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Bacteriological and histopathological findings in cetaceans that stranded in the Philippines from 2017 to 2018

Marie Christine M. Obusan, Jamaica Ann A. Caras, Lara Sabrina L. Lumang, Erika Joyce S. Calderon, Ren Mark D. Villanueva, Cristina C. Salibay, Maria Auxilia T. Siringan, Windell L. Rivera, Joseph S. Masangkay, Lemnuel V. Aragones

Preprint posted on November 30, 2020 https://www.biorxiv.org/content/10.1101/2020.11.30.403568v1

Navigating change: sentinels of the sea tell about ocean health and disease.

Selected by Paul Gerald L. Sanchez and Stefano Vianello

Overview and context

Around 70% of our planet is covered in water, with ~130 species of mammals living within oceanic ecosystems. Central to this preprint is the concept of sentinel organisms, whereby marine mammals can be seen as monitors and relayers of information about oceanic health (Bossart, 2011). Accordingly, monitoring the state of marine mammals can provide early reports of changing environmental pressures, as well as early warning signs of health threats, stressors, disease.

Indirectly, and through reporting on the health of their own populations and of their environment, marine sentinels also provide information about imminent health, environmental, and economic threat to the livelihood of the human communities associated with them. Putting the urgency of the matter in perspective, coastal areas bordering oceanic ecosystems are home of around 40% of the world’s human population.

 

Figure 1: sites of cetacean stranding in the Philippines in the year 2017-2018 (adapted from preprint Figure 1). Map is from snazzymaps.com (public domain). Cetaceans are from The Philippines’ Bureau of Fisheries and Aquatic Resources (“Protected Philippine aquatic wildlife” poster; CC-BY SA)

 

Stranding events of e.g. whales and dolphins, as tragic as they may be, represent a practical opportunity to interact with some of these marine mammal sentinels, and to collect the information they may carry with them. In the Philippines, a network of experts, professionals and volunteers (the Philippine Marine Mammal Stranding Network) readily mobilises upon stranding events, and as such allows not only rehabilitation and rescue of the animals, but also investigation of the cause of stranding, and sample collection.

In this study, the authors analyse histopathological and bacteriological samplings from 21 stranding events on Philippines coasts (see Figure 1). Crucially, these findings uncover troubling levels of multiple antibiotic resistance within bacterial populations of oceanic ecosystems, as well as histopathological evidence that cetacean may act as hosts of protozoan disease with zoonotic potential (specifically, Toxoplasma gondii). In practice, marine sentinel organisms are relaying forewarnings of significant threats to human health, while bearing the burden of increasing anthropogenic degradation of coastal and oceanic ecosystems.

 

Key Results

Histopathological findings

The authors perform histopathological examination of tissue samples obtained from stranded cetaceans. Many of the lesions observed are expectedly consequences of the trauma and stress associated with the stranding event itself: a stranded marine mammal will indeed quickly develop congestion of its internal tissues due to its body weight not being supported by water anymore.

Yet, other lesion types report environmental and parasitic stresses. Among many other lesion types, the authors document significant cases of glomerulopathy: a condition which has elsewhere been speculatively associated with chronic exposure to heavy metals. Even more jarringly, the authors provide the first histopathological evidence of Toxoplasma infection within local cetaceans. Infection by this parasite is most likely to originate from anthropogenic sewage runoff, and represents a potential threat also to humans if cetacean meat was to be consumed.

Bacteriological findings

Bacterial swabs from both external and internal areas of stranded cetaceans show species of Enterobacter, Escherichia, Klebsiella, Proteus, and Shigella bacteria. Very worryingly, the authors find that 79% of the sampled bacterial populations display multiple antibiotic resistance, some being resistant to up to 39% of the (18) antibiotics tested. Great point of concern is the detection of resistance against multiple carbapenems, currently considered the last available line of defence in antibacterial fight. The inference is that of heavily antibiotic contaminated surface waters, through which whales and dolphins are forced to navigate as they periodically resurface for air.

  

Figure 2: Photos of rescue operations. From the “Friends of Philippine Marine Mammal Stranding Network” Facebook page. Reused with permission

 

Significance

This study highlights the relevance of “sentinel organism” frameworks in the monitoring of oceanic and marine mammal health, and how such frameworks link these dimensions to human livelihood. Of note, the paper informs better strategies for marine mammal rescue, rehabilitation, and conservation (e.g. the identification of most effective antibiotic combinations for the treatment of stranded cetaceans), and documents a considerable protozoan burden in these animals.

Most significantly however, the paper highlights striking challenges faced by cetaceans in the wild, and pathophysiology consistent with poor oceanic quality and strong anthropogenic burden. The documentation of bacterial populations with multiple antibiotic resistance, and resistance to “last line of defence” antibiotics, is particularly jarring.

 

Questions to the authors (please see response below):

  • Do you believe parasitic burden and antibiotic resistance are nowadays a burden for cetaceans across the globe? Or would it just affect animals living in waters close to areas of high human activity?
  • Could you share some successes and struggles of doing research like this in the Philippines? How can the findings from your study impact policy (of animal conservation, water management, or health), locally and internationally?
  • You have found many animals with parasitic cysts. While the consumption of cetacean meat is illegal in the Philippines, you do envisage a threat of zoonotic transmission. Do you believe marine mammals could represent a reservoir for the resurgence of disease?
  • The current pandemic has highlighted once again the threat represented by animal-to-human viral zoonosis. Is anything known about cetaceans and viruses? Would the collection of viral information be possible from stranded cetaceans?

 

References and further reading

  • Bossart, Gregory D. “Marine mammals as sentinel species for oceans and human health.” Veterinary pathology 48.3 (2011): 676-690.
  • Obusan, Marie Christine M., et al. “Antibiotic Susceptibility Patterns of Bacteria Isolated from Cetaceans Stranded in the Philippines.” Aquatic Mammals 44.5 (2018): 568-579.

Tags: #toxoplasma, antibiotic resistance, cetaceans, marine mammals, mdr, philippines, pmmsn

Posted on: 13th January 2021 , updated on: 14th January 2021

doi: https://doi.org/10.1242/prelights.26953

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Author's response

Professors Marie Christine M. Obusan and Lemnuel V. Aragones shared

1. Do you believe parasitic burden and antibiotic resistance are nowadays a burden for cetaceans across the globe? Or would it just affect animals living in waters close to areas of high human activity?

We believe that parasitic burden and antibiotic resistance nowadays are emerging issues on cetaceans globally. The marine environment in general, serves as sink for terrestrial inputs (e.g., effluents) that carry pathogenic and potentially pathogenic agents and chemicals, including antibiotics. While the effects might be more crucial to, or more easily observed in marine mammal populations closer to areas where there are high human activities, diseases and antibiotic resistance are a concern for pelagic species as well.

 

2. Could you share some successes and struggles of doing research like this in the Philippines? How can the findings from your study impact policy (of animal conservation, water management, or health), locally and internationally?

Research on marine mammals in the Philippines, in general is a struggle. There is not much funding available for this types of research from the national government. Fortunately, we have access to funding from our own university and other foreign organizations. Also, we have been lucky to have more than enough samples from stranded marine mammals as we work closely with the Philippine Marine Mammal Stranding Network (PMMSN) for these types of research on marine mammal health and the like. We use marine mammals as sentinels of ocean health following the One Health paradigm. We believe our results can impact policies on the conservation and management of marine mammal species.

 

3. You have found many animals with parasitic cysts. While the consumption of cetacean meat is illegal in the Philippines, you do envisage a threat of zoonotic transmission. Do you believe marine mammals could represent a reservoir for the resurgence of disease?

The marine mammals have the potential to serve as reservoir of emerging or resurging diseases. Although we know that there are still some people eating marine mammal meat in the Philippines, they are less and probably insignificant in comparison to two decades ago. Also, there is generally lack of scientific information on the life history of these parasitic cysts and their prevalence in the marine environment, thus the need to investigate the specific roles of marine mammals in their transmission.

 

4. The current pandemic has highlighted once again the threat represented by animal-to-human viral zoonosis. Is anything known about cetaceans and viruses? Would the collection of viral information be possible from stranded cetaceans?

This is a great question! There is such thing as the cetacean morbillivirus (CeMV). This is a virus that infects cetaceans, which includes dolphins, porpoises, and whales. So far, three distinct strains have already been identified: dolphin, pilot whale and porpoise morbilliviruses. We have just written a proposal for this endeavour as well, as we would like to expand our examination of our stranded marine mammals in the Philippines.

1 comment

19 hours

Emmanuel Macapagal

This is a great question! There is such thing as the cetacean morbillivirus (CeMV). This is a virus that infects cetaceans, which includes dolphins, porpoises, and whales.” -mY QUESTION IS ON the nature of clinical signs of this in marine mammals because there is a known as Canine Paramyxovirus with Morbillivirus as its genus. Would it be neurologic that might somehow be the cause of “seizures” that cause them to loose their bearings and get adrift and land on shores, dead.

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