Page 915 - The Toxicology of Fishes

The Effects of Polycyclic Aromatic Hydrocarbons in Fish from Puget Sound, Washington 895

liver histopathology and a more limited set of biochemical markers in subadult English sole, rock sole,
and starry flounder at all seasonal sampling points (Myers et al., 1992) and relationships among the
various biochemical markers of contaminant exposure in English sole, rock sole, and starry flounder in
specimens of these species sampled at a single time point (Stein et al., 1992).
Although neoplasms were rarely detected in these subadult fish, whose average age was less than 2
years, higher prevalences of the earlier-occurring lesions were found in young sole from contaminated
sites. Prevalences for any of the earlier-occurring lesions were significantly higher at all of the moderately
to severely contaminated sites (Duwamish Waterway, inside Eagle Harbor, inside Everett Harbor, and
Commencement Bay). Confirming earlier results in adult English sole (Myers et al., 1990, 1994, 1998c),
biliary FAC levels were significant risk factors for prevalences of these early lesion categories in logistic
regression analyses. More interestingly, the study also identified induction of hepatic AHH activity as a
significant risk factor for prevalences of all of the early lesion categories, and DNA adduct level as a
significant risk factor for nuclear pleomorphism/hepatic megalocytosis as well as the inclusive early
lesion category.
With the acquisition of additional data on lesion occurrence, DNA adduct levels, and AHH activity in
wild fish, it has been possible to establish hepatic DNA adducts as a significant risk factor for hepatic
lesion occurrence on an individual fish basis. In stepwise logistic regression analyses that accounted for
the potential influences of fish age and sex on the risk of lesion occurrence, hepatic DNA adduct level
was identified as a positively significant (p ≤ 0.05) risk factor for the occurrence of hepatocellular nuclear
pleomorphism and hepatic megalocytosis in English sole, starry flounder, and rock sole and for preneo-
plastic foci of cellular alteration in English sole (Myers et al., 1998b,c). These findings give further
credence to the role of PAH exposure in the etiology of these lesions and suggest that xenobiotic–DNA
adduct formation is integral to the early initiation phase of hepatocarcinogenesis, as well as the induction
of these more prevalent lesions known to occur prior to the development of hepatic neoplasms in fish
and rodent models of hepatocarcinogenesis. Moreover, they support the utility of certain non-neoplastic
hepatic lesions as early indicators of biological damage in subadult and adult fish environmentally exposed
to xenobiotics. Overall, the collective available evidence shows a strong causal relationship between PAH
exposure and hepatic neoplasms and neoplasia-related liver lesions in English sole (Myers et al., 2003).

Reproductive Effects
In addition to toxicopathic liver disease, English sole residing in contaminated areas in Puget Sound also
suffer from various types of reproductive impairment. Field studies conducted in the late 1980s (Johnson
et al., 1988) showed that female English sole from areas with high concentrations of PAHs in sediment
were less likely to enter vitellogenesis and had lower plasma concentrations of the female reproductive
hormone 17β-estradiol than sole with low levels of contaminant exposure (Figure 22.12). At minimally
to moderately contaminated sites within Puget Sound such as Port Susan and Sinclair Inlet, approximately
80 to 90% of adult females underwent gonadal development, while at the Duwamish Waterway and Eagle
Harbor the percentage declined to 40 to 60%. A 1994 field study of English sole from the Hylebos
Waterway in Commencement Bay, a site with high sediment concentrations of CHs and PAHs, yielded
similar results (Johnson et al., 1999). Approximately 55% of adult female sole from the Hylebos Waterway
were vitellogenic, in comparison to 80% of adult sole from Colvos Passage, a nearby reference site. As
in the earlier study, exposure to PAHs was a major risk factor for inhibited ovarian development in adult
sole. English sole from PAH-contaminated areas also display increased ovarian atresia, particularly of
primary oocytes (Johnson et al., 1988, 1997). Increased atresia is associated with a trend toward reduced
egg production and increased egg weight, although the magnitude of the effect is not great. Similarly,
in gravid female dolly varden and yellowfin sole sampled following the Exxon Valdez oil spill, plasma
estradiol concentrations were depressed in fish with high biliary FAC levels (Sol et al., 2000).
Results of these field studies are supported by laboratory experiments showing that pretreatment of
gravid female English sole with extracts of contaminated sediment or crude oil containing high levels
of PAHs decreased levels of endogenous estradiol (Johnson et al., 1995; Stein et al., 1991). Related
experiments suggest that exposure to BaP- or PAH-contaminated sediment may suppress estradiol-
induced vitellogenin production in English sole (Anulacion et al., 1997).