The Significance of Gas Bubbles in Marine Mammals
IAAAM 2012
Sophie Dennison1,2,3; Andreas Fahlman4; Michael Moore5; Yara Bernaldo de Quiros5; Judy St. Ledger6; Kerri Danil7
1Marine Mammal Radiology, San Francisco, CA, USA; 2Animal Scan, Redwood City, CA, USA; 3School of Veterinary Medicine, University of Wisconsin, Madison, WI, USA; 4Department of Life Sciences, Texas A&M University, Corpus Christi, TX, USA; 5Woods Hole Oceanographic Institution, Woods Hole, MA, USA; 6Seaworld, San Diego, CA, USA; 7Southwest Fisheries Science Center, La Jolla, CA, USA

Abstract

Published reports of cetaceans including beaked whales that had evidence of acute and chronic gas and fat embolic disease4,6 and dysbaric osteonecrosis in sperm whales due to repetitive dive injury8 reignited a contentious debate on whether or not marine mammals are susceptible to decompression sickness (DCS). As a result, studies were performed to try and determine whether or not marine mammals develop gas bubbles and under what circumstances.

Our initial studies demonstrated that free ranging marine mammals that died at depth in gill nets had extensive bubbling after being hauled to the surface that was attributed to off-gassing of supersaturated tissues.9 Then, B-mode ultrasound studies in live-stranded, free-ranging cetaceans that had lost the opportunity to recompress demonstrated bilateral renal gas accumulations in all 22 cases examined. Four live-stranded animals that underwent ultrasound examination showing renal gas died and subsequently underwent computed tomography (CT) and necropsy examination that demonstrated multifocal gas accumulations not limited to the kidneys. Other live-stranded dolphins with ultrasound evidence of renal gas were successfully released and bubbles were presumed asymptomatic. Gas bubbles have not been identified in groups of captive-maintained cetaceans5 or stranded pinniped pups and adults.

Hyperbaric CT (HCT) was developed to evaluate the effects of depth on lung compression. Four animals were pressurized to mimic dives to known depths with lungs inflated to various degrees. Data showed that the depth of lung compression is dependent on lung volume at dive commencement10 and correlated with previous empirical7 and theoretical3 data. This suggests that gas exchange may continue through part of the water column where pressure is sufficient to drive nitrogen into the blood and permit a state of supersaturation to develop, and that our understanding of gas management in marine mammals is probably incomplete.

Three common dolphins underwent computed tomography (CT), magnetic resonance imaging (MRI) and necropsy within hours of death after swimming into an underwater detonation zone.2 Imaging studies demonstrated abnormal gas bubbles within cerebral, vertebral, coronary, pulmonary and hepatic vasculature as well as subcapsular and intravascular renal accumulations, perimandibular fat pad accumulations and pneumoperitoneum. One animal demonstrated acute fracture of the right tympanic plate with disruption of the auditory ossicles. Gas sampling and analysis was performed according to newly published methods.1 In addition to the abnormal gas, necropsy revealed pulmonary (subpleural), tracheal (mucosa and submucosal), bronchial, esophageal, and mandibular acoustic fat acute petechial to ecchymotic hemorrhage. Histologic review demonstrated fat emboli within pulmonary alveoli and lymph node subcapsular sinusoidal spaces. The cause of death was attributed to acute vascular gas embolism.

Advanced imaging allows non-disruptive description of the distribution of gas bubbles, but limitations exist. Distinction between different gas compositions is not possible using imaging alone but distinction is needed to determine the etiology of any gas present. The presence of gas does not necessarily indicate the cause of death. Imaging in combination with gas analysis, necropsy and histological evaluation is recommended for determining the presence, significance and etiology of gas bubbles identified in marine mammals.

References

1.  Bernaldo de Quiros Y, Gonzalez-Diaz O, Saavedra P, Arbelo M, Sierra E, Sacchini S, Jepson JD, Mazzariol S, Di Guardo G, Fernandez A. Methodology for in situ gas sampling, transport and laboratory analysis of gases from stranded cetaceans. Sci Rep. 2011;1:193 (doi 10.1038/srep00193).

2.  Danil K, St Leger JA. Seabird and dolphin mortality associated with underwater detonation exercises. Marine Technology Society Journal. 2011;45(6):89–95.

3.  Fahlman A, Hooker SK, Olszowka A, Bostrom BL, Jones DR. Estimating the effect of lung collapse and pulmonary shunt on gas exchange during breath-hold diving: the Scholander and Kooyman legacy. Resp Physiol Neurobiol. 2009;65:28–29.

4.  Fernandez A, Edwards JF, Rodriguez F, Espinosa de los Monteros A, Herraez P, Castro P, Jaber JR, Martin V, Arbelo M. Gas and fat embolic syndrome involving a mass stranding of beaked whales (Family Ziphiidae) exposed to anthropogenic sonar signals. Vet Pathol. 2005;42:446–457.

5.  Houser DS, Dankiewicz-Talmadge LA, Stockard TK, Ponganis PJ. Investigation of the potential for vascular bubble formation in a repetitively diving dolphin. J Exp Biol. 2009;213:52–62.

6.  Jepson PD, Deaville IAP, Patterson AM, Pocknell HM, Ross JR, Baker FE, Howie FE, Reid RJ, Colloff A, Cunningham AA. Acute and chronic gas bubble lesions in cetaceans stranded in the United Kingdom. Vet Pathol. 2005;42:291–305.

7.  Kooyman GL, Sinnett EE. Pulmonary shunts in harbor seals and sea lions during simulated dives to depth. Physiol Zool. 1982;55(1):105–111.

8.  Moore MJ, Early GA. Cumulative sperm whale bone damage and the bends. Science. 2004;306:2215.

9.  Moore MJ, Bogomolni AL, Dennison SE, Early G, Garner MM, Hayward BA, Lentell BJ, Rotstein DS. Gas bubbles in seals, dolphins and porpoises entangled and drowned at depth in gillnets. Vet Pathol. 2009;46:536–547.

10. Moore MJ, Hammar T, Arruda J, Cramer S, Dennison S, Montie E, Fahlman A. Hyperbaric computed tomographic measurements of lung compression in seals and dolphins. J Exp Biol. 2011;214:2390–2397.

  

Speaker Information
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Sophie Dennison
Marine Mammal Radiology
San Francisco, CA, USA


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