranded Risso’s dolphin provided further support for this hypothesis since the gas was found to contain approximately 95 % nitrogen without evidence of gas related to decomposition (Bernaldo de Quirós et al. 2012). Since 1990, stranded and by-caught cetaceans from waters of Schleswig-Holstein are systematically investigated for their health status. This is the first case with gas bubbles similar to those described in cetaceans from other areas. Due to starting decomposition, detailed examination of other organs including the brain and inner ears was not performed. Parasites in the lung, ear sinuses and bile ducts as well as associated inflammation are regularly found in harbour porpoises from the same area (Siebert et al. 2001; Lehnert et al. 2005). The emaciated body condition in association with hepatic vein thrombosis of unknown origin may be related to the death. However, the animal obviously survived the gas embolism for at least some weeks to develop thick fibrous capsules around the gas bubbles. Information on the movement of harbour porpoise individuals in the North Sea is not available due to missing tagging studies. Therefore, it is not possible to retrace the position, where the animal was probably exposed to activities, resulting in lesions indicative for decompression sickness. On the Danish coastline, 85 harbour porpoises stranded unprecedentedly from 7th to 15th April, 2005. A statistical model indicated that naval presence is correlated with higher rates of porpoise strandings. It was confirmed that military vessels from various countries were in the area from the 7th April 2005, taking part in the largest naval exercise in Danish waters to date (Wright et al. 2013). The present case shows that systematic pathological investigations are needed to detect and understand effects of anthropogenic activities on cetaceans. Acknowledgments The harbour porpoise was investigated as part of the health monitoring of small cetaceans funded by the SchleswigHolstein Ministry of Agriculture, Environment and Rural Areas. We thank all colleagues for their help during the necropsy and Dr. E. Prenger-Berninghoff for bacteriological investigations. Conflict of interest None of the authors of this paper has a financial or personal relationship with other people or organisations that could inappropriately influence or bias the content of the paper.
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