Tumors in Brown Bullheads in the Chesapeake Bay Watershed: Analysis of Survey Data from 1992 through 2006

Abstract

Liver and skin tumor prevalences in brown bullheads Ameiurus nebulosus have been used in the North American Great Lakes to designate highly contaminated areas of concern and monitor their recovery. Here we interpret the results of six surveys conducted in the Chesapeake Bay watershed between 1992 and 2006, with data for 647 fish. The objective has been to develop an adequate database to critically evaluate the use of tumor prevalence as a habitat quality indicator within the watershed. Surveys featured randomized fish collection; recording of sex, length, weight, and age; and histopathology of all livers and all raised skin lesions. The Bayes information criterion was used to analyze all possible combinations of age, gender, length, and weight as covariates for logistic regression. Length and gender were the covariates that best described liver tumor prevalence. There were no covariates in the model for skin tumor prevalence. In some surveys, biomarkers, such as biliary polynuclear aromatic hydrocarbon (PAH)-like metabolites, hepatic cytochrome P450 activity, and hepatic DNA adducts, were used with sediment and tissue chemistry data to evaluate classes of chemicals as likely contributors to tumor prevalence. We highlight two surveys of the Anacostia River, Washington, D.C. (average = 55% liver tumors, 23% skin tumors), where sediment PAHs, biliary PAH-like metabolites, and hepatic DNA adducts were high, suggesting that PAHs play a major role. We show that logistic regression is an appropriate procedure for comparing "contaminated" versus "reference" locations, and we evaluate the utility of tumor surveys as an environmental indicator for the Chesapeake Bay watershed.

A historical perspective on the “fish tumors or other deformities” beneficial use impairment at Great Lakes Areas of Concern

“…Nevertheless, there is some evidence of a quantitative relationship between sediment total PAH concentrations and bullhead liver neoplasms. Using data from the Chesapeake Bay, Pinkney et al (2009) placed 18 points with paired sediment-liver neoplasm data on a scatterplot and reported a dramatic increase in the prevalence of liver neoplasms beginning at a total sediment PAH concentration of 15 ppm. Baumann (USGS, personal communication) analyzed the decline in liver neoplasm rates in Black River brown bullhead along with declines in sediment total PAH concentrations.…”

“…He recommended 10 ppm total PAH as a sediment remediation goal for the Grand Calumet River (Indiana) AOC. Pinkney et al (2009) also constructed a scatterplot with 18 points with paired skin neoplasm and total PAH data. There was no indication of a threshold or relationship between sediment total PAH concentrations and the prevalence of skin neoplasms.…”

“…In a later study, Pinkney et al (2004a) reported an increased risk of 1.547 times per year for liver neoplasms of any type and no significant (p N 0.05) relationship between age and skin neoplasms. Recently, Pinkney et al (2009) applied logistic regression to analyze the effects of covariates (including length, weight, age, and gender) on liver and skin neoplasms on the entire Chesapeake Bay database of 602 brown bullhead with a total length of at least 260 mm. The researchers used multiple regression procedures to select the model that best fit the data with the least complexity.…”

“…For example, the probability of a female brown bullhead from the South River, MD having a liver tumor increased from about 20% for a 280 mm fish to about 40% for a 320 mm fish. Pinkney et al (2009) noted that these analyses were based on spine-aged fish and suggested that future analysis based on otolith-aged fish may yield a model where age is a significant covariate for liver neoplasms. With respect to skin neoplasms, these authors reported that both length and age were not significant (p N 0.05) covariates.…”

An integrated assessment of sediment remediation in a midwestern U.S. stream using sediment chemistry, water quality, bioassessment, and fish biomarkers

“…High levels of PAHs in sediment have been associated with the development of tumors and lesions in fish [7][8][9]. The singlecell gel electrophoresis method (comet assay) [10] can be used to quantify DNA damage and provide an index of exposure to genotoxic, tumor-inducing chemicals in biological populations, including fish.…”