Polycyclic musk compounds in higher trophic level aquatic organisms and humans from the United States

Chemosphere 61 (2005) 693–700 www.elsevier.com/locate/chemosphere

Polycyclic musk compounds in higher trophic level aquatic organisms and humans from the United States Kurunthachalam Kannan a,*, Jessica L. Reiner a, Se Hun Yun a, Emily E. Perrotta a, Lin Tao a, Boris Johnson-Restrepo a, Bruce D. Rodan a

b

Wadsworth Center, New York State Department of Health, and Department of Environmental Health Sciences, State University of New York at Albany, Empire State Plaza, P.O. Box 509, Albany, NY 12201-0509, USA b U.S. Environmental Protection Agency, Office of Research and Development, Washington, DC 20460, USA Received 2 December 2004; received in revised form 14 March 2005; accepted 15 March 2005 Available online 26 April 2005

Abstract Polycyclic musks, 1,3,4,6,7,8-hexahydro-4,6,6,7,8,8-hexamethylcyclopenta[g]-2-benzopyran (HHCB) and 7-acetyl1,1,3,4,4,6-hexamethyl-1,2,3,4-tetrahydronaphthalene (AHTN), are used as fragrance ingredients in numerous consumer products such as cleaning agents and personal care products. Studies have reported the widespread occurrence of these musks in surface waters and fish from western European countries. Nevertheless, little is known about their accumulation in humans and wildlife in the United States. In this study, we measured concentrations of HHCB and AHTN in human adipose fat collected from New York City. Furthermore, tissues from marine mammals, water birds, and fish collected from US waters were analyzed to determine the concentrations of HHCB and AHTN. Concentrations of HHCB and AHTN in human adipose fat samples ranged from 12 to 798 and from <5 to 134 ng/g, on a lipid weight basis, respectively. A significant correlation existed between the concentrations of HHCB and AHTN in human adipose fat. Concentrations of HHCB and AHTN were not positively correlated with age or gender of the donors. HHCB was found in tissues of several wildlife species, but not in the livers of polar bear from the Alaskan Arctic. Among wildlife species analyzed, spinner and bottlenose dolphins collected from Florida coastal waters contained measurable concentrations of HHCB.
2005 Elsevier Ltd. All rights reserved. Keywords: Polycyclic musk; Human exposure; HHCB; AHTN; Marine mammals

1. Introduction Polycyclic musk compounds such as, HHCB (1,3,4,6,7,8-hexahydro-4,6,6,7,8,8-hexamethylcyclopenta [g]-2-benzopyran; trade names include Galaxolide) and

* Corresponding author. Tel.: +1 518 474 0015; fax: +1 518 473 2895. E-mail address: [email protected] (K. Kannan).

AHTN (7-acetyl-1,1,3,4,4,6-hexamethyl-1,2,3,4-tetrahydronaphthalene; trade names include Tonalide) (Fig. 1) are used as fragrances in a variety of consumer products, including washing and cleaning agents and personal-care products (e.g., perfumes, aftershave lotions, body lotions, shampoos). The production of these two polycyclic musks was approximately 1800 tons/year in Europe in the late 1990s (Rimkus, 1999). Among several polycyclic musks, HHCB and AHTN are the most commonly detected compounds in water and biota. In

0045-6535/$ - see front matter
2005 Elsevier Ltd. All rights reserved. doi:10.1016/j.chemosphere.2005.03.041

694

K. Kannan et al. / Chemosphere 61 (2005) 693–700 HHCB H3 C

measured concentrations of HHCB and AHTN in a variety of higher trophic level aquatic organisms and human tissues collected from the United States. To our knowledge, this is the first study to document the occurrence of these compounds in biological matrices from the United States.

CH3

CH3

H3 C

O

H3C

CH3

2. Materials and methods AHTN

CH3

CH3

2.1. Samples

CH3

O CH3

CH3 CH3

CH3

Fig. 1. Chemical structures of HHCB and AHTN.

the United States, HHCB is listed by the US Environmental Protection Agency (EPA), as a high production-volume chemical, which suggests that the production is more than 4500 tons/year, for uses that are reportable under the Toxic Substances Control Act (USEPA, 2003). Due to their property of lipophilicity (log Kow values of 5.4–6.3) (Heberer, 2002), HHCB and AHTN have been shown to accumulate in several aquatic organisms, such as fish and mussels (Bester et al., 1998; Fromme et al., 2001; Gatermann et al., 2002) and river otters (Lutra lutra) (Leonard and de Boer, 2004). Similarly, occurrence of HHCB and AHTN in human adipose tissues from Germany and Switzerland has been reported (Mu¨ller et al., 1996; Rimkus and Wolf, 1996). Recently, HHCB and AHTN have been shown to accumulate in the tissues of finless porpoise and shark collected from Japanese coastal waters (Nakata, 2005). Several studies have reported the widespread occurrence of HHCB and AHTN in municipal wastewater, surface water, sediment, and biota collected from western European countries (Draisci et al., 1998; Fromme et al., 1999; Gatermann et al., 1999; Dsikowitzky et al., 2002; Bester, 2004). Nevertheless, only a few studies have been conducted on the environmental distribution of synthetic musks in the United States. Recently, Peck and Hornbuckle (2004) reported the occurrence of several polycyclic musks in air and water from Lake Michigan. Simonich et al. (2002) reported the occurrence of polycyclic musks in wastewater treatment plant discharges in the United States. In addition to their persistence and lipophilicity, polycyclic musk compounds have been shown to elicit antiestrogenic effects in various bioassays (Schreurs et al., 2004). Because of their volume of use and bioaccumulation potential, these polycyclic musks raise concern regarding environmental exposure and potential for toxic effects (Balk and Ford, 1999; Salvito et al., 2004). In this study, we have

Human adipose fat samples were obtained from a hospital in New York City during 2003–2004 (Table 1). Fat samples were obtained from individuals undergoing liposuction. A typical liposuction involved removal of one to several liters of body fat. An aliquot of the homogenized fat tissue was taken in a clean I-chem jar for analysis. The samples were void of personal identifiers. The only known demographic factors were age, gender, ethnicity, and occupation. Institutional approval for the analysis of human tissues was obtained from the New York State Department of Health Institutional Review Board (IRB). Tissues of marine mammals were acquired from federal and state agencies and all samples were collected under permission of appropriate agencies. Details regarding wildlife samples analyzed in this study are given in Table 2. Livers from polar bears (Ursus maritimus), originating from coastal waters of Alaska, were collected from native subsistence hunters. Livers from sea otters (Enhydra lutris nereis), harbor seals (Phoca vitulina), and California sea lions (Zalophus californianus) were acquired from the Marine Mammal Center, Sausalito, California; these animals had been found stranded along the central California coast. Blubber from bottlenose dolphins (Tursiops truncatus), spinner dolphins (Stenella clymene), and pygmy sperm whales (Kogia breviceps) were collected from animals stranded in Florida coastal waters. Livers from Atlantic sharpnose sharks (Rhizoprionodon terraenovae) were collected from Florida coastal waters. Livers from river otters (Lutra canadensis) and mink (Mustela vison) were from Michigan and Illinois, respectively. Livers of common merganser (Mergus merganser), lesser scaup (Aythya affinis), greater scaup (Aythya marila) and mallard (Anas platyrhynchos) were collected from Buffalo, New York. Atlantic salmon (Salmo salar) were collected between August 2003 and March 2004 from retail markets in New York. Smallmouth bass (Micropterus dolomieu) were collected from Rock Pond and Effley water reservoir in New York in 2003. All of the samples were collected originally for the analysis of trace organic pollutants, including pesticides and polychlorinated biphenyls (PCBs). The samples were collected in solvent-cleaned jars and were stored at 20 C until analysis.

K. Kannan et al. / Chemosphere 61 (2005) 693–700

695

Table 1 Concentrations of HHCB and AHTN (ng/g) in human adipose fat from New York City, USA Fat (%)

Wet weight

Lipid weight

HHCB

AHTN

HHCB

AHTN

34 ± 9 33 21–51

72.2 ± 75 49.3 6.1–251 100

20.5 ± 14 17.0 <5–54 83

136 ± 143 90.5 12–509 100

39 ± 29 31.5 <8–110 83

Female (n = 37) Mean ± SD Median Range % Positive

31 ± 7.3 31 18–51

105 ± 90 84.6 10.6–435 100

23.5 ± 11 21.3 <5–64 87

192 ± 170 180 18–798 100

43 ± 22 38.7 <8–134 87

Overall (n = 49) Mean ± SD Median Range % Positive

32 ± 7.8 32 18–51

96.9 ± 88 73.7 6.1–435 100

22.8 ± 12 19.8 <5–64 86

178 ± 166 149 12–798 100

42 ± 24 37.4 <8–134 86

Male (n = 12) Mean ± SD Median Range % Positive

Values below the quantitation limit were not included in the calculation of mean.

2.2. Chemicals HHCB and AHTN standards were obtained from Dr. Ehrenstorfer GmbH (Augsburg, Germany); their purities were 51% and 98%, respectively. Reported concentrations were not corrected for the purities of standards. Deuterated (d10) phenanthrene (Accustandard Inc., New Haven, CT) was used as a surrogate standard. 2.3. Chemical analysis The method used in this study was similar to those reported earlier (Mu¨ller et al., 1996; Gatermann et al., 2002), with some modifications. Sample tissues (1–5 g) were ground with anhydrous sodium sulfate and extracted with mixed solvents of dichloromethane and hexane (3:1) for 12 h using a Soxhlet apparatus. The extract was concentrated to 11 ml, and a portion of the extract was used for the measurement of lipid content by gravimetry. Seventy-five nanograms of d10-phenanthrene was spiked into an aliquot of the extract, as a surrogate standard. Lipid in the sample extract was removed by gel permeation chromatography (GPC) using a Bio-beads S-X3 (Bio-Rad Laboratories, Hercules, CA, USA) packed glass column (380 mm · 22 mm i.d.). A mixture of 50% hexane in dichloromethane was used as the mobile phase at a flow rate of 5 ml/ min. The first 100 ml of the eluate was discarded, and the following 100 ml fraction, which contained HHCB, AHTN, and d10-phenanthrene, was collected. The extract was then passed through a cartridge packed with 0.5 g of silica gel (100–200 mesh; Aldrich, Milwaukee, WI, USA) for cleanup. The solvent was concentrated to 200 ll or 1 ml, depending on the sample, and was then

injected into a gas chromatograph interfaced with a mass spectrometer (GC–MS, Agilent Technologies 6890 GC and 5973 Series MS). The ions were monitored at m/z 243, 258, 213 for HHCB; 243, 258 and 159 for AHTN; and 188 for d10-phenanthrene. The GC column used was a DB-5 (5%-phenyl-methylpolysiloxane, Agilent Technologies, Foster City, CA, USA) fused silica capillary column (30 m · 0.25 mm i.d.). The oven temperature was programmed from 120 C to 160 C at a rate of 10 C/min, and was held for 10 min. The temperature was then increased to 300 C at a rate of 3 C/min, with a final hold time of 20 min. The temperatures of injector and detector were set at 250 C and 300 C, respectively. Helium was used as a carrier gas. 2.4. Quality control A standard mixture containing HHCB, AHTN, and d10-phenanthrene was spiked into salad oil (0.5 g) at 20, 50, and 100 ng, and was then passed through the analytical procedure for determination of recovery rates of the compounds. Three replicate analyses were performed for each concentration. Average recoveries of HHCB and AHTN ranged from 85% to 98%. The coefficient of variation of replicate analysis was <10%. Care was taken by analysts not to wear lotion or musk in the laboratory. Procedural blanks were analyzed with every set of six samples to check for laboratory contamination and to correct sample values, if necessary. Procedural blanks contained trace levels of HHCB and AHTN. The limit of quantitation (LOQ) was set to be twice the concentration that was found in blanks. Concentration factors, and a nominal sample weight of 5 g, were used in the determination of LOQ. The LOQ for HHCB

696

Table 2 Concentrations of HHCB and AHTN (ng/g, wet weight) in tissues of wildlife samples collected from US waters n

Tissue

Location

Year

Growth stage

Gender

Fat (%)

HHCB

AHTN

Polar bear

5

Liver

1997–2000

4 adults, 1 cub

1F, 3M, 1UK

7–10.3 [8.9]

<1 (0)

<1 (0)

Sea otter

8

Liver

1993–1999

Adults

F

1.1–3.8 [2.4]

<1–3.2 (38)

<1 (0)

Harbor seal California sea lion River otter Bottlenose dolphin Striped dolphin Pygmy sperm whale Atlantic sharpnose shark

3 3 3 4 3 1 3

Liver Liver Liver Blubber Blubber Blubber Liver

1996–1997 1993–1996 1997 1994–2000 1995–1997 2000 2004

2 adults, 1 juv Adults Adults Adult 3–16 years length: 283 cm NA

F 2F, 1M 3M 3F, 1M 2F, 1 M M NA

4.4–5.5 [4.8] 1.5–4.4 [2.8] 2.4–3 [2.8] 4.2–20.5 [12] 8.1–25 [14] 6.6 4.6–5.2 [4.8]

1.9–2.3 [2.1] <1–2 [1.5] <1–1.2 [1.1] NA NA <1 1.4–1.7 [1.6]

Mink Common merganser Greater and lesser scaup Mallard Atlantic salmon

4 2 2 1 6

Liver Liver Liver Liver Skin-on fillet

1997 1999 1995–1999 1995 2003

2 adult, 2 juv 2 adult 1 adult, 1 juv adult NA

2F, 2M M 1F, 1M M NA

2.2–5.3 [3.7] 3.7–4.2 [4] 1.9–2.7 [2.3] 2.7 <1–3.2 (83)

1.1–2.7 [1.9] 1.6–1.7 [1.7] 1–1.1 [1] 1.1 <1–1.6 (17)

Smallmouth bass

3

Liver

Alaska (Gambell, Barrow, Diomede) Monterey Bay, Moss Landing, California Central California coast Central California coast Grand River, Michigan Florida coast Florida coast Florida coast Indian River Lagoon, Florida coast Aurora/Plainfield, IL Buffalo harbor, NY Niagara River, NY North Tonawanda Creek, NY Farmed and wild, local market, NY Effley Falls Reservoir and Rock Pond, NY

2003

NA

F

4.3–5.4 [4.8]

1.6–1.9 [1.8]

Values in parentheses ( ) indicate % of samples containing detectable concentrations. Values in brackets [ ] indicate mean. NA = Not analyzed; UK = unknown; juv = juvenile.

10–78 [44] 5–62 [36] 89

2.4–14 [5.4] 2.2–3.8 [3] 1.5–2.5 [2] 2.9 4.2–19.8 [11]

K. Kannan et al. / Chemosphere 61 (2005) 693–700

Species

K. Kannan et al. / Chemosphere 61 (2005) 693–700

3. Results and discussion 3.1. Accumulation in humans HHCB was found in all of the human fat samples analyzed, at concentrations ranging from 6.1 to 435 (mean: 97) ng/g, on a wet weight basis. AHTN was found in 86% of the samples analyzed, at concentrations ranging from <5 to 64 (mean: 23) ng/g, wet weight (Table 1). The overall mean concentration of AHTN in human fat was fourfold lower than the mean HHCB concentration. The higher concentrations of HHCB than AHTN can be explained by greater production and usage rates of the former, relative to the latter. It has been reported that in Western Europe the usage rate of HHCB (1427 tons) was fourfold higher than that of AHTN (343 tons) in 2000 (Heberer, 2002). A similar ratio is expected for the production of HHCB and AHTN in the United States, although production statistics for HHCB and AHTN in the United States are not available. As has been found in human fat samples, the concentration ratio of HHCB to AHTN in Lake Michigan waters was 4.7 (Peck and Hornbuckle, 2004), further suggesting greater usage rates of HHCB than AHTN. On a lipid weight basis, concentrations of HHCB and AHTN measured in our study were in the ranges of 12– 798 (mean: 178) and <8 to 134 (mean: 42) ng/g, lipid weight, respectively; these values are two- to threefold higher than those measured in German and Swiss adipose fat samples collected 10 years ago. HHCB and AHTN have been reported in human fat samples collected from Germany during 1993–1995 at concentrations ranging from 28 to 189 (mean: 82) ng/g lipid weight for HHCB, and from 8 to 33 (mean: 19) ng/g lipid weight for AHTN (Rimkus and Wolf, 1996). HHCB and AHTN have also been reported to occur in human milk samples from Germany (Rimkus and Wolf, 1996). Similarly, concentrations of HHCB and AHTN in human adipose fat collected from Switzerland during 1983–1994 were in the ranges of 12–135 (mean: 67) and 1–23 (mean: 9) ng/g, lipid weight, respectively (Mu¨ller et al., 1996). The adipose fat samples collected in our study originated from the individuals who under-

12 10

HHCB

8

Frequency (no. of samples)

and for AHTN was 1 ng/g, wet weight, in wildlife samples, and 5 ng/g, wet weight, in human fat samples. Concentrations of HHCB and AHTN were determined through comparison of peak areas of samples with those in external calibration standards prepared at concentrations ranging from 5 to 200 ng/ml. Sample peak areas were subtracted from blank peak areas for determining concentrations. Recoveries of surrogate standards ranged from 65% to 90%, and the concentrations in samples were corrected for the recoveries of surrogate standard.

697

6 4 2 0 0

100 200 300 400 500 600 700 800 900

10

AHTN

8 6 4 2 0 0

20

40

60

80

100 120 140

Concentration (ng/g, lipid weight) Fig. 2. Frequency distributions of concentrations of HHCB and AHTN in human fat samples from New York City, USA.

went liposuction. These individuals may be concerned with appearance, and therefore, there exists a possibility that they may be prone to frequent usage and high exposure to musk compounds. Concentrations of HHCB and AHTN in human fat were log-normally distributed (Fig. 2). The highest concentration of 798 ng/g, lipid weight, was found in a sample from 35-year old female. However, no gender-related difference was observed in the concentrations of HHCB and AHTN in human fat (p > 0.05) (Fig. 3). Although high concentrations of HHCB were found in individuals aged between 25 and 35 years, no trend of age-related increase in the concentrations of HHCB and AHTN could be discerned (Fig. 4). Concentrations of HHCB and AHTN were not positively correlated with lipid content in human fat. These features are similar to those reported in earlier studies, which showed no apparent trends in the concentrations of HHCB and AHTN with age, gender, or time of obtaining human fat samples (Mu¨ller et al., 1996; Rimkus and Wolf, 1996). However, the number of samples analyzed in earlier studies was less. These accumulation characteristics are different from those observed for persistent organic pollutants such as PCBs. The differences in accumulation features of HHCB and AHTN, compared with those of PCBs, could result from differences in the sources of human exposures. While contaminated diet is the major source of human exposure to PCBs (Kannan et al., 1997), percutaneous absorption of musk-containing perfumes

698

K. Kannan et al. / Chemosphere 61 (2005) 693–700

Concentration (ng/g, lipid wt)

HHCB

AHTN 150

800 700

120

600 500

90

400 300

60

200

30

100 0

0

Male

Female

Male

Female

Fig. 3. Box and whisker plots of adipose fat concentrations of HHCB and AHTN in humans, stratified by gender. The boxes indicate the interquartile ranges of the concentrations; the crosses within each box represent the mean; the whiskers extend to the last observation within 1.5 times the interquartile range; and the circles outside the whiskers represent observations outside the 1.5· interquartile range.

900

HHCB

750

y = -2.46x + 257 R2 = 0.01

Concentration (ng/g, lipid wt)

600 450 300 150 0

0

150

10

20

30

40

50

60

y = -0.92x + 66 R2 = 0.08

AHTN

120

3.2. Accumulation in wildlife

90 60 30 0

AHTN suggests metabolism and excretion of these compounds. If metabolism were slow in humans, then there would be an age dependency, as continued use of musk products would lead to buildup in the body. Because there is no age dependency, the data does suggest metabolism. HHCB has been shown to be transformed to HHCB lactone in fish (Biselli et al., 2004). Concentrations of HHCB in human fat were significantly correlated with AHTN concentrations (p < 0.01) (Fig. 5), which suggests co-exposure of humans to the two musks.

0

10

20

30

40

50

60

Age (years) Fig. 4. Relationship between age and concentrations of HHCB and AHTN in human fat samples from New York, USA.

and cosmetics to the skin, or absorption from textiles, is thought to be a major source of HHCB and AHTN exposure in humans (Cadby et al., 2002). The lack of age- or gender-dependent increase in the concentrations, coupled with elevated concentrations in individuals aged 25–35 years, supports the hypothesis that dermal application is a source of exposure to humans. Nevertheless, inhalation related exposure cannot be ruled out. Specifically, individuals in this age range (25–35 years) are expected to apply more musk products. Further studies are needed to examine the sources of exposure. Lack of age-dependent increase in concentrations of HHCB and

HHCB and AHTN were found in tissue samples from marine mammals, birds, and fish (Table 2). Among the wildlife species analyzed, the highest concentration (on a wet weight basis) was found in the blubber of dolphins collected in coastal Florida. The measured concentrations of HHCB in dolphins were within the range of concentrations reported for finless porpoises (Neophocaena phocaenoides) from Japanese coastal waters (Nakata, 2005). When the concentrations in our study were normalized on a lipid basis, the highest HHCB concentration, 183 ng/g, was found in the blubber of an adult male spinner dolphin. Concentrations of HHCB in bottlenose dolphin were in the range of 12–76 ng/g, lipid weight, whereas the lowest concentration was found in pygmy sperm whale (7.4 ng/g, lipid weight). AHTN could not be analyzed in the blubber of bottlenose dolphin and spinner dolphin, due to an interference. The concentration of AHTN was below the limit of quantitation in the blubber of a pygmy sperm whale. An earlier study reported less-frequent detection of AHTN in finless porpoise from Japanese coast, although HHCB was invariably present in the samples (Nakata, 2005).

K. Kannan et al. / Chemosphere 61 (2005) 693–700

699

AHTN concentration (ng/g, lipid weight)

140 y = 0.06x + 25.8 R2 = 0.17

120 100 80 60 40 20 0 0

150

300

450

600

750

900

HHCB concentration (ng/g, lipid weight) Fig. 5. Relationship between HHCB and AHTN concentrations in human fat samples from New York, USA.

A comparison of concentrations of HHCB in the blubber of dolphins from Florida with that of PCBs suggested that HHCB concentrations were 2–3 orders of magnitude lower than PCB concentrations (Watanabe et al., 2000). HHCB was detected in liver tissues of seals, sea lions, Atlantic sharpnose shark, river otter, mink, common merganser, lesser scaup, greater scaup, and mallard. Concentrations of HHCB in the livers of these wildlife species were between 1.5 and 5.3 ng/g, wet weight. Fish species such as Atlantic salmon and smallmouth bass also contained detectable concentrations of HHCB. Concentrations of HHCB in fish samples were lower than those reported for fish from European waters (Fromme et al., 1999; Rimkus, 1999; Gatermann et al., 2002; Heberer, 2002). Concentrations of AHTN in wildlife samples were, in general, two- to threefold lower than HHCB concentrations. Neither HHCB nor AHTN was detected in the livers of polar bear from the Alaskan Arctic. Discharges from wastewater treatment plants have been suggested as an important source of HHCB and AHTN for surface waters, and thereby for aquatic organisms (Rimkus, 1999; Bester, 2004). Several studies have reported the occurrence of HHCB and AHTN in sewage treatment plant influent and effluent samples (Rimkus, 1999; Ricking et al., 2003). Similarly, HHCB and AHTN have also been detected in fresh water and sea water collected from several European countries (Bester et al., 1998; Rimkus, 1999) and the United States (Peck and Hornbuckle, 2004). Relatively low concentrations of HHCB and AHTN in aquatic organisms from US waters could be due to efficient removal of these compounds in wastewater treatment processes. In a study of 10 typical wastewater treatment plants in the United States, significant removal of HHCB and AHTN during the treatment processes has been shown (Simonich et al., 2002). In summary, the results of this study suggest widespread occurrence of HHCB and AHTN in human tissues. Dermal absorption arising from the use of

personal-care products is thought to be a major source of human exposure to these compounds. HHCB and AHTN are also found in marine mammals, birds, and fish, but at relatively low concentrations. This is the first study to report the occurrence of HHCB and AHTN in wildlife and humans from the United States. The present study has not addressed the issue of risks from polycyclic musks to humans or wildlife. Risk is a factor of both exposure and hazard (toxicity). Further studies are needed to evaluate and characterize exposures and toxicity of these compounds on humans and wildlife.

Acknowledgments We thank Thomas Evans (U.S. Fish and Wildlife Service, Anchorage, AK) for polar bear samples; Dr. Nancy Thomas (National Wildlife Health Center, Madison, WI) for sea otter samples; Dr. Frances Gulland (The Marine Mammal Center, Sausalito, CA) for pinniped samples from California; Doug Adams (Florida Fish and Wildlife Conservation Commission, Melbourne, FL) for shark from Florida; Dr. Richard Halbrook (Southern Illinois University, Carbondale, IL) for mink from Illinois; Dr. David Mayack (New York State Department of Environment Conservation, Gloversville, NY) for waterfowl samples from New York. This study was funded in part by a grant from the US Environmental Protection Agency (EPA). The contents of this publication do not necessarily reflect the views or policies of the US EPA. Mention of trade names or commercial products does not constitute endorsement or recommendation for use.

References Balk, F., Ford, R.A., 1999. Environmental risk assessment for the polycyclic musks, AHTN and HHCB. Toxicol. Lett. 111, 81–94.

700

K. Kannan et al. / Chemosphere 61 (2005) 693–700

Bester, K., 2004. Retention characteristics and balance assessment for two polycyclic musk fragrances (HHCB and AHTN) in a typical German sewage treatment plant. Chemosphere 57, 863–870. Bester, K., Hu¨hnerfuss, H., Lange, W., Rimkus, G.G., Theobald, N., 1998. Results of non-target screening of lipophilic organic pollutants in the German Bight II: Polycyclic musk fragrances. Water Res. 32, 1857–1863. Biselli, S., Gatermann, R., Kallenborn, R., Sydnes, L.K., Hu¨hnerfuss, H., 2004. Synthetic musk fragrances in the environment. In: The Handbook of Environmental Chemistry. Springer-Verlag, Berlin, pp. 189–212. Cadby, P.A., Troy, W.R., Vey, M.G.H., 2002. Consumer exposure to fragrance ingredients: Providing estimates for safety evaluation. Reg. Toxicol. Pharmacol. 36, 246–252. Draisci, R., Marchiafava, C., Ferretti, E., Palleschi, L., Catellani, G., Anastasio, A., 1998. Evaluation of musk contamination of freshwater fish in Italy by accelerated solvent extraction and gas chromatography with mass spectrometric detection. J. Chromatogr. 814, 187–197. Dsikowitzky, L., Schwarzbauer, J., Littke, R., 2002. Distribution of polycyclic musks in water and particulate matter of the Lippe River (Germany). Org. Geochem. 33, 1747–1758. Fromme, H., Otto, T., Pilz, K., 2001. Polycyclic musk fragrances in different environmental compartments in Berlin (Germany). Water Res. 35, 121–128. Fromme, H., Otto, T., Pilz, K., Neugebauer, F., 1999. Levels of synthetic musks; bromocyclene and PCBs in eel (Anguilla anguilla) and PCBs in sediment samples from some waters of Berlin/Germany. Chemosphere 39, 1723–1735. Gatermann, R., Hellou, J., Hu¨hnerfuss, H., Rimkus, G., Zitko, V., 1999. Polycyclic and nitro musks in the environment: A comparison between Canadian and European aquatic biota. Chemosphere 38, 3431–3441. Gatermann, R., Biselli, S., Hu¨hnerfuss, H., Rimkus, G., Hecker, M., Karbe, L., 2002. Synthetic musks in the environment. Part 1: Species-dependent bioaccumulation of polycyclic and nitro musk fragrances in freshwater fish and mussels. Arch. Environ. Contam. Toxicol. 42, 437–446. Heberer, T., 2002. Occurrence, fate and assessment of polycyclic musk residues in the aquatic environment of urban areas––a review. Acta Hydrochim. Hydrobiol. 30, 227–243. Kannan, K., Tanabe, S., Giesy, J.P., Tasukawa, R., 1997. Organochlorine pesticides and polychlorinated biphenyls in

foodstuffs from Asian and Oceanic countries. Rev. Environ. Contam. Toxicol. 152, 1–55. Leonard, P.E.G., de Boer, J., 2004. Synthetic musk fragrances in the environment. In: The Handbook of Environmental Chemistry 3X. Springer-Verlag, Berlin, Heidelberg, pp. 49– 84. Mu¨ller, S., Schmid, P., Schlatter, C., 1996. Occurrence of nitro and non-nitro benzenoid musk compounds in human adipose tissue. Chemosphere 33, 17–28. Nakata, H., 2005. Occurrence of synthetic musk fragrances in marine mammals and sharks from Japanese coastal waters. Environ. Sci. Technol. 39, in press. Peck, A.M., Hornbuckle, K.C., 2004. Synthetic musk fragrances in Lake Michigan. Environ. Sci. Technol. 38, 367– 372. Ricking, M., Schwarzbauer, J., Hellou, J., Svenson, A., Zitko, V., 2003. Polycyclic aromatic musk compounds in sewage treatment plant effluents of Canada and Sweden-first results. Mar. Pollut. Bull. 46, 410–417. Rimkus, G.G., 1999. Polycyclic musk fragrances in the aquatic environment. Toxicol. Lett. 111, 37–56. Rimkus, G.G., Wolf, M., 1996. Polycyclic musk fragrances in human adipose tissue and human milk. Chemosphere 33, 2033–2043. Salvito, D.T., Vey, M.G.H., Senna, R.J., 2004. Fragrance materials and their environmental impact. Flavour Fragr. J. 19, 105–108. Schreurs, R.H.M.M., Legler, J., Artola-Garicano, E., Sinnige, T.L., Lanser, P.H., Seinen, W., van den Burg, B., 2004. In vitro and in vivo antiestrogenic effects of polycyclic musks in zebrafish. Environ. Sci. Technol. 38, 997–1002. Simonich, S.L., Federle, T.W., Eckhoff, W.S., Rottiers, A., Webb, S., Sabaliunas, D., de Wolf, W., 2002. Removal of fragrance materials during U.S. and European wastewater treatment. Environ. Sci. Technol. 36, 2839–2847. USEPA, 2003. Toxic substances control act inventory, High Production Volume (HPV) Chemical List Database. Available from: . Watanabe, M., Kannan, K., Takahashi, A., Loganathan, B.G., Odell, D.K., Tanabe, S., Giesy, J.P., 2000. Polychlorinated biphenyls, organochlorine pesticides, tris(4-chlorophenyl)methane, and tris(4-chlorophenyl)methanol in livers of small cetaceans stranded along Florida coastal waters, USA. Environ. Toxicol. Chem. 19, 1566–1574.