Most of us have an attitude of “flush it and forget it,” but to scientists like Rolf
Halden, our waste is a bonanza of valuable information on population-level chemical
exposures. Halden is an environmental scientist at Arizona State University’s Biodesign
Institute, where he maintains the National Sewage Sludge Repository—a collection of
hundreds of samples of raw sewage and sludge collected from more than 200 sites around
the United States.
1
The sample bottles are filled with a brownish-black slurry derived from raw sewage,
“so it has everything that is flushed down the toilet,” says Arjunkrishna Venkatesan,
a postdoctoral research associate on Halden’s team. “If you collect samples from sewerage
manholes, sampling equipment is going to get clogged, and you’re going to have hair,
condoms, and all sorts of stuff.” The laboratory staff filter out most of those solids,
then freeze the samples for storage.
The emerging field of sewage chemical-information mining is taking advantage of a
readily available yet underappreciated resource: the untreated waste flowing under
our feet and the biosolids remaining after treatment. It turns out that sewage and
sewage sludge hold a wealth of data on chemical consumption and exposure, and potentially
even the health status of whole communities.
EHP
As disgusting as the samples may be, the repository is helping to open up a field
known broadly as sewage chemical-information mining (SCIM). This field is using the
sewage destined for wastewater treatment plants as a medium for chemical exposures
within a community, exposures that are impractical to measure by other means. Other
studies are looking at sewage sludge (the solids that remain after wastewater treatment)
for information on chemicals that can accumulate in the human body. Still another
approach, known as BioSCIM, measures biomarkers in sewage as a way to assess the overall
health status of communities.
SCIM initially took off in 2001 when scientists hypothesized they could measure the
metabolites of illicit drugs like cocaine, heroin, and methamphetamine in untreated
wastewater collected from city sewers.
2
This particular application of SCIM was originally known as “sewage epidemiology.”
The success of this technique has been tested in Europe
3
,
4
and most recently provided per capita estimates of drug usage in cities including
Antwerp, Stockholm, and London.
5
Now sewage epidemiology is being applied to substances beyond illicit drugs. Since
2010 Halden has published nearly 50 papers on the subject. One study calculated per
capita chemical consumption and, based on levels found in sewage sludge, estimated
exposure to more than 70 pharmaceuticals and other chemicals used in consumer products.
6
“This work lets us put a finger on the chemical pulse of a nation,” Halden says.
Surveying Sludge
As part of the passage of the Clean Water Act in 1972, the U.S. Environmental Protection
Agency (EPA) established requirements for safely disposing of sewage sludge and assessing
the nation’s sludge to stay on top of the chemicals it contains.
7
That’s especially important for treated sewage sludge, which is a popular fertilizer
for agricultural fields. To date, the EPA has conducted four national surveys, most
recently testing samples of sewage sludge from municipal wastewater treatment plants
for dioxins, pharmaceuticals and personal care products (PPCPs), brominated flame
retardants, nine different heavy metals, bacteria, viruses, and parasites.
7
Freezers at the National Sewage Sludge Repository hold hundreds of samples of raw
sewage and sludge collected from more than 200 sites around the United States.
© Arjunkrishna Venkatesan
Awareness of PPCPs as a potential concern began with a 1999 report by Christian Daughton,
a senior research scientist at the EPA, and colleague Thomas A. Ternes. They pointed
out that sewage was a conduit by which low levels of these chemicals were entering
the environment virtually unnoticed. Moreover, it was becoming clear that PPCPs and
other so-called contaminants of emerging concern—those chemicals that are being detected
for the first time or in increasing amounts—tend to elude treatment and remain in
treated water and sewage sludge, returning to the environment and in some cases accumulating
in living organisms, including humans.
8
“There were chemicals that we didn’t know were there, that we didn’t know could be
a health concern, and that we didn’t think to analyze,” Daughton says. “Sewage was
mostly ignored—it’s not seen as being actually in the environment, and it’s not pleasant
to work with.”
Measuring human exposure to all commercially available chemicals is impossible. Testing
for even a handful can be prohibitively expensive, and fully understanding the body
burden of these chemicals would require blood, urine, hair, and fecal samples from
thousands of individuals. Wastewater and residual sludge, however, contain urine and
feces from large numbers of people, and there is plenty of it. And since the samples
can’t be tied to individuals, researchers don’t have to worry about obtaining informed
consent from subjects or approval from institutional review boards.
The EPA began testing for contaminants of emerging concern in the 2001 National Sewage
Sludge Survey, gathering samples from 94 wastewater treatment plants from 32 states
and the District of Columbia.
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But eventually the EPA had more samples than it could use. When Halden, then at the
Johns Hopkins School of Public Health, was asked if he might be interested in taking
charge of the leftovers, he jumped at the chance. “I realized that what they had,
although smelly, represented a human health observatory,” Halden says.
Putting Sludge to Work
Since 2001, Halden had been studying the widely used antimicrobials triclosan and
triclocarban. In 2002, millions of pounds of triclosan and triclocarban were added
to everything from toothpaste to plastics.
10
Halden’s work in the Baltimore metro area had indicated that triclocarban was, at
that time, probably one of the top 10 most frequently occurring organic water contaminants.
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The market for these products has been estimated at $886 million,
12
but publicly available production data for these and other commercially important
chemicals are too vague to use in determining year-to-year trends in chemical consumption,
Halden says. (Meanwhile, his work is contributing to these compounds being phased
out of use in many products.)
What’s more, no one knew exactly what was happening to these products in the environment,
how much might be remaining in treated wastewater, how much was in the biosolids being
used as fertilizer on agricultural land, and how much humans were actually exposed
to in their daily lives. Halden believed samples from the National Sewage Sludge Repository
could provide some of those answers.
The wastewater treatment process involves a variety of physical, chemical, and microbial
processes to remove objects from wastewater (everything from toilet paper and tampons
to dead animals) and eliminate organic matter, harmful microbes, and other contaminants.
The water is then suitable for further treatment to become drinking water.
13
Most chemicals that people are exposed to via consumer products are ultimately washed
off or excreted; they are collected in municipal sewers and sent to wastewater treatment
plants (WWTPs). Fat-soluble chemicals—i.e., those that can accumulate in the human
body—tend to be the ones that resist treatment.
Courtesy Arizona State University
Given that this process is intended to degrade many chemicals, Halden wasn’t sure
if he could find measurable amounts of these antimicrobials in the sewage sludge.
But a preliminary analysis published in 2010 revealed that not only were triclosan
and triclocarban present, their amounts were far higher than Halden expected, accounting
for two-thirds of the PPCPs his team measured in biosolids. The two chemicals amounted
to between 210 and 250 metric tons of product found in sewage sludge around the country
each year, chemicals that were then reapplied to farmland in fertilizer
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and were found to persist in the soil over time.
15
Halden knew from the start that simply measuring the amounts of triclosan and triclocarban
in sludge wouldn’t tell him accurately how much humans had been exposed to. Many of
the products that contained these two antimicrobials—such as soaps and toothpastes—were
designed to be washed down the drain after contact with the human body. So he tested
raw and treated sewage sludge for metabolites of triclosan and triclocarban, such
as 2'-hydroxy-3,4,4'-trichlorocarbanilide, which would more accurately assess human
exposure via ingestion, inhalation, and skin exposure.
16
Halden and colleagues used liquid chromatography–tandem mass spectrometry to measure
the amount of the antimicrobial metabolites in the sludge samples. Next they back-calculated
the amount the average person was exposed to, based on the number of people served
by the wastewater treatment plant. They adjusted for industrial, agricultural, and
commercial contributions to wastewater as well as any recent weather events (in the
eastern United States, storm sewers and sanitary sewers are generally combined before
reaching the treatment plant, so rainfall dilutes the sewage; in the West, they’re
generally kept separate
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).
“Even when looking at the consumer compounds themselves, rather than their metabolites
only, there was a remarkably strong positive linear relationship between both the
types and amounts of chemicals we found in sewage sludge and what the CDC [Centers
for Disease Control and Prevention] found in human testing, which says that this technique
can provide information on chemical body burdens,” Venkatesan says. “This placed in
our hands a real-time screening tool to narrow down what to test for, and to bring
to light in an inexpensive fashion the chemical composition and potential exposures
of millions of people.”
In addition to triclosan and triclocarban, Halden and Venkatesan discovered in the
sludge some 121 chemicals listed as contaminants of emerging concern. About 70% of
the chemicals detected in the sludge had also been measured in human tissue samples
collected as part of the National Health and Nutrition Examination Survey (NHANES).
6
The researchers had some of their first evidence that sewage sludge could provide
reasonably accurate measurements of human exposures to environmental contaminants.
Broadening the Search
The advantages of sewage epidemiology methods over traditional methods of assessing
human exposure to environmental contaminants were becoming clear. As part of NHANES,
the CDC collects urine and blood specimens to measure everything from metals like
lead, copper, arsenic, and mercury to the popular insect repellant DEET. In the world
of environmental studies, NHANES is big—since its inception it has surveyed over 140,000
Americans.
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But the data collected from the 2006–2007 Targeted National Sewage Sludge Survey provided
information on chemical measurements that the authors said could be extrapolated to
more than 3,300 wastewater treatment plants serving millions nationwide.
7
With these advantages in mind, and his early successes looking at triclosan and triclocarban
in sewage sludge, Halden and postdoc Venkatesan began to expand the list of chemicals
they looked for.
When it comes to selecting which compounds to study in sewage and sludge samples,
scientists can’t just blindly begin testing samples. For one thing, not all chemicals
make their way into sludge, especially pharmaceuticals that are highly water soluble.
Those chemicals that tend to be found in sludge are more likely to be hydrophobic,
and therefore fat soluble. “Whatever chemicals are left in the sludge are the persistent
ones. They do not degrade in the sewer lines or in the wastewater treatment plants,
and so [they] can accumulate in sludge,” Venkatesan says. “And chemicals that can
accumulate in sludge can also potentially accumulate in the human body.”
Persistent substances that withstand treatment can find their way into fertilizer
derived from sewage sludge. This popular soil amendment for agricultural fields thus
represents a potential route for anthropogenic chemicals to enter the food supply.
© Justin Kase zsixz/Alamy
Some of the first compounds on Halden’s list were other PPCPs, a laundry list of prescription
medications (including antibiotics, antidepressants, and statins), over-the-counter
medications (acetaminophen, ibuprofen), and surfactants (including alkylphenols and
their ethoxylates, and perfluorinated compounds). As the consumption of drugs increased
with the number of prescriptions written, Halden found, so did the potential for these
chemicals to build up in the water supply and in biosolids. Findings from the 2006–2007
National Sewage Sludge Survey showed that antibiotics including ciprofloxacin had
been in the environment for a long time and were present at relatively stable levels
across the country.
14
As with triclosan and triclocarban, these initial sludge data told Halden how much
of these chemicals might be returned inadvertently to soil.
19
,
20
And for chemicals that persisted during treatment and accumulated in sludge, it also
provided clues on human exposure and other risks, such as the potential for development
of antibiotic resistance in microorganisms native to soils receiving sludge applications.
21
Halden and his team continue to broaden the suite of chemicals they are looking for,
and they have set up a system to share sewage and sludge samples with collaborators
worldwide.
1
For instance, Kurunthachalam Kannan, an environmental scientist at the New York State
Department of Health, worked with Halden and other scientists to show that bisphenol
A and its chemical replacements could be found in sludge, although the amounts that
persisted in biosolids would reflect only a tiny fraction of a human’s average exposure.
22
Halden’s group also detected N-nitrosamines,
23
carcinogens that can arise as by-products of chlorination during wastewater treatment,
24
from residential sources,
25
and from the production of rubber consumer goods.
26
In other studies, they measured levels of brominated flame retardants
27
and their derivative contaminants, which include polybrominated dibenzo-p-dioxins
and dibenzofurans.
28
Halden and Venkatesan have documented the presence of perfluoroalkyl substances
29
(persistent, toxic chemicals used in a variety of industrial, military, and firefighting
processes
30
) and alkylphenol ethoxylates
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(widely used endocrine-active commercial and household detergents).
32
It is especially worrisome that relatively high concentrations of these compounds
were readily found in biosolids from across the United States, because it creates
a positive feedback loop, says Jörg Drewes, a water systems engineer at the Technical
University of Munich in Germany. High human exposures mean higher concentrations in
biosolids, and with the use of biosolids as fertilizer, humans have an additional
route of exposure.
“The simple paradigm in drinking water supply is to provide separation between sewage
and [treated] drinking water. It seemed to work for decades, but then the analytical
chemistry became more sensitive, and we could look at a different level and see that
some of these chemicals were showing up in the drinking water supply,” Drewes says.
Opening Up New Possibilities
According to Halden and Vankatesan, scientists have only begun to scratch the surface
of what can be learned from this type of research. The chemical exposures measured
in NHANES and similar surveys require that scientists know what they are looking for.
The high sensitivity and specificity of liquid chromatography–tandem mass spectrometry
means that researchers can conduct an unbiased search for chemicals in sewage sludge
that may be present in unusually high amounts. When Halden and Vankatesan did just
that, they were able to track 26 chemicals previously unmonitored in U.S. biosolids,
33
as well as identify a variety of potentially problematic chemicals that are produced
in high volumes.
34
Other scientists are taking a new direction. In an unpublished study, a team led by
Italian researcher Sara Castiglioni of the Mario Negri Institute for Pharmacological
Research in Milan has been analyzing the relationship between days with high levels
of air pollution and amounts of albuterol and metabolites found in untreated wastewater.
Albuterol is a medication used in asthma inhalers. Castiglioni’s work thus uses measurements
of these substances at different points in time as a proxy for measuring increases
in asthma symptoms. “We are trying to see whether the use of bronchodilators corresponds
to days with high particulate matter in the air,” she says.
The work is not without its limits, however. Instead of estimating an individual’s
exposure levels, it captures a per capita level that is a community average. Information
gleaned about a community’s chemical exposures also has an inherent amount of uncertainty
in it, as the population is in a constant state of flux. People move away, others
come to the area for business, and heavy rains or melting snow can affect the amount
of water in the sewage system.
Surveys of sewage sludge have revealed varying concentrations of dozens of anthropogenic
chemicals, including a) compounds used in pharmaceuticals and personal care products,
b) surfactants, c) perfluorinated compounds, and d) brominated flame retardants. Analysis
of samples archived at the National Sewage Sludge Repository has revealed the presence
of previously unmonitored compounds (orange bars).
Source: Venkatesan et al. (2015)
1
“We need to distinguish between levels of occurrence and levels of exposure,” Drewes
says, because unmetabolized “parent” chemicals measured in the sewage system can also
reflect situations such as people flushing unused medications down the toilet.
Despite these limits, Halden and others believe that the information flowing through
our sewers provides valuable insights into human health. “It’s like the microbiome,”
he says. “The tools were there, but no one thought to look at all the microbes on
our body. Now it’s a huge field.”
Insights into Whole Communities
Work published in 2001
2
by the EPA’s Daughton served as the foundation for sewage monitoring in estimating
community-wide per capita exposure as well as estimating community health. In 2012
he proposed for the first time that endogenous biomarkers could be used to estimate
actual levels of biological stress or disease in a defined population
35
—this is BioSCIM.
“Up until this work, the chemicals that were targeted in sewage monitoring were anthropogenic
chemicals that were not suited to reflecting stress or health,” Daughton says. His
work showed for the first time that it was possible to estimate health status as a
combined function of all stressors, rather than just exposure to a select class of
chemicals.
More recently, Daughton has focused on molecules called isoprostanes, which are markers
of oxidative stress in the body.
36
High levels of oxidative stress characterize a variety of acute and chronic conditions,
including diabetes, heart disease, cancer, and obesity, and also reflect a wide variety
of unhealthy practices (e.g., smoking) and lifestyles.
37
Daughton hopes that measuring isoprostane levels (or levels of any of numerous other
possible biomarkers) in the sewer systems can provide a snapshot of a community’s
health. The feasibility of the analytical methodology required for monitoring sewage
for isoprostanes was demonstrated in a 2015 report.
38
However, he says, more work is necessary to prove the full feasibility of the approach.
Daughton also believes obesity trends could possibly be gauged by monitoring microbial
signatures in wastewater—that’s because obese individuals tend to have different gut
microbiome signatures than people of normal weight.
39
Preliminary evidence reported in 2015 suggests this may in fact be the case.
40
Researchers found that although microbial species from the human gut made up only
about 15% of the bacterial DNA signatures in sewage, they captured 97% of the species
found in human feces. Further analysis of their data revealed that they could predict
with 81–89% accuracy whether the bacteria in their samples came from “lean” or “obese”
cities (as determined by the percentage of obese residents).
“In the last 15 years, sewage is finally being looked at as a source of chemical information—what
information can be mined, and how can we use it,” Daughton says.
And the field is just getting started. Researchers at the Massachusetts Institute
of Technology recently undertook the development of “smart sewers” that may one day
monitor the bacteria and viruses circulating in sewage to detect infectious disease
outbreaks before they occur.
41
In Europe, a research project called SEWPROF (short for A New Paradigm in Drug Use
and Human Health Risk Assessment: Sewage Profiling at the Community Level)
42
hopes to fund early-career scientists to improve wastewater analysis techniques and
identify biomarkers for tracking human health. Another European initiative conducted
through the European Cooperation in Science and Technology (COST)
43
also seeks to improve community health by identifying sewage biomarkers.
Daughton says many additional applications will likely come to light in the future.
“One example of another distinct application is the estimation of community population
size in near real time—something that has never been possible before,” he says. “Real-time
estimation of population size is critical to SCIM because it’s required to perform
more accurate per capita back-calculations.”
For most people, encountering sewage remains a smelly and profoundly distasteful event,
one that entails a call to the plumber and a pair of sturdy rubber gloves. But the
smelly sewage so many of us write off could provide scientists with the ability to
gauge human health at the population level for greatly reduced cost and in nearly
real time. “This,” Daughton says, “would represent a paradigm shift in the tracking
of public health trends and concerns.”
Halden puts it another way. “This is an information superhighway,” he says. “There
is a huge flow of information that goes almost completely untapped because of our
ignorance.”