The growth of the modern sewage treatment system has enabled human populations to exist in ever higher numbers and
densities, due primarily to the ability of systems to transport pathogens in excrement away from cities (Rockefeller 8). As
these systems have grown larger in size, logistical problems associated with the sheer quantity of effluent solids have forced
managers to seek alternatives for disposal (Rockefeller 15). With the passage of the Ocean Dumping Ban Act of 1988, pressures
for disposal were exacerbated and both municipalities and regulators increasingly viewed land application of biosolids for
fertilizer use as an attractive solution (U.S. Cong. 210-212).
While the suitability of biosolids for use in agriculture has been controversial due to the presence of pathogens and
heavy metals, recent evidence indicates that a significant number of other contaminants are present in biosolids and that
some of these chemicals may have a significant ecological impact (Renner A667). Because contaminants can migrate via a number
of pathways, they represent a source of contamination to surface and groundwater resources in areas where biosolids are applied
(Drewes and Shore 221). Governments at all levels must re-evaluate legislative mandates for fertilizer applications of biosolids,
incorporating these recent findings into policies. Because multiple systems play a role in the introduction and environmental
fate of these compounds, concurrent changes may need to be introduced into several large systems in order to rationally permit
the use of biosolids for agricultural fertilizer.
Contaminants in Biosolids
Several studies have examined contaminants in biosolids. The U.S. Environmental Protection Agency (EPA) performed the
first National Sewage Sludge Survey (NSSS) in 1988, identifying heavy metals, chlorinated organic pollutants, pesticides,
and plasticizers in a large number of biosolid samples (EPA, NSSS 47229-47231). Despite finding widespread presence of contaminants,
EPA initially decided to regulate only the following elemental pollutants: arsenic, cadmium, chromium, copper, lead, mercury,
molybdenum, nickel, selenium, and zinc (EPA, A Guide to the Biosolids Risk Assessments 99).
Studies since the 1988 NSSS have shown that a number of additional chemicals are present in biosolids. These contaminants
include a wide variety of pharmaceuticals (Daughton and Ternes), surfactants used in many personal care products (La Guardia
et al.; Petrovic and Barceló), a class of flame retardants known as brominated diphenol ethers (BDE’s) (Hale et al.),
synthetic musks from fragrances (Heberer and Grosch), and plasticizers known as phthlates from a variety of sources (de Jonge
et al.). Radioactive materials were detected in sludge and ash in sewage treatment facilities nine times from 1984 to 1994,
yet at the time of their report, the U.S. General Accounting Office found that only 15 of the 2100 facilities receiving nuclear
wastes had been inspected by the Nuclear Regulatory Commission (1-3).
Studies examining contamination of streams are also useful in terms of identifying contaminants and pathways of significance,
since land application of biosolids as fertilizers behaves as a non-point source of pollution. For example, estrogen from
biosolids has been found to migrate to nearby surface water mainly through surface runoff, while testosterone percolates down
to the groundwater (Drewes and Shore 221). A national reconnaissance of pharmaceuticals, hormones, and other organic wastewater
contaminants has been an ongoing program of the United States Geological Survey (USGS) since 1999; data reported in 2002 show
contamination by at least some of these chemicals in 80% of the 139 streams sampled (Kolpin et al. 1202). Chemicals frequently
found included detergent metabolites, hormones, plasticizers, and nonprescription drugs (Kolpin et al. 1209).
Pharmaceuticals and personal care products (PPCPs) are a group of chemicals that include: all pharmaceuticals including
veterinary and illicit drugs, cosmetics ingredients, food supplements and other personal care products such as soaps, shampoos,
hair dyes, and metabolic and transformation products of all these groups (Daughton and Ternes 908). While PPCP use has increased
dramatically since the 1950’s, only recently has attention turned to their ecological impacts and the potential for
difficult-to-detect chronic changes in numerous species (Daughton, 2).
While some PPCP’s are water-soluble and present mainly in the aqueous effluent, hydrophobic PPCPs readily adsorb
onto particulate matter in the sewage treatment plant during processing and may later be released through leaching or surface
water run-off from agricultural fields treated with biosolids (Daughton and Ternes 922). Important classes of drugs that have
been detected in the environment and potentially present in biosolids include: endogenous hormones, synthetic hormonally active
compounds, antibiotics, blood lipid regulators, non-opioid analgesics/non-steroidal anti-inflammatory drugs, beta-blockers,
bronchodilators, antidepressants, obsessive-compulsive regulators, antiepileptics, antineoplastics (cancer drugs), impotence
drugs, tranquilizers, retinoids, diagnostic contrast media, and numerous personal care products, including fragrances (synthetic
musks), preservatives, disinfectants, antiseptics, sunscreen agents, and herbal remedies, also known as nutraceuticals (Daughton
and Ternes 932). Production of personal care products are significant, as the table below demonstrates for the case of Germany
(Daughton and Ternes 930). Data for the U.S. are generally not available.
Table 1: Personal care products produced in Germany (1993)
sprays, setting lotions, hair dyes
Metal Contaminants in Biosolids
Because metals are elements, they do not breakdown in the environment; the only possible change is transformation to
a different form, often resulting in more toxic compounds (Ridley et al. 44). Tin,
arsenic, selenium, tellurium, lead, gold, mercury, titanium, platinum, and palladium have all been reported to undergo conversion
into organic forms by microorganisms in the environment and in organic form are bioaccumulative toxins, particularly to the
central nervous system. (Ridley et al. 44). Metals in soils repeatedly applied with biosolids will necessarily have increased
metal concentrations; any decreases must be due to uptake into plants, diffusion into groundwater, run-off via surface water,
or transformation into another form.
A recent study by the Washington State Department of Agriculture (WSDA) examined cadmium in soil and in crops, finding
that crop uptake of cadmium occurs, but noted that repeated application of fertilizers high in cadmium may increase concentrations
in the soil if not offset by uptake in plants (WSDA 16). Factors that affect the uptake into crops include: the source of
the metal, existing soil metal concentrations, soil pH, soil type, and the amount of plant material tilled back into the soil
after harvest (WSDA 18). The report noted that cadmium was of special concern due to the high concentrations of cadmium present
in many fertilizers, whereas lead and arsenic are present in low amounts (WSDA 5). However, based upon the NSSS, average levels
of lead in biosolids are 5-10 times higher than cadmium, whereas levels of arsenic are significantly smaller (EPA, NSSS 47229).
Mahaffey, et. al. examined total dietary metal levels using a “market
basket” sampling of foods from around the country in 1975, finding that many foods contained significant levels of heavy
metals. The authors noted that the measured levels for lead, cadmium, and mercury were below the World Health Organization
tolerable intake levels, but stated that increased concentrations should be avoided (Mahaffey et al. 67). Recent studies have
shown that cadmium activates the estrogen receptor (Stoica et al. 545), and may play a role in prostate cancer (Martin et
al. 263). Similarly, lead and mercury are well-known neurotoxins, capable of inducing a large number cognitive and behavioral
changes (Schantz and Widholm 1197).
While some metals are regulated by the EPA under the part 503 biosolids rule, concerns over the allowable levels have
been expressed by a number of environmental groups. In one case, when the United States Department of Agriculture (USDA) proposed
the use of biosolids for organic crops in December 1997, the Environmental Working Group published a document highlighting
the fact that the national average of heavy metals in biosolids based on the NSSS was 20 times higher than the average concentration
in soil nationally (Hettenbach et al. 3).
In the last decade, the recognition that a large number of common chemicals behave like hormones or otherwise interfere
with the endocrine system has generated a great deal of concern among scientists, public health officials, and the public
(National Research Council 1). These chemicals have been collectively termed endocrine disrupting chemicals (EDCs), due to
their ability to alter signaling pathways of the endocrine system (Cooper and Kavlock 159). Concern stems from a number of
assumptions commonly applied when setting regulatory levels based on animal toxicology tests, such as an assumption of a linear
dose-response curve (Schettler et al. 31), or that cancer is the most sensitive endpoint of concern (Colborn, vom Saal, and
Soto 383). Both of these assumptions are invalid in the case of endocrine disruption, as the dose-response curve may instead
form the shape of an inverted “U”, invalidating the linear extrapolation assumption fundamental to toxicological
risk assessment (Colborn, Dumanoski, and Myers 169-170). Also, experimental data in various species have shown that endocrine
disruption effects are seen for some chemicals in the parts-per-trillion range, rather than parts-per-million or parts-per-billion
range commonly required for carcinogens to cause an effect (Solomon and Schettler 1474).
Significantly, biosolids often contain high levels of the natural female sex hormones estradiol and estrone (Drewes
and Shore 221), and can contain a number of other synthetic endocrine disruptors present in many pharmaceuticals and personal
care products (Daughton and Ternes 926). These chemicals have been associated with sex changes or complete sex-reversal in
a number of species, including fish (Routledge et al. 1559), amphibians (Mayer, Dyer, and Propper 557), and mammals (Zarn,
Brüschweiler, and Schlatter 255). In the Hanford Reach portion of the Columbia River, researchers found that 84% of the phenotypic
female Chinook salmon carried a genetic marker for the Y chromosome (Nagler et al. 67), indicating they had been sex-reversed,
possibly due to endocrine disruption although more study is needed.
Recent studies in humans have documented a decline in sperm counts since the 1950’s (Schettler et al. 164-165).
Many authors attribute this decrease to an increase in the manufacture and distribution of EDC’s (Telisman, et al. 45;
Sharpe and Skakkebaek 1392). Another study showed that a combination of 11 environmental estrogens, each below their respective
no-observed-effect concentration (NOEC), resulted in a dramatic increase in the estrogenic activity as reported by an estrogenic
yeast screening assay (Rajapakse, Silva, and Kortenkamp 917). This implies that it is not possible to set limits on a chemical-by-chemical
basis because real-life exposures comprise numerous chemicals and various exposure pathways, many of which cannot be controlled.
When the Environmental Protection Agency (EPA) set initial biosolids rules, there were several assumptions that were
applied when the risk analysis was performed. They initially identified 200 potential pollutants of significance, and over
a three year period, four panels of experts reduced the number of chemicals to 50 (EPA, Guide 10). The analysis was modified
several times, but ultimately the EPA identified fourteen pathways whereby humans could be exposed to contaminants present
in biosolids (EPA, Guide 27). Only one pathway considered effects on a child; the pathway was direct ingestion of biosolids,
which assumed that the daily intake would be 0.2 grams (EPA, Guide 69), an unrealistically small amount. Endocrine disruption,
however, is most significant for the developing fetus, as hormones are signals that guide many aspects of differentiation
and growth (Bern 10-11). This is particularly true for sexual development, since reproduction is closely associated with proper
The endpoint used to determine regulatory requirements for chemicals found in sludge was cancer; the EPA chose the
acceptable risk level to be one in ten-thousand, one-hundred times weaker than the commonly chosen value of one in a million
(EPA, Guide 35-36). Given that endocrine disruption is a far more sensitive endpoint, having effects in the parts-per-trillion
range, and that fetuses are at the most sensitive stage of growth, coupled with the observation that multiple chemical exposures
below the NOEC have an effect, it is clear that the regulations are inadequate: metals may not be the only significant contaminants
and cancer is not the most sensitive endpoint. Additionally, the EPA has not yet made a determination for dioxin in biosolids
applied to land, which has been under consideration for some time without any resolution (EPA, Standards 66227). Because dioxin
is a persistent chemical that resists breakdown in the environment and is one of the most potent endocrine disruptors known
(Colborn, Dumanoski, and Myers 116), this omission is significant.
In a recent review article on environmental signaling and endocrine disruptors, it was noted that as early as 1958,
Dr. Roy Hertz aptly described the potential of a “steroid cycle,” whereby hormones are introduced into agriculture
and via uptake into plants are recycled back in the animal and human populations (McLachlan 319). Hertz is quoted saying:
“I think that we are now actually setting up a steroid cycle in our environment, and we have to give very serious consideration
to its implications for our subsequent development and growth and possibly reproductive function (McLachlan 320).” What
was true for hormones used in farm animals is also true for biosolids, since they can contain virtually every element, every
compound made by man, in addition to a very large number of metabolic and transformation products created when added together
in the sewage treatment system. Because many modern city sewage systems recapture storm-water runoff in addition to influent
from industry, hospitals, and humans, the highly toxic dirt of an entire society is captured in biosolids (Rockefeller 10).
The chemical-by-chemical regulatory approach that has been pursued up to this point must be reassessed, particularly given
the fact that small but chronic exposures to multiple chemicals over long periods of time would likely result in precisely
the kind of subtle changes that would be impossible to detect with epidemiological methods (Weiss; Daughton and Ternes 933).
If epidemiological methods are rendered totally ineffective due to this process and human studies are unethical, there is
little chance for arguments based upon science to be useful tools for initiating regulatory action.
While biosolids indisputably provide valuable nutrients to agriculture, advocates of biosolids have not adequately
addressed concerns raised by those opposed to the practice. A severe lack of data exists on the consequences and fate of many
chemicals likely to be present in biosolids, precluding arguments against the practice based on scientific data. Conversely,
advocates cannot claim an absence of evidence is justification for continuation of a practice that fails the logic of common
sense. Because effects of contaminants commonly found in biosolids are believed to be associated with declining sperm counts
and reproductive failure, the stakes could not be higher for the future with respect to the choices we make now. As a start
towards solving this difficult problem, the Washington State Legislature should 1) fully fund the Department of Ecology’s
dioxin and mercury elimination program ($800,000), 2) implement an independent publicly-funded biosolids tracking, surveillance,
and reporting system that provides easy public access to data regarding the quantities, locations applied, and contaminant
content, and 3) eliminate known sources of influent contamination from industry, hospitals, and other identifiable groups
who contribute directly or indirectly to the degradation of biosolids quality.
Bern, Howard A. "The Fragile Fetus." Chemically-Induced Alterations in Sexual
Development: The Wildlife/Human Connection. Eds. Theo Colborn and
Coralie Clement. Princeton: Princeton Scientific Publishing, 1992.
Theo, Frederick S. vom Saal, and Ana M. Soto. "Developmental Effects of Endocrine-Disrupting Chemicals in Wildlife and Humans."
Environmental Health Perspectives 101 (1993): 378-84.
Theo, Dianne Dumanoski, and John Peterson Myers. Our Stolen Future: Are We Threatening Our Fertility, Intelligence, and
Survival? A Scientific Detective Story. New York: Plume, 1997.
R.L., and R.J. Kavlock. "Endocrine Disruptors and Reproductive Development: A Weight-of-Evidence Review." J. Endocrinology
152 (1997): 159-66.
Christian G., and Thomas A. Ternes. "Pharmaceuticals and Personal Care Products in the Environment: Agents of Subtle Change?"
Environmental Health Perspectives 107.Suppl. 6 (1999): 907-38.
Christian G. "Pharmaceuticals and Personal Care Products in the Environment: Overarching Issues and Overview." Pharmaceuticals
and Personal Care Products in the Environment: Scientific and Regulatory Issues. Eds. Christian G. Daughton and Tammy
L. Jones-Lepp. Vol. 791. Washington, D.C.: American Chemical Society, 2001. 2-38.
Jörg E., and Laurence S. Shore. "Concerns About Pharmaceuticals in Water Reuse, Groundwater Recharge, and Animal Waste." Pharmaceuticals
and Personal Care Products in the Environment: Scientific and Regulatory Issues. Eds. Christian G. Daughton and Tammy
L. Jones-Lepp. Vol. 791. Washington, D.C.: American Chemical Society, 2001. 206-28.
Robert C., et al. "Persistent Pollutants in Land-Applied Sludges." Nature 412 (2001): 140-41.
Th., A. These, and U.A. Grosch. "Occurrence and Fate of Synthetic Musks in the Aquatic System of Urban Areas: Polycyclic and
Nitro Musks as Environmental Pollutants in Surface Waters, Sediments, and Aquatic Biota." Pharmaceuticals and Personal
Care Products in the Environment: Scientific and Regulatory Issues. Eds. Christian G. Daughton and Tammy L. Jones-Lepp.
Vol. 791. Washington, D.C.: American Chemical Society, 2001. 142-55.
Todd, et al. Dumping Sewage Sludge on Organic Farms?: Why USDA Should Just Say No. Washington D.C.: Environmental Working
Jonge, H., et al. "Transport of Di(2-Ethylhexyl)Phthlate (DEHP) Applied with Sewage Sludge to Undisturbed and Repacked Soil
Columns." J. Environ. Qual. 31 (2002): 1963-71.
Dana W., et al. "Pharmaceuticals, Hormones, and Other Organic Wastewater Contaminants in U.S. Streams, 1999-2000: A National
Reconnaissance." Environ. Sci. Technol. 36 (2002): 1202-11.
Guardia, Mark J., et al. "Alkylphenol Ethoxylate Degradation Products in Land-Applied Sewage Sludge (Biosolids)." Environ.
Sci. Technol. 35 (2001): 4798-804.
K.R., et al. "Heavy Metal Exposure from Foods." Environmental Health Perspectives 12 (1975): 63-69.
Martin, Mary Beth,
et al. "Role of Cadmium in the Regulation of AR Gene Expression and Activity." Endocrinology 143 (2002): 263-75.
Loretta P., Cheryl A. Dyer, and Catherine R. Propper. "Exposure to 4-Tert-Octylphenol Accelerates Sexual Differentiation and
Disrupts Expression of Steroidogenic Factor 1 in Developing Bullfrogs." Environmental Health Perspectives 111 (2003):
John A. "Environmental Signaling: What Embryos and Evolution Teach Us About Endocrine Disrupting Chemicals." Endocrine
Reviews 22 (2001): 319-41.
James J., et al. "High Incidence of a Male-Specific Genetic Marker in Phenotypic Female Chinook Salmon from the Columbia River."
Environmental Health Perspectives 109 (2001): 67-69.
Research Council. Hormonally Active Agents in the Environment. Washington, D.C.: National Academy Press, 1999.
Mira, and Damià Barceló. "Determination of Anionic and Nonionic Surfactants, Their Degradation Products, and Endocrine-Disrupting
Compounds in Sewage Sludge by Liquid Chromotography/Mass Spectrometry." Anal. Chem. 72 (2000): 4560-67.
Nissanka, Elisabete Silva, and Andreas Kortenkamp. "Combining Xenoestrogens at Levels Below Individual No-Observed-Effect
Concentrations Dramatically Enhances Steroid Hormone Action." Environmental Health Perspectives 110 (2002): 917-21.
Rebecca. "Is Sludge Safe?" Environmental Health Perspectives 110 (2002): A667.
W.P., et al. "Recent Studies on Biomethylation and Demethylation of Toxic Elements." Environmental Health Perspectives
19 (1977): 42-46.
Abby A. "Civilization and Sludge: Notes on the History of the Management of Human Excreta." CNS 9.3 (1998): 3-18.
Routledge, E. J., et
al. "Identification of Estrogenic Chemicals in Stw Effluent. 2. In Vivo Reponses in Trout and Roach." Environ. Sci. Technol.
32 (1998): 1559-65.
Schantz, Susan L.,
and John J. Widholm. "Cognitive Effects of Endocrine Disrupting Chemicals in Animals." Environmental Health Perspectives
109 (2001): 1197-206.
Ted, et al. Generations at Risk: Reproductive Health and the Environment. Cambrige, MA: MIT P, 2000.
Sharpe, Richard M.,
and Niels E. Skakkebaek. "Are Oestrogens Involved in Falling Sperm Counts and Disorders of the Male Reproductive Tract?" Lancet
341 (1993): 1392-95.
Gina M., and Ted Schettler. "Environment and Health: 6. Endocrine Disruption and Potential Human Health Implications." CMAJ
163 (2000): 1471-76.
Stoica, Adriana, Benita
Katzenellenbogen, and Mary Beth Martin. "Activation of Estrogen Receptor-a by the
Heavy Metal Cadmium." Molecular Endocrinology 14 (2000): 545-53.
Spomenka, et al. "Semen Quality and Reproductive Endocrine Function in Relation to Biomarkers of Lead, Cadmium, Zinc, and
Copper in Men." Environmental Health Perspectives 108 (2000): 45-53.
States. Cong. House. Committee on Science. Epa's Sludge Rule: Closed Minds or Open Debate?. Second Session. Hearing,
March 22, 2000. Washington: Government Printing Office, 2001.
Environmental Protection Agency. "National Sewage Sludge Survey; Availability of Information and Data, and Anticipated Impacts
on Proposed Regulations; Proposed Rule." Federal Register 55 (November 9, 1990): 47210-47283.
---. "Standards for the Use or Disposal of Sewage Sludge." Federal Register 66 (December 21, 2001): 66227-66235.
---. ---. A Guide to
the Biosolids Risk Assessments for the Epa Part 503 Rule. Washington, D.C.:
General Accounting Office. “Nuclear Regulation: Action Needed to Control Radioactive
Contamination at Sewage Treatment Plants.” Letter Report, May 18, 1994.
State. Department of Agriculture . A Report on the Plant Uptake of Metals from Fertilizers: Submitted to Washington
State Legislature December 31, 2001.
Bernard. "Sexually Dimorphic Nonreproductive Behaviors as Indicators of Endocrine Disruption." Environmental Health Perspectives
Supplements 110 (2002): 387-91.
Zarn, Jürg A., Beat
J. Brüschweiler, and Josef R. Schlatter. "Azole Fungicides Affect Mammalian Steroidogenesis by Inhibiting Sterol 14a-Demethylase and Aromatase." Environmental Health Perspectives 111 (2003): 255-61.