Page 866 - The Toxicology of Fishes

846 The Toxicology of Fishes

Field Observations of Dioxin-Like Pathologies in Great Lakes Salmonines

Dioxin-specific pathologies observed in salmonines in the Great Lakes provide further evidence for the
adverse effects of HAH chemicals. Studies that measure survival and growth of Great Lakes lake trout
or other salmonine species relative to concentrations of PCBs, HAHs, and resulting TEQs are critical
to estimate effects of these chemicals on population dynamics; however, survival and growth can be
generic endpoints if specific symptoms were not monitored in a study and, as such, may not provide
the necessary linkages to specific chemicals required for establishment of causality. Chemical-specific
responses have been found at the suborganismal level and help provide evidence for causal linkages
between HAHs and organism-level effects in Great Lakes lake trout. In particular, chemical-specific
pathologies associated with HAHs have been observed in both adult and early life stages of salmonines;
thus, comparisons of observed pathologies in Great Lakes lake trout and other salmonines with dioxin-
like symptoms of toxicity provide helpful diagnostic information for evaluation of cause-and-effect
linkages (Fox, 1991).
A hallmark response of vertebrates to HAHs is induction of CYP1A1. Fish are no exception and
exhibit a strong CYP1A1 response in a variety of tissues after exposure to HAHs (Stegeman and Hahn,
1994; Whyte et al., 2000). Evidence of a response in Great Lakes salmonines to HAH exposure first
came from CYP1A1 induction in the tissues and gametes of lake trout collected in 1981 (Binder and
Lech, 1984). Lake trout embryos spawned from adult lake trout collected from Lake Michigan or Green
Bay had significantly induced aryl hydrocarbon hydroxylase (AHH) activity (CYP1A1 activity) relative
to embryos from hatchery broodstock. Enzymatic characteristics of AHH induction by PCBs and
inhibition by α-naphthoflavone (ANF) in hatchery trout offspring were identical to the enzymatic
characteristics observed in offspring of Lake Michigan lake trout (Binder and Lech, 1984). Additionally,
a reduction in AHH (CYP1A1) induction in offspring from the Lake Michigan lake trout was observed
with increased age of the offspring, consistent with the reductions in PCB content of the offspring and
indicating that dilution of the PCB concentration by growth of the offspring had occurred. Lake trout
are known to be sensitive to CYP1A1 induction by the planar PCBs, such as PCB 126 (3,3′,4,4′,5-
pentachlorbiphenyl), even at doses as low as 0.6 ng/g (Palace et al., 1996). Later in that same decade,
Chinook salmon collected from Lake Michigan in 1987 were observed to have only slightly induced
hepatic EROD activity (Ankley et al., 1989). At the same period in Lake Ontario (the late 1980s), lake
trout were observed to have 6 to 62 times the hepatic AHH activity as lake trout collected from Lake
Superior (Luxon et al., 1987). Lake trout collected from Lake Ontario in the beginning of the 1990s had
only marginally induced EROD activity compared to lake trout collected at the same time from Lake
Superior (Palace et al., 1998). No comprehensive evaluation of CYP1A induction has been conducted
in Great Lakes fish, but the existing data are consistent with the concentration of HAHs measured in
fish over the past three decades. The greatest amount of induction of monooxygenase activity was
observed at the times when the HAH concentrations were highest, and subsequent investigations have
observed decreasing hepatic CYP1A activity that corresponds with decreasing PCBs and other HAHs
(see Figure 21.3) (DeVault et al., 1989; Hickey et al., 2006; Stow et al., 1995).
Hypothyroidism, thyroid hyperplasia, and altered thyroid status have also been observed in trout and
salmon from the Great Lakes. Altered thyroid function is associated with HAH or dioxin-like toxicity
in controlled laboratory exposures (Brown et al., 2004a; Kohn et al., 1996). Thyroid hyperplasia (Moccia
et al., 1981) and altered thyroid hormones (Leatherland and Sonstegard, 1981) have been observed in
several species of Great Lakes salmon from the mid-1970s through the 1990s (Rolland, 2000). Although
other factors can cause thyroid hyperplasia and reductions in circulating thyroid hormones (iodine
deficiency most notably), the existing experimental evidence for Great Lakes salmon suggests that the
observed effects were not due to a general iodine deficiency (Leatherland and Sonstegard, 1984); however,
the evidence that thyroid dysfunction observed in salmon and trout from the Great Lakes was linked to
chemical contamination by HAHs is controvertible. Correlations of contaminant concentrations in Great
Lakes salmon with the spatial extent of thyroid pathogenesis were never established (Leatherland, 1992,
1993; Moccia et al., 1977; Sonstegard and Leatherland, 1982). Additionally, laboratory treatments of
fish with HAHs have not led to thyroid gland pathologies (Brown et al., 2004b; Grinwis et al., 2000;
Leatherland and Sonstegard, 1978, 1979, 1980; Palace et al., 2001), even when thyroid hormone