Evaluating Decomposition Condition in Stranded Cetaceans Using Postmortem Computed Tomography and Radiological Alteration Index
Abstract
Postmortem changes occur in carcasses immediately and progressively after death through a wide range of processes including decomposition under influence from the internal and external environments. These changes affect the interpretation of pathological conditions at postmortem examination and can provide information regarding the time since death (postmortem interval).1 In stranded marine mammals, the decomposition status is conventionally graded using the decomposition condition code (DCC) system, where stranded animals are classified as either live, freshly dead, moderately decomposed, advanced decomposed, and mummified or skeletal remains (DCC 1–5) based on characteristics indicative of postmortem changes.2 DCC is often used to guide stranding response, prioritise sampling during necropsy of marine mammals, and even to establish inclusion/exclusion criteria in systematic studies.2,3 However, the grading of DCC relies on individual interpretation of the descriptions, thus making this system variable, as well as observer- and experience-dependent.
Postmortem computed tomography (PMCT) is one of the virtopsy techniques that has been used to examine deceased humans during forensic autopsies, of which one of the applications is to assess postmortem changes through various imaging features such as gas accumulation.4 The radiological alteration index (RAI) is an established method in humans to score the level of postmortem changes based on the presence of decomposition gas in selected sites, which allows efficient and easy evaluation of postmortem changes that can be reliably used by non-experienced observers.5 Since 2014, Kot and his team in Hong Kong have pioneered the routine use of PMCT to examine stranded cetaceans and the technique has been increasingly adopted in stranding investigations around the world.6-8 Therefore, adapting the RAI system to cetaceans would provide an efficient and reliable method to assess the level of postmortem changes in stranded carcasses which is valuable for stranding investigation and research.
In the current study, we analysed the PMCT scans of 74 cetaceans stranded in Hong Kong and Taiwan ranging from freshly dead to advanced decomposed (DCC 2–4). We adapted the RAI system from humans to stranded cetaceans, and the level of postmortem change in each case was independently scored using RAI by an experienced imaging clinician and two veterinary students. The level of postmortem change was also verified via histopathology in selected cases. A high level of inter-observer reliability in RAI scores was found between observers of different experience levels (ICC2,1=0.980; 95% CI 0.970–0.987). We revealed mismatches between DCC classes and RAI, indicating there were potential inconsistencies in scoring DCC which relies heavily on external features and may not account for the internal condition of the carcasses that can be non-invasively assessed by PMCT and RAI. We also note that pathological gas accumulation (e.g., gas embolism from decompression sickness, subcutaneous emphysema, infection) should be considered when interpreting postmortem changes in stranded cetaceans using PMCT.9,10 Overall, this study demonstrated that RAI is an effective and reproducible method for assessing decomposition conditions in stranded cetaceans and can be used alongside DCC given the growing application of PMCT in stranding investigation.
Acknowledgements
We would like to thank the Agriculture, Fisheries, and Conservation Department of the Hong Kong Special Administrative Region Government for the continuous support in the Hong Kong cetacean stranding response programme. Sincere appreciation is extended to the veterinarians, staff, and volunteers from the Ocean Park Conservation Foundation Hong Kong, the Marine Mammal Department of Ocean Park Hong Kong, as well as the Aquatic Animal Virtopsy Lab, City University of Hong Kong. This study was also contributed to by the cetacean stranding response network in Taiwan; and we would like to thank Prof. Wei-Cheng Yang from the National Taiwan University and Dr. Wen-Ta Li from the Taiwan Cetacean Society for sharing the cetacean stranding cases and assisting in the histopathological interpretations in this study.
Literature Cited
1. Brooks JW. Postmortem changes in animal carcasses and estimation of the postmortem interval. Vet Pathol. 2016;53(5):929–940.
2. Geraci JR, Lounsbury VJ. Marine Mammals Ashore: A Field Guide for Strandings. 2nd ed. Baltimore, MD: National Aquarium in Baltimore; 2005.
3. IJsseldijk LL, Brownlow AC, Mazzariol S. Best Practice on Cetacean Post Mortem Investigation and Tissue Sampling. Joint ACCOBAMS and ASCOBANS document. 2019.
4. Levy AD, Harcke HT, Mallak CT. Postmortem imaging: MDCT features of postmortem change and decomposition. Am J Forensic Med Pathol. 2010;31(1):12–17.
5. Egger C, Vaucher P, Doenz F, Palmiere C, Mangin P, Grabherr S. Development and validation of a postmortem radiological alteration index: the RA-Index. Int J Legal Med. 2012;126(4):559–566.
6. Tsui HCL, Kot BCW, Chung TYT, Chan DKP. Virtopsy as a revolutionary tool for cetacean stranding programs: implementation and management. Front Mar Sci. 2020;7:542015.
7. Kuijpers NW, van Schalkwijk L, IJsseldijk LL, Willems DS, Veraa S. Post mortem computed tomography pulmonary findings in harbor porpoises (Phocoena phocoena). Animals. 2022;12(11):1454.
8. Granados-Zapata A, Robles-Malagamba MJ, González-Barrientos R, Kot BC, Barquero-Calvo E, Cordero-Chavaría M, Suárez-Esquivel M, Guzmán-Verri C, Palacios-Alfaro JD, Tien-Sung C, Moreno E. Pathological studies and postmortem computed tomography of dolphins with meningoencephalomyelitis and osteoarthritis caused by Brucella ceti. Oceans. 2022;3(2):189–203.
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(3):536–547.
10. Danil K, St Leger JA, Dennison S, Bernaldo de Quirós Y, Scadeng M, Nilson E, Beaulieu N. Clostridium perfringens septicemia in a long-beaked common dolphin Delphinus capensis: an etiology of gas bubble accumulation in cetaceans. Dis Aquat Organ. 2014;111(3):183–190.