Melanomas in brown bullhead from the Lake Memphremagog, Quebec

Brown bullhead captured in Lake Memphrémagog with a large elevated black mass diagnosed as a cutaneous melanoma (photo credit: Jean-Sébastien Messier).

In July 2023, brown bullheads were captured in Lake Memphremagog, Quebec, as part of a research project by the Ministère de l’Environnement, de la Lutte contre les changements climatiques, de la Faune et des Parcs. Five of the captured bullheads exhibited black spots or masses on their skin, including the flanks, head, opercula, fins, or lips. These skin lesions varied in size and shape, appearing raised or smooth, and could be solitary or multiple (photo 1). Despite the presence of these masses, the affected fish seemed to be in good condition.

Histologic section of the lip of a brown bullhead affected by a melanoma. Notice the marked invasion of the epidermis, dermis, muscles, and bone structures (dense pink material) by numerous neoplastic melanocytes (black cells).

Microscopic examination of tissue samples for analysis showed proliferative changes in melanocytes (pigmented cells) in the skin. Some of the proliferative lesions involved both the epidermis and superficial dermis, with larger masses characterized by extensive destruction of the epidermis and infiltration of subcutaneous tissues, muscles, and even bone by numerous melanocytes (photo 2). The melanocytic cells often exhibited characteristics suggestive of neoplastic cells, such as a decrease in melanin pigment density. The histologic appearance of these masses is characteristic of melanomas, potentially malignant tumours arising from melanocytes.

Interestingly, a research group from the Vermont Fish and Wildlife Department documented this syndrome in Lake Memphrémagog in 2019, reporting similar lesions in 31% of adult brown bullheads captured in recent years.1 This suggests a marked increase in the occurrence of this condition in the water body. While occasional skin tumours in wild fish are observed, the simultaneous occurrence of multiple cases of the same type of tumour in a species in a water body suggests exposure to one or more risk factors.

Over the past decade, proliferative lesions of melanocytes have been reported in various populations of wild fish. In some cases, such as in species of groupers in Australia, it is suggested that increased exposure to ultraviolet (UV) radiation could be the cause of these lesions’ development.5 The fact that Lake Memphrémagog is generally a shallow lake (depth at capture sites ranging from >2 to 4 metres) could enhance fish exposure to UV, potentially explaining the high occurrence of this condition at these sites. There is also consideration of the possible impact of the recent introduction of the invasive zebra mussel into this lake. This mussel species, which reproduces rapidly, filters large amounts of water, leading to increased water transparency. The presence of these mussels could therefore elevate fish exposure to UV. However, it is essential to mention that documentation of melanomas in brown bullheads in Lake Memphrémagog (2014) predates the first observation of zebra mussels in this lake (2017). Consequently, the introduction of this mussel species cannot account for the onset of these cancers. Nevertheless, the proliferation of these exotic mussels could potentially exacerbate this issue if UV radiation indeed plays a role in the development of these tumours.

Smallmouth bass captured in Lake Memphrémagog showing typical lesions of melanosis, also known as “blotchy bass syndrome” (photo credit: Florent Philibert).

Hyperplastic lesions of melanocytes (known as “blotchy bass syndrome”) have also been documented in several populations of largemouth bass in North America, including in Lake Memphrémagog (photo 3). A recent study on this condition revealed the presence of a virus (adomavirus) in largemouth bass affected by these lesions.2 Although the exact role of this virus in the development of these lesions remains uncertain, this observation supports the hypothesis that the melanomas observed in brown bullheads could indeed have a viral origin.

Finally, it is necessary to mention a possible link between these neoplastic changes and exposure to various carcinogenic chemical contaminants. For instance, a correlation between the prevalence of proliferative melanocyte lesions has been proposed in different fish species in Japan.4 Additionally, exposure to organochlorine pesticides and polychlorinated biphenyls (PCBs) has been identified as a risk factor for melanoma development in people.3

Due to the severity of several of these lesions, it is reasonable to assume that this condition will lead to mortalities in affected brown bullheads. However, the impact of this emerging neoplastic syndrome on the population dynamics of brown bullheads in Lake Memphrémagog remains uncertain.

Studies are underway to specify the cause of this emerging neoplasm in this system, which will help us better understand the impact of environmental changes on this new syndrome.

References:

  1. Blazer VS, Shaw CH, Smith CR, Emerson P, Jones T. Malignant melanoma of brown bullhead (Ameiurus nebulosus) in Lake Memphremagog, Vermont/Quebec. J Fish Dis. 2020;43(1):91-100.
  2. Blazer VS, Young KT, Smith GD, Sperry AJ, Iwanowicz LR. Hyperpigmented melanistic skin lesions of smallmouth bass Micropterus dolomieu from the Chesapeake Bay watershed. Dis Aquat Organ. 2020;139:199-212.
  3. Gallagher RP, Macarthur AC, Lee TK, Weber JP, Leblanc A, Mark Elwood J, Borugian M, Abanto Z, Spinelli JJ. Plasma levels of polychlorinated biphenyls and risk of cutaneous malignant melanoma: a preliminary study. Int J Cancer. 2011;128(8):1872-1880.
  4. Kinae N, Yamashita M, Tomita I, Kimura I, Ishida H, Kumai H, Nakamura G. A possible correlation between environmental chemicals and pigment cell neoplasia in fish. Sci Total Environ. 1990;94(1-2):143-153.
  5. Sweet M, Kirkham N, Bendall M, Currey L, Bythell J, Heupel M. Evidence of melanoma in wild marine fish populations. PloS one. 2012;7(8):e41989.

Olivier Skelling et Stéphane Lair, CWHC-Quebec.

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