In the Puget Sound studies, it was noted that the concentrations
of persistent organic chemicals, e.g., PCB's, were higher in fish
than in sediments; however, concentrations of labile organic
chemicals, e.g., PAH's, were higher in sediments than in fish. For
this reason, tissue contaminant levels were not used as evidence
of exposure to chemicals in sediments. The prevalence of liver
neoplasms in Puget Sound English sole was positively correlated
with the concentrations of PAH's in bottom sediments (10).

Recent studies of organic pollutants from Boston Harbor (4, 16)
have revealed that levels are high. In one study (4) total PCB
concentrations ranged from 70 to 330 ppb (mean 140 ppb). These
values are comparable to.those found in other polluted harbor
sediments, but are lower than those found in the Arthur Kill and
Newark Bay, New York, or New Bedford Harbor. PAH concentrations
in Boston Harbor ranged from 2.4 to 880 ppm (mean 180 ppm). The
high mean value is the result of a single high value at a sediment
station sampled in the northern part of the harbor (near Deer
Island). The range in harbor sediment PAH concentrations excluding
this single value is 2.4-6.5 ppm (mean 4.4 ppm), approximately
twice as high as PAH concentrations in the New York Bight apex.
Computation of a Fossil Fuel Pollution Index (FFPI) (2, 3) which
qualified the PAH values as either due to fossil PAH's (petroleum,
coal) or combustion PAH's (fossil fuel combustion products,
airborne particulates) indicates that there are multiple sources
of sediment PAH's in the harbor. At the station near Deer Island,
the sources of PAH's are approximately equal, i.e., both petroleum
and combustion hydrocarbons.

Concentrations of coprostanol, a steroid whose presence in the
harbor signifies contamination by sewage effluents, are high (1-16
ppm) and comparable to those found in the sewage sludge disposal
site in the New York Bight. The highest coprostanol value (15.9
ppm) was obtained at the sediment station near Deer Island.
Coprostanol/total steroid ratios also are highest at this station,
signifying that the sterol composition of the sediment sample is
approximating that of pure sewage sludge.

In the second study (16) substantially higher concentrations of
PCB's and PAH's were found in Boston Harbor sediments. The mean
concentration (1984, 1985) of total PCB's was approximately 8000
ppb. In sediments from western Long Island Sound, Narragansett Bay
(RI), and eastern Long Island Sound mean total PCB's were
approximately 170 ppb, 220 ppb and 5 ppb, respectively. The mean
concentration of total PAH's in Boston Harbor sediments for the
same period was approximately 17,000 ppb. In sediments from
western Long Island Sound, Narragansett Bay (RI), and eastern Long
Island Sound mean total PAH's were approximately 4400 ppb, 2200
ppb, and 100 ppb, respectively.

Few organic chemical analyses of Boston Harbor winter flounder
hepatic tissues have been made. Recent determinations (dry weight)
disclosed substantially elevated contaminant levels (total
chlorinated pesticides = 1078 ppb; DDT = 827 ppb; PCB = 10,487 ppb)

-10-


importance and size. The winter flounder fishery is by far the
largest in the harbor and is of substantial economic importance to
the area. Although winter flounder are caught by recreational
fishermen in the harbor, when the fish migrate to nearby
Massachusetts Bay they are caught in trawls by commercial
fishermen.

The primary economically valuable crustacean resource in Boston
Harbor is the American lobster (Homarus americanus). Lobsters are
trapped throughout the harbor between April and October.

The soft-shell clam (Mya arenaria) is the most economically
important molluscan resource in the harbor. Harvesting of clams
from areas with coliform most probable numbers (MPN) of 71-700/100
ml is restricted and clams must be depurated before sale; areas
where coliform MPN exceed 700/100 ml are closed to clamming.

The Fish

Winter flounder can be found from Newfoundland to the Chesapeake
Bay; however, individual fish have been captured as far north as
Labrador and as far south as Georgia (1).

Winter flounder are estuarine dependent and spend a major part of
each year in shallow nearshore waters. Their seaward migrations
are mediated by changes in water temperature and determine the
abundance and distribution of the fish in all coastal areas,
including Boston Harbor (8). Winter flounder north of Cape Cod
seek lower temperatures in deeper waters when inshore temperatures
are unusually high in summer, and higher temperatures in deeper
waters when inshore temperatures are unusually low in winter.
Sexually mature fish migrate to shallow breeding areas, 2-6 m (7-20
ft) deep, in the fall and winter and spawn in late winter through >
early spring. Winter flounder from Massachusetts are sexually
mature when they are 3-4 yr old. Young fish remain in shallow
inshore waters (nursery grounds) and do not migrate.

The winter flounder commercial fishery is conducted almost
exclusively with otter trawls in the spring and fall. In 1983,
the total U.S. catch of winter flounder was 14,967.7 metric tons
(mt) valued at 15,795,000 dollars (Thompson; pers. comm. ). The
New England catch (Connecticut, Maine, Massachusetts, New
Hampshire, Rhode Island) was 14,147.9 mt, the Middle Atlantic catch
(Delaware, New Jersey, New York) was 794.4 mt, and the Chesapeake
catch (Maryland, Virginia) was 24.5 mt. The winter flounder catch
in Massachusetts was 10,642.2 mt valued at 11,557,000 dollars. The
Massachusetts landings constituted 64.6% of the U.S. total in
weight and 73.1% of the U.S. total in dollars; 90.2% (8,729.5 mt)

‘Thompson, B.G.; U.S. Dept. of Commerce, NOAA, National Marine
Fisheries Service, Office of Data and Information Management,
National Fishery Statistics Program, Washington, DC 20235.

-4-


REFERENCES CITED

1. Bigelow, H.B., and W.C. Schroeder. 1953. Fishes of the Gulf
of Maine. Fish. Bull., U.S. 53. 557 pp.

2. Boehm, P. 1983a. Estuarine-continental shelf and benthic-
water column coupling of organic pollutants in the New York Bight
region. Can. J. Fish. Aquat. Sci. 40: 262.

3. Boehm, P. 1983b. Chemical contaminants in northeast United
States marine sediments. NOAA Tech. Rep. NOS 99. NOAA Nat.
Ocean Serv., Rockville, MD. 82 pp.

4. Boehm, P.D., W. Steinhauer, and J. Brown. 1984. Organic
pollutant biogeochemistry studies northeast U.S. marine
environment. Battelle New England Mar. Res. Lab. Final Rep.
Contr. No. NA-83-FA-C-00022 to NOAA Nat. Mar. Fish. Serv.,
Highlands, N.J. 61 pp.

5. Consensus Committee. 1984. Summary and recommendations; a
consensus report, pp. 397-404. In K.L. Hoover, ed., Use of small
fish species in carcinogenicity testing. Nat. Cancer Inst.
Monogr. 65.

6. Deys, B.F. 1969. Papillomas in the Atlantic eel, Anguilla
vulgaris, pp. 187-193. In C.J. Dawe and J.C. Harshbarger, eds.,
A symposium on neoplasms and related disorders of invertebrate
and lower vertebrate animals. Nat. Cancer. Inst. Monogr. 31.

7. + ‘Falkmer, S., S. Marklund, P.E. Mattson, and C. Rappe. 1977.
Hepatomas and other neoplasms in the Atlantic hagfish (Myxine
glutinosa): a histopathologic and chemical study. Ann. N.Y.
Acad. Sci. 298: 342-355.

8. Howe, A.B., and P.G. Coates. 1975. Winter flounder
movements, growth, and mortality off Massachusetts. Trans. Am.
Fish. Soc. 104: 13-29.

9. Krahn, M.M., M.S. Meyers, D.G. Burrows, and D.C. Malins.
1984. Determination of metabolites of xenobiotics in the bile of
fish from polluted waterways. Xenobiotica 14: 633-646.

10. Malins, D.C., B.B. McCain, D.W. Brown, S. Chan, M.S. Meyers,
J.T. Landahl, P.G. Prohaska, A.J. Freidman, L.D. Rhodes, D.G.
Burrows, W.D. Gronlund, and H.O. Hodgins. 1984. Chemical
pollutants in sediments and diseases of bottom-dwelling fish in
Puget Sound, Washington. Environ. Sci. Technol. 18: 705-713.

11. McCain, B.B., K.V. Pierce, S.R. Wellings, and B.S. Miller.

1977. Hepatomas in marine fish from an urban estuary. Bull.
Environ. Contam. Toxicol. 18: 1-2.

-14-


BIBLIOGRAPHIC INFORMATION

PB89- 139737

Report Nos: NOAA~TM-NMFS~F/NEC-61

Title: Fish as Sentinels of Environmental Health.
Date: Sep 88

Authors: R. A. Murchelano.

Performing Organization: National Marine Fisheries Service, Woods Hole, MA.
Northeast Fisheries Center.

Type of Report and Period Covered: Technical memo.,

NTIS Field/Group Codes: 68D, 47D, 48G
Price: PC AQ3/MF AOL

Availability: Available from the National Technical Information Service,
Springfield, VA. 22161

Number of Pages: 23p

Keywords: *Runoff, *Flatfishes, “Water pollution, “Boston Harbor, Indicator
species, Animal diseases, Hepatitis, Malignant neoplasms, Hydrocarbons, Polycyclic
compounds, Chlorine organic compounds, Biphenyl, *Pseudopleuronectes americanus,
Flounder, Polychlorinated biphenyls, Biphenyl/chloro.

Abstract: Boston Harbor, Massachusetts, is polluted by storm water runoff,
municipal wastewater, and sewage sludge, as well as riverborne domestic and
industrial pollutants, and introductions characteristic of and related to the
sustained heavy commercial ship traffic in the port. Shallow areas of the inner
harbor provide suitable spawning and nursery areas for winter flounder
(Pseudopleuronectes americanus). The harbor contains large numbers of winter
flounder during most of the year and is virtually a sanctuary for the species since
commercial fishing is prohibited. Recent disease surveys have shown that harbor
winter flounder have a high prevalence of gross and microscopic hepatic lesions,
including carcinomas. Although harbor sediments contain high concentrations of
polycyclic aromatic hydrocarbons (PAH) and polychlorinated biphenyls (PCB),
presently the evidence ascribing either one of these organic chemicals as a direct
cause of the neoplastic lesions observed is circumstantial.


(15). Total hepatic chlorinated pesticides in winter founder from
western Long Island Sound, Narragansett Bay (RI), and eastern Long
Island Sound were 282 ppb, 119 ppb and 101 ppb, respectively.
Hepatic DDT levels were 105 ppb, 105 ppb and 49 ppb and hepatic PCB
levels were 3222 ppb, 221 ppb and 1577 ppb, respectively in livers
of winter flounder from the aforementioned areas. Livers of winter
flounder from Great Bay, New Jersey, a relatively clean area, had
a median PCB concentration (wet weight) of 0.89 ppm (18); however,
median PCB concentrations in livers of winter flounder with fin rot
from Sandy Hook/Raritan Bays, New Jersey, and the New York Bight
apex, all degraded areas, were 4.2 ppm and 2.8 ppm, respectively.
No analyses of hepatic PAH content of Boston Harbor winter flounder
have been made. Hepatic tissue of winter flounder contains
cytochrome P-450 dependent mixed-function oxydases (MFO) (22, 23);
therefore, the PAH's themselves may not be detectable, but rather
their metabolic derivatives. Concentrations of winter flounder
hepatic microsomal MFO and other enzymes involved in election
transport were generally less than in mammals (mice), but were
capable of transforming PAH's to mutagenic metabolites.
Biochemical studies conducted by the above authors (22) led them
to conclude that, "the results indicate that coastal marine fishes
may be at a risk to carcinogenic aromatic hydrocarbons in marine
sediments".

Although relatively little research has been conducted to determine
the cause of Boston Harbor winter flounder neoplasms, several years
of research on hepatic carcinoma and other hepatic lesions of
English sole from Puget Sound revealed positive correlations (p <
0.003) between the numbers of total hepatic lesions and both PAH's
and metals in sediments. The number of neoplasms, however, was
positively correlated only to PAH concentrations in sediments (10).
Positive correlations were not found with chlorinated hydrocarbons.
Additional studies disclosed that the relative amounts of
benzo(a)pyrene (BAP) 7,8 diol (the penultimate carcinogen of BAP)
metabolized by English sole from BAP are higher than in rat liver.
Sole from polluted areas had concentrations of bile metabolites
(fluorescence spectra compatible with naphthalene, phenanthrene,
and BAP) that were substantially higher than in bile of sole from
reference sites (9). Fish with liver lesions from polluted areas
had significantly higher concentrations of metabolites with
BAP-like fluorescence than fish without liver lesions. Although
these studies seem to implicate PAH's as the cause of the hepatic
neoplasms observed, the large number of chemicals in polluted
sediments with unknown effects, and the complexity ‘of the
biological processes themselves, dictate caution in the
interpretation of the data.

The Significance

The consequences of hepatic carcinoma for winter flounder
populations presently are unknown. The majority of fish with
hepatic neoplasms appear as robust as those without such neoplasms;
however, objective estimates of "condition" of healthy and diseased
fish have not been made. It also is not known if the ages of the

-ll- -


ACKNOWLEDGMENTS

I thank Philip Coates, Lee Bridges, Vincent Durso, Louis Emerald,
and Shirley Mitchell of the Massachusetts Division of Marine
Fisheries, and Harriet Diamond of the Massachusetts Office of
Coastal Zone Management for assistance in obtaining fish from
Boston Harbor. I also thank Clyde Dawe, John Harshbarger, Harold
Steward, John Strandberg, Jerry Ward, and Martin Newman for advice
and counsel in the interpretation of the microscopic lesions. I
thank Joyce Evans and Linda Despres-Patanjo for assistance in the
collection and preparation of tissues for microscopic study.

-13-


liver of winter flounder

The hepatocytes are poorly formed

‘i

ca ae
ere et
Ber

and pleomorphic and the tumor has a solid appearance.

Hepatocellular carcinoma in

from Boston Harbor.

3.

igure

F




NOAA Technical Memorandum NMFS-F/NEC-61

This TM series is used for documentation and timely communication of preliminary results, interim
reports, or special purpose information, and has not received complete formal review, editorial control,

ordetailed editing.

Fish as Sentinels
of Environmenial Health

Robert A. Murchelano
Woods Hole Lab., National Marine Fisheries Service, Woods Hole, MA 02543

U. S. DEPARTMENT OF COMMERCE
C. William Verity, Secretary

National Oceanic and Atmospheric Administration
William E. Evans, Administrator

National Marine Fisheries Service
James W. Brennan, Assistant Administrator for Fisheries

Northeast Fisheries Center
Woods Hole, Massachusetts

September 1988

-l-@




(7 og WS 8

BN ane

Figure 4. Cholangiocellular carcinoma. The proliferating
cells form structures which resemble bile ducts.
‘Arrows define the advancing edge of the lesion.

-9-


Abstract... .
Introduction . .
The Environment
The Fish... .
The Lesions . .
The Cause ...
The Significance
Acknowledgments

References Cited

CONTENTS

-/f-

11

13

14


12. Meyers, T.R., and J.D. Hendricks. 1985. Histopathology,
pp. 283-331. In G.M. Rand and S.R. Petrocelli, eds.,
Fundamentals of aquatic toxicology. Hemisphere Publ. Corp., New
York, N.Y.

13. Murchelano, R.A. 1982. Some pollution-associated diseases
and abnormalities of marine fishes and shellfishes: a
perspective for the New York Bight, pp. 327-346. In G.F. Mayer,
ed., Ecological stress and the New York Bight: science and
Management. Estuar. Res. Fed., Columbia, S.C.

14. Murchelano, R.A., and R.E. Wolke. 1985. Epizootic
carcinoma in the winter flounder (Pseudopleuronectes americanus).
Science 228: 587-589.

15. NOAA, National Status and Trends Program for Marine
Environmental Quality, Progress Report, A summary of selected
data on chemical contaminants in tissues collected during 1984,
1985 and 1986. NOAA Technical Memorandum, NOS, OMA 38.

16. Northeast Fisheries Center. 1988. National Status and
Trends Program Benthic Surveillance Project: summary report 1984-
1988. Available from National Marine Fisheries Service, 1335
East-West’ Highway, Silver Springs, MD 20910.

17. Peters, G. 1975. Seasonal fluctuations in the incidence
of epidermal papillomas of the European eel (Anguilla anquilla L.
J. Fish. Biol. 7: 415-422.

18. Sherwood, M.J. 1982. Fin erosion, liver condition, and
trace contaminant exposure in fishes from three coastal regions,
pp. 359-377. In G.F. Mayer, ed., Ecological stress and the New
York Bight: science and management. Estuar. Res. Fed.,
Columbia, S.C.

19. Sindermann, C.J. 1979. Pollution-associated diseases and
abnormalities of fish and shellfish: a review. Fish. Bull.,
U.S. 76: 717-748.

20. Sindermann, C.J., F.E. Bang, N.O. Christensen, V.
Dethlefsen, J.C. Harshbarger, J.R. Mitchell, and M.F. Mulcahy.
1980. The role and value of pathobiology in pollution effects
monitoring programs. Rapp. P. -V Reun. Comm. Int. Explor. Sci.
Mer 179: 135-151.

21. Smith, C.E. 1979. Hepatomas in Atlantic tomcod (Microgadus
tomcod) (Walbaum) collected in the Hudson River estuary in New
York. J. Fish. Dis. 2: 313-319.

22. Stegeman, J.J., T.R. Skopek, and W.G. Thilly. 1982.
Bioactivation of polynuclear aromatic hydrocarbons to cytotoxic
and mutagenic products by marine fish, pp. 201-211. In
Symposium: carcinogenic polynuclear aromatic hydrocarbons in the
marine environment. EPA Environ. Res. Lab., Gulf Breeze, Fla.

-15-


i

NOAA Technical Memorandum NMFS-F/NEC-61

Fish as Sentinels

of Environmental! Health

U.S. DEPARTMENT OF COMMERCE
National Oceanic and Atmospheric Administration
National Marine Fisherles Service
Northeast Fisherles Center
Woods Hole, Massachusetts

September 1988

U.S. Department of Commerce
National Techical information Service

‘Springfield, Virginia 22161


The Environment

Boston Harbor is an estuary whose exit to Massachusetts Bay is
bounded on the northeast by Deer Island and on the southeast by
Hull (Fig. 1). The harbor contains about a dozen islands of
varying size; the larger ones are clustered in the central part
and, together with a seaward extension of the harbor's western
shore, divide the harbor into northern and southern parts. The
northern harbor consists of Dorchester Bay and the inner harbor.
A deep shipping channel, President Roads, traverses the northern
harbor from the inner harbor to Massachusetts Bay. President Roads
is 1.6 km (1 mi) wide and up to 22 m (73 ft) deep. The southern
part of the harbor consists of Hingham and Quincy Bays. A second
deep shipping channel, Nantasket Roads, proceeds from Massachusetts
Bay to Quincy Bay; the channel has several smaller branches
terminating in Hull Bay.

Except for dredged channels, Boston Harbor is relatively shallow
with mean depths (at mean high tide) of 5.4 m (17.7 ft) in
Dorchester Bay, 6.8 m (22.4 ft) in Quincy Bay, and 5.1 m (16.7 ft)
in Hull Bay. Freshwater inputs to the harbor from north to south
include the Mystic, Charles, Neponset, Weymouth Fore, Weymouth
Back, and Weir Rivers. The harbor is a saline estuary (salinity
= 25 0/00) which is well mixed during periods of greatest
freshwater flow (late winter, spring) and stratified in late summer
(August) when freshwater input is minimum. Water temperature and
salinity vary seasonally.

As with most estuaries located adjacent to large population
centers, Boston Harbor is the recipient of a large variety of point
and non-point source pollutants, including substantial quantities
of domestic sewage and industrial wastes. In the northern harbor,
there are numerous storm sewer outlets and one major treatment
plant discharge (Deer Island). There also is a major treatment
plant discharge in the southern part of the harbor (Nut Island).
The Deer Island plant services the northern municipalities and
provides primary treatment for an average daily flow of 343 million
gallons per day (mgd). The plant began operating in 1895 ang
serves a Rppulation of approximately 1,340,000 people in a 273 km
(105.4 mi“) area. The Nut Island plant services the southern
municipalities and provides primary treatment for an average daily
flow of 112 mgd. The plant began operating in 1904 and serves,a
population of approximately 630,000 people in a 258 km* (99.6 mi“)
area. The Deer Island plant discharges into President Roads and
the Nut Island plant into Nantasket Roads.

Because of its shallow bays and numerous creeks and marshes, Boston
Harbor is a habitat for several economically important species of
fish and shellfish. Other than for Atlantic menhaden (Brevoortia
tyrannus), there are no commercial finfisheries in the harbor.
Recreational fisheries for Atlantic cod (Gadus morhua), bluefish
(Pomatomous saltatrix), American eel (Anguilla rostrata), pollock
(Pollachius virens), striped bass (Morone saxatilis), and winter
flounder are seasonal (summer primarily) and vary considerably in

-2-


ABSTRACT

Boston Harbor, Massachusetts, is polluted by storm water runoff,
municipal wastewater, and sewage sludge, as well as riverborne

domestic and industrial pollutants, and introductions
characteristic of and related to the sustained heavy commercial
ship traffic in the port. Shallow areas of the inner harbor

provide suitable spawning and nursery areas for winter flounder
(Pseudopleuronectes americanus). The harbor contains. large numbers
of winter flounder during most of the year and is virtually a
sanctuary for the species since commercial fishing is prohibited.
Recent disease surveys have shown that harbor winter flounder have
a high prevalence of gross and microscopic hepatic lesions,
including carcinomas... Although harbor sediments contain high
concentrations of polycyclic aromatic hydrocarbons (PAH) and
polychlorinated biphenyls (PCB), presently thé evidence ascribing
either one of these organic chemicals as a direct cause of the
neoplastic lesions observed is circumstantial.--As a case study,
however, investigations as to the cause and prevalence of hepatic
carcinoma in Boston Harbor winter flounder will attest to the
utility of fish as sentinels of aquatic environmental health.

INTRODUCTION

It is well known that anthropogenic activity has contributed to
deterioration in marine water quality, especially in coastal areas
adjacent to centers of large populations. A variety of effects,
including diseases, have been studied in marine fishes,
crustaceans, and mollusks from polluted marine environments (12,
13, 19, 20). Neoplastic diseases of the integument (papilloma)
and liver (hepatoma), particularly of bottom-dwelling fishes, are
more prevalent in coastal’ areas than areas which are relatively
pristine (6, 10, 11, 17, 21). Metabolic transformations,
especially those mediated ‘by cytochrome P-450 dependent
mixed-function oxygenases, may predispose certain fish species to
the development of hepatic neoplasms.(22). Boston Harbor winter
flounder (Pseudopleuronectes americanus), which are important
commercial and recreational fish, have a high prevalence of hepatic
carcinoma which may be caused by environmental carcinogens (14).

-1-




two groups (diseased and healthy) being compared are the same since
comparable length does not necessarily signify comparable age. The
survival of individual diseased fish depends on many factors,
including the extent of liver damage, the degree of toxicity
resulting from decreased hepatic function, the impairment of other
essential organs, whether metastasis occurs, and the degree of
behavioral modification (the ability to capture prey and avoid
predators may be compromised). Population effects are possible if
large numbers of fish with hepatic carcinoma die and/or if the
fecundity of individual fish is reduced. If gonadal tissues
contain organic contaminants such as PAH's and PCB's, the viability
of eggs and sperm, and vigor of zygotes may be reduced. Analyses
for these chemicals in sexually mature, prespawning fish are
needed. If elevated levels are found, laboratory experiments with
eggs and sperm from Boston Harbor winter flounder should be
conducted to evaluate the viability and normality of the larvae.
It is possible. that gonadal organic contaminants decrease the
number of live larvae and/or increase the percentage of abnormal
larvae in the progeny. If these phenomena occur, then the
abundance of winter flounder, at least locally, may be affected.

High prevalence of hepatic carcinoma in Boston Harbor winter
flounder may affect the acceptability of the fish as food, although
no evidence presently exists substantiating that edible tissues
(muscle) contain unacceptable levels of either PAH's or PCB's.

The most significant aspect of the high prevalence of hepatic
carcinoma observed in Boston Harbor winter flounder is its
relationship to poor environmental quality. Data on the prevalence
of hepatic lesions, including carcinoma, in winter flounder from
East Coast environments which have not been substantially degraded
by anthropogenic activity (south shore of eastern Long Island, New
York; Georges Bank; western Gulf of Maine) substantiate that the
overall prevalence of microscopically detectable hepatic lesions
is low and that no spontaneous carcinomas are present (Murchelano,
unpubl.). As discussed above, both PAH's and PCB's are chemicals
which are potential carcinogens. Although elevated levels of PCB's
have been found in livers of Boston Harbor winter flounder, no
experimental studies have implicated the specific role of PCB's in
tumor induction in these fish. Planned analyses to evaluate the
content of PAH metabolites in bile of fish with and without
carcinomas should be informative. Although circumstantial evidence
exists linking these (and other) hepatic lesions to environmental
contaminants, determining the specific cause of neoplastic disease
in any animal species is a complex, time-intensive process which
is not likely to be resolved quickly. In spite of the lack of
adequate experimental data implicating a specific environmental
contaminant as the cause of the hepatic carcinomas observed in
Boston Harbor winter flounder, there appears to be a relationship
between environmental quality and fish health which suggests that
fish are good sentinels of poor environmental quality.

--12-




of the Massachusetts catch is made within 3 to 200 miles of the
coastline. The bulk of the U.S. catch, especially in the New
England States, comes from Georges Bank. As in most bottom fish
fisheries, the most trawled areas are those with abundant fish and
favorable bottom characteristics.

Although winter flounder support a substantial otter trawl
commercial fishery, the size and value of the recreational catch
also are very significant. The fish can be caught along the entire
U.S. Middle Atlantic and Northeast coasts by recreational fishermen
using hook and line. In 1982 (the latest year with complete
statistics), the New England recreational catch of winter flounder
was 5,575.9 mt (Thompson; pers. comm.*). The Middle Atlantic
recreational catch was 3,163.9 mt. Together, the 1982 New England
and Middle Atlantic recreational catch of winter flounder totaled
8,739.8 mt; the commercial catch in the same year was 16,163.6 mt.
By percentage, the commercial catch was 63% and the recreational
catch 37% of the total catch. Although economically important to
the Commonwealth of Massachusetts, the dollar value of the Boston
Harbor recreational winter flounder fishery is unknown.

The Lesions

Histology is that discipline of biology which is: concerned with
the normal microscopic structure of tissues. Histopathology,
however, is concerned with ‘the structure of abnormal tissue.
Histopathology, with some exceptions, is not used extensively in

the diagnosis of diseases of warm-blooded animals.- Modern
diagnostic medicine employs biochemical, hematologic, radiographic,
and other innumerable sophisticated technologies. In human

medicine, histopathology is used primarily to identify presumptive
neoplastic lesions and in surgical pathology to substantiate the
need for operative procedures. The use of histopathology to
diagnose diseases of fish has considerably more appeal than it does
with warm-blooded animals, partly because of the limited value of
other procedures and partly because the fish can be sacrificed and
all organs examined for the presence of structural changes.

In recent years, several species of marine fishes have been found
to have high prevalences of hepatic neoplastic lesions, including
Atlantic hagfish (Myxine glutinosa) (7), English sole (Parophrys
vetulus) (11), and Atlantic tomcod (Microgadus tomcod) (21).
Winter flounder from Boston Harbor display a variety of hepatic
lesions. The most numerically prevalent ones are hypertrophy and
hyperplasia of macrophage aggregates and a modified form of
hepatocyte apoptosis. Other significant’ lesions include
pericholangitis and focal parenchymal cell necrosis. Lesions which
are presumed to be preneoplastic include basophilic, eosinophilic,
and vacuolated cell foci. Non-neoplastic, proliferative lesions
include cholangiolar (bile duct) hyperplasia and cholangiofibrosis.

*Thompson, B.G., op. cit., p.4.

-5-


i
'T Reproduced trom

best available copy.

Hepatocellular adenoma in liver of winter flounder
from Boston Harbor. Hepatocytes of adenoma are darker
and less vacuolated than those of adjacent liver

parenchyma.

Arrows define the edge of the lesion.

-7-


GENERAL DISCLAIMER

This document may be affected by one or more of the following statements

This document has been reproduced from the best copy furnished by
the sponsoring agency. It is being released in the interest of making
available as much information as possible.

This document may contain data which exceeds the sheet
parameters. It was furnished in this condition by the sponsoring
agency and is the best copy available.

This document may contain tone-on-tone or color graphs, charts
and/or pictures which have been reproduced in black and white.

This document is paginated as submitted by the original source.
Portions of this document are not fully legible due to the historical

nature of some of the material. However, it is the best reproduction
available from the original submission.


23. Stegeman, J.J., B.R. Woodin, and R.L. Binder. 1984.

Patterns of benzo(a)pyrene metabolism by varied species, organs,
and developmental stages of fish, pp. 371-377. In K.L. Hoover,
ed., Use of small fish species in carcinogenicity testing. Nat.

Cancer Inst. Monogr. 65.

-16-


Recent Issues in this serles

33. MARMAP Surveys of the Continental Shelf from Cape Hatteras, North Carolina, to Cape Sable, Nova Scotia
(1977-1983). Atlas No, 1. Summary of Operations. By John D. Sibunka and Myron J. Silverman. November 1984.
vii + 306 p., 52 figs., 2 tables. NTIS Access. No. PB85-150985/AS.

34. Oceanology: Biology of the Ocean. Volume 2. Blological Productivity of the Ocean. By M. E. Vinogradov,
editor in chief. First printed by Nauka Press, Moscow, 1977. Translated from the Russian by Albert L. Peabody.
January 1985. x + 518 p., 81 figs., 59 tables. NTIS Access. No. PB85-204683/AS.

35. Annual NEMP Report on the Health of the Northeast Coastal Waters, 1982. By John B. Pearce, Car) R.
Berman, and Marlene R. Rosen, eds., and Robert N. Reid (bentbos), Catherine E. Warsh (water quality), and Edith
Gould (biological effects), topic coords. January 1985. xi + 68 p., 29 figs., 5 tables. NTIS Access. No. PB85-219129/
AS..

36. Growth and Survival of Larval Fishes in Relation to the Trophodynamics of Georges Bank Cod and
Haddock. By Geoffrey C. Laurence and R. Gregory Lough. January 1985. xvi + 150 p., 67 figs., 15 tables, 1 app. NTIS
Access. No. PB85-220093/AS.

37. Regional Action Plan. By Bruce E. Higgins, Ruth Rehfus, John B. Pearce, Robert J. Pawlowski, Robert L.
Lippson, Timothy Goodger, Susan Mello Roe, and Douglas W. Beach. April 1985. ix + 84 p., 4 figs., 6 tables, 9 app.
NTIS Access. No. PB85-219962/AS.

38. The Shelf/Slope Front South of Nantucket Shoals and Georges Bank as Delineated by Satellite Infrared
Imagery and Shipboard Hydrographic and Plankton Observations. By J. B. Colton, Jr., J. L. Anderson, J. E.
O'Reilly, C. A. Evans-Zetlin, and H. G. Marshal]. May 1985. vi + 22 p., 14 figs. NTIS Access. No. PB85-221083/AS.

39. USA Hisforical Catch Data, 1904-82, for Major Georges Bank Fisheries. By Anne M. T. Lange and Joan E.
Palmer. May 1985. iii + 21 p., 12 figs., 2 tables. NTIS Access. No. PB85-233948/AS.

40. Indexing the Economic Health of the U.S. Fishing Industry’s Harvesting Sector. By Virgil J. Norton, Morton
M. Miller, and Elizabeth Kenney. May 1985. v + 42:p., 44 figs., 25 tables, 1 app. NTIS Access. No. PB85-217958/
AS.

41. Calculation of Standing Stocks and Energetic Requirements of the Cetaceans of the Northeast United States
Outer Continental Shelf. By Robert D. Kenney, Martin A. M. Hyman, and Howard E. Winn. May 1985. iv + 99 p.,
1 fig., 5 tables, 1 app. NTIS Access. No. PB85-239937/AS.

42, Status of the Fishery Resources Off the Northeastern United States for 1985. By Conservation & Utilization
Division, Northeast Fisheries Center, August 1985. iii + 137 p., 46 figs., 49 tables. NTIS Access. No. PB86-125473/ -
AS. .

43. Status of the Fishery Resources Off the Northeastern United States for 1986. By Conservation & Utilization
ivision, Northeast Fisheries Center, September 1986. iii + 130 p., 45 figs., 48 tables. NTIS Access. No. PBS7-122115/
AS.

44. NOAA's Northeast Monitoring Program (NEMP): A Report on Progress of the First Five Years (1979-84)
and a Plan for the Future. By Robert N. Reid, Merton C. Ingham, and John B. Pearce, eds., and Catherine E. Warsh
(water quality), Robert N. Reid (sediments & bottom organisms), Adriana Y. Cantillo (trace contaminants in tissues),
and Edith Gould (biological effects), topic coords. May 1987. xi + 138 p., 13 figs., 1 table, 9 app. NTIS Access. No.
PB87-210100.

45. Food and Distribution of Juveniles of Seventeen Northwest Atlantic Fish Species, 1973-1976. By Ray E.
Bowman, Thomas R. Azarovitz, Esther S. Howard, and Brian P. Hayden. May 1987. xi + 57 p., 10 figs., 19 tables. NTIS
Access. No. PB87-215851/AS.

(continued on inside back cover)


T
42°20'

MASSACHUSETTS -
BAY

Deer

BOSTON %&,\!sland
HARBOR 3

President . g o eo,
Roads :

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g Long os .
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&

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Figure 1. Chart of Boston Harbor. Major sources of freshwater
are shown. :

-3-


\
Neoplastic lesions include adenoma, cholangiocarcinoma, and
hepatocarcinoma (Figs. 2, 3, 4). The neoplastic lesions observed
resemble those experimentally induced with carcinogens in rodents.
Although the hepatic carcinomas frequently were large and involved
a substantial portion of the liver, no grossly visible metastatic
lesions were observed in gill, heart, intestine, kidney, or spleen.

For the non-specialist, the abnormalities seen in the livers of the
Boston Harbor winter flounder include inflammation, necrosis (cell
death), and tumor formation. The liver tumors (neoplasms) are
comparable microscopically to several types of liver cancers of
warm-blooded animals, including man. Presently, there is no
evidence that the winter flounder liver cancers spread to other
organs. :

The Cause

Discussions of the cause(s) of the hepatic neoplastic lesions
observed in winter flounder from Boston Harbor are necessarily
speculative. For marine fishes, no conclusive evidence (based on
experimentally derived data) presently exists substantiating a
specific chemical agent as the inducer of a particular neoplastic
lesion. Any of innumerable environmental chemical contaminants
could be the cause of the neoplasms. Experimentally induced
tumorigenesis has been studied in few fishes, and with relatively
few chemicals, at least in proportion to the number of chemicals
likely to be present in anthropogenically degraded aquatic
environments (5). All the fish used in studies of experimentally
induced carcinogenicity have been freshwater species and include,
in descending order of use, rainbow trout (Salmo gairdneri), guppy
(Poecilia reticulata), medaka (Oryzias latipes), and zebra danio
(Danio rerio). The chemical agents used in laboratory studies of
tumor induction include primarily aflatoxins and nitrosamines; the
liver was the principal organ affected by neoplastic
transformation.

Relatively few studies have focused on the cause of epizotic
neoplasia in marine fishes. Polychlorinated biphenyls (PCB) have
been implicated as the inducers of hepatic neoplasms in Atlantic
hagfish from Swedish fjords (7) and Atlantic tomcod from the Hudson
River (21). Although PCB's initially were, implicated as possible
causes of hepatic neoplasms in English sole from Puget Sound (11),
more recent studies suggest that polycyclic aromatic hydrocarbons
(PAH) may be responsible (10). PCB concentrations (wet weight)
were approximately 5 ppm in livers of Atlantic hagfish with
hepatomas, and were 10.9-98.2 ppm (mean 37.5 ppm) in livers of
Atlantic tomcod with hepatomas. Concentrations (dry weight) of
PcB's in livers of English sole from two urban areas in Puget
Sound, Commencement and Elliot Bays, were 39 ppm and 47 ppm,
respectively (for liver, dry weight/2 approximates wet weight).
PCB concentrations in livers of English sole from two non-urban
areas, Case Inlet and Port Madison, averaged 2.3 ppm.