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Discipline
Biological
Keywords
Shark Reef Marine Reserve
Fiji
Cancer
Tumour
Direct Observation
Observation Type
Standalone
Nature
Case study
Submitted
Jun 10th, 2017
Published
Oct 12th, 2017
  • Abstract

    Neoplastic lesions have been described in the literature from a variety of shark species, but the inability to observe morphological changes of a tumour through time remains a challenge. Here, we describe the growth of a proliferation through a 7–year period from a female bull shark (Carcharhinus leucas), characterise the proliferation, and speculate on its origin. Based on macroscopic observation from photographs and videos, the most likely morphological diagnosis is chronic, proliferative gingivitis and cellulitis with necrosis and deformation of lower jaw cartilage due to multiple events of fishing gear embedded in the mandibular angle.

  • Figure
  • Introduction

    Chondrichthyans (sharks, batoids, and chimaeras) have been identified as having a remarkable ability to heal and regenerate from grave injuries such as gill destruction or body wall penetration. In the early 1990s, this ability extended to claims that sharks do not, or rarely, get cancer. This misconception has repeatedly been shown to be inaccurate, with 44 cases of lesions being reported in the Registry of Tumors in Lower Animals in 21 species over 9 families and 6 of the 9 extant chondrichthyan orders. At least 15 of these cases were malignant and some individual sharks have been reported with more than one neoplasm.

    Compared with bony fishes, there is scant literature describing diseases or lesions of chondrichthyans. However, the popularity of sharks as exhibit animals in aquariums with the consequent need for adequate care, increased awareness of conservation issues, and evidence that the epigonal cells of sharks can inhibit growth of mammalian tumour cell lines have recently led to an increased interest in describing tumours from various shark species. However, the two main difficulties with diagnosing tumours are the logistical constraints of obtaining the necessary samples to diagnose the lesion (but see) and the inability to observe morphological changes of a tumour through time.

  • Objective

    Here, regular visits of a female bull shark (Carcharhinus leucas) across multiple years at a site where wildlife tourism occurs provided the rare opportunity to describe the growth of a proliferation through a 7–year period. This individual was identified across the study period based on an injury of the right lower jaw and a growing lesion. Characterisation of the proliferation and speculation on its origin is provided based on macroscopic examination of high-resolution photographs and video footage.

  • Results & Discussion

    Since January 2010, a female bull shark, identified based on a healed injury of its right lower jaw, has been regularly observed at the Shark Reef Marine Reserve. It was observed 67 times between January 1, 2010 and December 31, 2016, typically and most often in the first half of the calendar year (Table 1). Photographs that were taken in January 2010 (Figure 1A, B) and footage from April 2010 (Video 1) showed a small proliferation in the right corner of the shark’s mouth. This region looks like an erosion with a centrally located elongated dark fissure, compatible with a fishing hook or a lesion created by a detached hook. Only little growth, if any, was documented until May–June 2011 (Figure 1C). At the end of May 2011, a fishing lure can be seen attached to the right mandibular corner, with a discolored slightly sunken area of the gingival margin visible anteriorly to the lure (Video 2). The dark hook-compatible structure visible in April 2010 is visible and looks like a deep fissure central to an irregularly outlined wound in the corner of the mouth. By June 2011, the shark had lost the fishing lure and a mild light pink multi-lobulated tissue proliferation can be seen, forming a small, irregularly outlined mass where the fishing lure was attached. With the fishing lure gone, a downward deformation of the gingival area inferiorly to the lesion and lack of dentition in the affected region can be seen. Observations from March 2013 onwards reveal a large red-brown multi-lobulated mass, attached the gingival margin via a narrow, white stalk (Figure 1D–F, Video 3), similar in appearance to the proliferative lesion recently documented in a white shark Carcharodon carcharias. The stalk is long enough to allow the mass to move in and out from the oral cavity (Figure 1G). This female shark has been a regular feeder at the Shark Reef Marine Reserve. Direct observations show that the proliferation wobbles, and when the shark is taking a fish head from the feeder can dangle inside the mouth (Figure 1G). This likely leads to the shark chewing on the proliferation. Footage that was taken on January 5, 2017 shows the proliferation inside the mouth of the shark and seemingly being bitten (Video 4). This was, however, at a provisioning site and such biting on the proliferation might not occur or might occur less frequently during natural predation. The multi-lobulated surface is compatible with chronic proliferative processes including granulation tissue and fibrosis, but a neoplastic process cannot be excluded. The mandibular angle is deformed and ulcerated, the central fissure is still visible, and the skin adjacent to the lesion is irregularly pitted indicating of underlying remodeling processes within the jaw. By April 2014, the lesion is similar to March 2013, but a fishing hook can be seen embedded in the lower jaw anteriorly to the mass. In videos from January 2017, the pedunculated mass seems similar to 2014, but the lower jaw appears to have a more pronounced angular ventral deformity.

    Origin of the proliferation

    Based on macroscopic observation from photographs and videos, the most likely morphological diagnosis is chronic, proliferative gingivitis and cellulitis with necrosis and deformation of lower jaw cartilage due to multiple events of fishing gear embedded in the right mandibular angle. The persistent foreign objects (fishing hook or lure) resulted in a fibro-proliferative tissue response that created a pedunculated mass compatible with fibropapilloma. Histological evaluation of multiple biopsies or serial sectioning of the entire mass is required for a more precise diagnosis i.e. confirmation of a neoplastic transformation within the affected tissues. Based on observations of tissue responses in sharks with retained fishing gear or chronic lesions due to attached gut parasites, we speculate that a neoplastic transformation of the affected tissues is likely. Although gingival neoplasms have been reported in sharks previously, this is the first documentation that links them causally to retained fishing gear and expands the types of lesions caused by such gear in sharks.

  • Alt. Explanations

    Alternatively, the lesion might be a proliferative papillomatous lesion due to a viral or bacterial infection. Herpes and Papilloma viruses have been described in marine turtles and fishes. In the case of bacterial infection, the most likely cause of granulomatous infections in fish are mycobacteria. Tunas, which are fed to bull sharks at the Shark Reef Marine Reserve, may be infected with mycobacteria, and an infection at the gingiva, which may be injured during feeding and exposed to infectious tissue, is considered a possibility.

  • Conjectures

    It will be interesting to observe the development of the proliferation in the coming years. In order to do this best, citizen scientist diving in the Shark Reef Marine Reserve are invited to share their photographs and videos of the female shark with the authors.

  • Methods

    All observations were made between January 2010 and January 2017 at the Shark Reef Marine Reserve, a shark diving site on the southern coast of Viti Levu, Fiji​. At this site, sharks are hand-fed, allowing to take close-up observations, photographs, and footage. We used reports from and footage taken by staff members of a local dive shop who have been diving the site 3–5 times per week since 2002. The description and characterisation of the proliferation are based on high-resolution photographs taken by professional underwater photographers at the Shark Reef Marine Reserve.

  • Acknowledgements

    The authors wish to thank Sam Cahir and Martin Graf for use of the photographs and Mike Neumann for use of the video footage.

  • Ethics statement

    Not applicable.

  • References
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    Matters Select22/30

    Multi-year growth progression of a neoplastic lesion on a bull shark (Carcharhinus leucas)

    Abstractlink

    Neoplastic lesions have been described in the literature from a variety of shark species, but the inability to observe morphological changes of a tumour through time remains a challenge. Here, we describe the growth of a proliferation through a 7–year period from a female bull shark (Carcharhinus leucas), characterise the proliferation, and speculate on its origin. Based on macroscopic observation from photographs and videos, the most likely morphological diagnosis is chronic, proliferative gingivitis and cellulitis with necrosis and deformation of lower jaw cartilage due to multiple events of fishing gear embedded in the mandibular angle.

    Figurelink

    Figure 1. Growth progression of a proliferation through a 7-year period.

    A,B Carcharhinus leucas photographed on January 10, 2010, C June 7, 2011, D March 24, 2013, E April 26, 2014, F June 3, 2016. The healed injury (broken jaw) is visible in A–F. G Sequence showing the proliferation dangling inside the mouth when the shark takes a fish head from the feeder. Photographs taken on March 24, 2013.

    Introductionlink

    Chondrichthyans (sharks, batoids, and chimaeras) have been identified as having a remarkable ability to heal and regenerate from grave injuries such as gill destruction or body wall penetration[1][2][3]. In the early 1990s, this ability extended to claims that sharks do not, or rarely, get cancer[4][5]. This misconception has repeatedly been shown to be inaccurate, with 44 cases of lesions being reported in the Registry of Tumors in Lower Animals in 21 species over 9 families and 6 of the 9 extant chondrichthyan orders. At least 15 of these cases were malignant and some individual sharks have been reported with more than one neoplasm[6].

    Compared with bony fishes, there is scant literature describing diseases or lesions of chondrichthyans. However, the popularity of sharks as exhibit animals in aquariums with the consequent need for adequate care[7], increased awareness of conservation issues[8], and evidence that the epigonal cells of sharks can inhibit growth of mammalian tumour cell lines[9] have recently led to an increased interest in describing tumours from various shark species. However, the two main difficulties with diagnosing tumours are the logistical constraints of obtaining the necessary samples to diagnose the lesion (but see[10]) and the inability to observe morphological changes of a tumour through time.

    Objectivelink

    Here, regular visits of a female bull shark (Carcharhinus leucas) across multiple years at a site where wildlife tourism occurs[11] provided the rare opportunity to describe the growth of a proliferation through a 7–year period. This individual was identified across the study period based on an injury of the right lower jaw and a growing lesion. Characterisation of the proliferation and speculation on its origin is provided based on macroscopic examination of high-resolution photographs and video footage.

    Results & Discussionlink

    Since January 2010, a female bull shark, identified based on a healed injury of its right lower jaw, has been regularly observed at the Shark Reef Marine Reserve. It was observed 67 times between January 1, 2010 and December 31, 2016, typically and most often in the first half of the calendar year (Table 1). Photographs that were taken in January 2010 (Figure 1A, B) and footage from April 2010 (Video 1) showed a small proliferation in the right corner of the shark’s mouth. This region looks like an erosion with a centrally located elongated dark fissure, compatible with a fishing hook or a lesion created by a detached hook. Only little growth, if any, was documented until May–June 2011 (Figure 1C). At the end of May 2011, a fishing lure can be seen attached to the right mandibular corner, with a discolored slightly sunken area of the gingival margin visible anteriorly to the lure (Video 2). The dark hook-compatible structure visible in April 2010 is visible and looks like a deep fissure central to an irregularly outlined wound in the corner of the mouth. By June 2011, the shark had lost the fishing lure and a mild light pink multi-lobulated tissue proliferation can be seen, forming a small, irregularly outlined mass where the fishing lure was attached. With the fishing lure gone, a downward deformation of the gingival area inferiorly to the lesion and lack of dentition in the affected region can be seen. Observations from March 2013 onwards reveal a large red-brown multi-lobulated mass, attached the gingival margin via a narrow, white stalk (Figure 1D–F, Video 3), similar in appearance to the proliferative lesion recently documented in a white shark Carcharodon carcharias[10]. The stalk is long enough to allow the mass to move in and out from the oral cavity (Figure 1G). This female shark has been a regular feeder at the Shark Reef Marine Reserve. Direct observations show that the proliferation wobbles, and when the shark is taking a fish head from the feeder can dangle inside the mouth (Figure 1G). This likely leads to the shark chewing on the proliferation. Footage that was taken on January 5, 2017 shows the proliferation inside the mouth of the shark and seemingly being bitten (Video 4). This was, however, at a provisioning site and such biting on the proliferation might not occur or might occur less frequently during natural predation. The multi-lobulated surface is compatible with chronic proliferative processes including granulation tissue and fibrosis, but a neoplastic process cannot be excluded. The mandibular angle is deformed and ulcerated, the central fissure is still visible, and the skin adjacent to the lesion is irregularly pitted indicating of underlying remodeling processes within the jaw. By April 2014, the lesion is similar to March 2013, but a fishing hook can be seen embedded in the lower jaw anteriorly to the mass. In videos from January 2017, the pedunculated mass seems similar to 2014, but the lower jaw appears to have a more pronounced angular ventral deformity.

    Origin of the proliferation

    Based on macroscopic observation from photographs and videos, the most likely morphological diagnosis is chronic, proliferative gingivitis and cellulitis with necrosis and deformation of lower jaw cartilage due to multiple events of fishing gear embedded in the right mandibular angle. The persistent foreign objects (fishing hook or lure) resulted in a fibro-proliferative tissue response that created a pedunculated mass compatible with fibropapilloma. Histological evaluation of multiple biopsies or serial sectioning of the entire mass is required for a more precise diagnosis i.e. confirmation of a neoplastic transformation within the affected tissues. Based on observations of tissue responses in sharks with retained fishing gear[13] or chronic lesions due to attached gut parasites[14], we speculate that a neoplastic transformation of the affected tissues is likely. Although gingival neoplasms have been reported in sharks previously[15], this is the first documentation that links them causally to retained fishing gear and expands the types of lesions caused by such gear in sharks[16].

    Alternative Explanationslink

    Alternatively, the lesion might be a proliferative papillomatous lesion due to a viral or bacterial infection. Herpes and Papilloma viruses have been described in marine turtles and fishes[17]. In the case of bacterial infection, the most likely cause of granulomatous infections in fish are mycobacteria[18]. Tunas, which are fed to bull sharks at the Shark Reef Marine Reserve[19], may be infected with mycobacteria, and an infection at the gingiva, which may be injured during feeding and exposed to infectious tissue, is considered a possibility.

    Conjectureslink

    It will be interesting to observe the development of the proliferation in the coming years. In order to do this best, citizen scientist[20] diving in the Shark Reef Marine Reserve are invited to share their photographs and videos of the female shark with the authors.

    Methodslink

    All observations were made between January 2010 and January 2017 at the Shark Reef Marine Reserve, a shark diving site on the southern coast of Viti Levu, Fiji[11]​. At this site, sharks are hand-fed, allowing to take close-up observations, photographs, and footage. We used reports from and footage taken by staff members of a local dive shop who have been diving the site 3–5 times per week since 2002. The description and characterisation of the proliferation are based on high-resolution photographs taken by professional underwater photographers at the Shark Reef Marine Reserve.

    Acknowledgementslink

    The authors wish to thank Sam Cahir and Martin Graf for use of the photographs and Mike Neumann for use of the video footage.

    Conflict of interestlink

    The authors declare no conflicts of interest.

    Ethics Statementlink

    Not applicable.

    No fraudulence is committed in performing these experiments or during processing of the data. We understand that in the case of fraudulence, the study can be retracted by Matters.

    Referenceslink
    1. Towner Alison, Smale Malcolm, Jewell Oliver
      Boat-Strike Wound Healing in Carcharodon carcharias
      Global Perspectives on the Biology and Life History of the White Shark, 2012, pages 77-84 DOI: 10.1201/b11532-8chrome_reader_mode
    2. Chin Andrew, Mourier Johann, Rummer Jodie L.
      Blacktip reef sharks (Carcharhinus melanopterus) show high capacity for wound healing and recovery following injury
      Conservation Physiology, 3/2015, page cov062 DOI: 10.1093/conphys/cov062chrome_reader_mode
    3. Kessel S., Fraser J., van Bonn W., Brooks J., Guttridge T., Hussey N., Gruber S.
      Transcoelomic expulsion of an ingested foreign object by a carcharhinid shark
      Marine & Freshwater Research, in press/2017 chrome_reader_mode
    4. Lane I., Comac L.
      Sharks don’t get cancer
      Garden City Park, NY, Avery Publishing Group, 1992 chrome_reader_mode
    5. Lane I., Comac L.
      Sharks still don’t get cancer
      Garden City Park, NY, Avery Publishing Group, 1996 chrome_reader_mode
    6. Ostrander, Gary K., Cheng, Keith C., Wolf, Jeffrey C., Wolfe, Marilyn J.
      Shark Cartilage, Cancer and the Growing Threat of Pseudoscience
      Cancer Research, 64/2004, pages 8485-8491 DOI: 10.1158/0008-5472.can-04-2260chrome_reader_mode
    7. Smith M., Warmolts D., Thoney D., Hueter R. (editors)
      The Elasmobranch Husbandry Manual: Captive Care of Sharks, Rays and their Relatives
      Special Publication of the Ohio Biological Survey, 2004, pages 201-226 chrome_reader_mode
    8. Simpfendorfer C. A., Heupel M. R., White W. T., Dulvy N. K.
      The importance of research and public opinion to conservation management of sharks and rays: a synthesis
      Marine and Freshwater Research, 62/2011, page 518 DOI: 10.1071/mf11086chrome_reader_mode
    9. Walsh C. J., Luer C. A., Bodine A.B.,more_horiz, Gasparetto M.
      Elasmobranch immune cells as a source of novel tumor cell inhibitors: Implications for public health
      Integrative and Comparative Biology, 46/2006, pages 1072-1081 DOI: 10.1093/icb/icl041chrome_reader_mode
    10. Huveneers C, Klebe S, Fox A,more_horiz, Z Michael M
      First histological examination of a neoplastic lesion from a free-swimming white shark, Carcharodon carcharias L.
      Journal of Fish Diseases, 39/2016, pages 1269-1273 DOI: 10.1111/jfd.12458chrome_reader_mode
    11. Brunnschweiler Juerg M., Abrantes Kátya G., Barnett Adam
      Long-Term Changes in Species Composition and Relative Abundances of Sharks at a Provisioning Site
    12. Robbins Rachel, Bruce Barry, Fox Andrew
      First reports of proliferative lesions in the great white shark,Carcharodon carchariasL., and bronze whaler shark,Carcharhinus brachyurusGünther
      Journal of Fish Diseases, 37/2013, pages 997-1000 DOI: 10.1111/jfd.12203chrome_reader_mode
    13. Borucinska J D, Harshbarger J C, Bogicevic T
      Hepatic cholangiocarcinoma and testicular mesothelioma in a wild-caught blue shark, Prionace glauca (L.)
      Journal of Fish Diseases, 26/2003, pages 43-49 DOI: 10.1046/j.1365-2761.2003.00435.xchrome_reader_mode
    14. Borucinska J, Dunham A
      Lesions associated with attachment of the cestodeTentaculariasp. to the duodeno-spiral junction in the blue shark,Prionace glauca(L.), with a description of the intestinal morphology of the shark
      Journal of Fish Diseases, 23/2000, pages 353-359 DOI: 10.1046/j.1365-2761.2000.00253.xchrome_reader_mode
    15. Borucinska J D, Harshbarger J C, Reimschuessel R, Bogicevic T
      Gingival neoplasms in a captive sand tiger shark, Carcharias taurus (Rafinesque), and a wild-caught blue shark, Prionace glauca (L.)
      Journal of Fish Diseases, 27/2004, pages 185-191 DOI: 10.1111/j.1365-2761.2004.00532.xchrome_reader_mode
    16. Adams D H, Borucinska J D, Maillett K,more_horiz, Sander T E
      Mortality due to a retained circle hook in a longfin mako sharkIsurus paucus(Guitart-Manday)
      Journal of Fish Diseases, 38/2014, pages 621-628 DOI: 10.1111/jfd.12277chrome_reader_mode
    17. Lu Yuanan, Yu Qigui, Zamzow Jill P.,more_horiz, Yanagihara Richard
      Detection of Green Turtle Herpesviral Sequence in Saddleback WrasseThalassoma duperrey: A Possible Mode of Transmission of Green Turtle Fibropapilloma
      Journal of Aquatic Animal Health, 12/2000, pages 58-63 DOI: 10.1577/1548-8667(2000)012<0058:dogths>2.0.co;2chrome_reader_mode
    18. Lescenko P., Matlova L., Dvorska L., Bartos M., Vavra O., Navratil S., Novotny L., Pavlik I.
      Mycobacterial infection in aquarium fish
      Veterinarni Medicina, 48/2003, pages 71-79 chrome_reader_mode
    19. Brunnschweiler J. M., Payne N. L., Barnett A.
      Hand feeding can periodically fuel a major portion of bull shark energy requirements at a provisioning site in Fiji
    20. Silvertown Jonathan
      A new dawn for citizen science
      Trends in Ecology & Evolution, 24/2009, pages 467-471 DOI: 10.1016/j.tree.2009.03.017chrome_reader_mode
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