Environmental engineers and scientists have played pivotal roles in protecting the
public from viral illnesses, and continue to do so today. We develop drinking
water and municipal wastewater treatment technologies, make discoveries that
inform related regulations and policies, and conduct critical research on the
presence, persistence, and transport of viruses in the environment. A wide range
of impactful research in our field has focused mainly on nonenveloped human
enteric viruses such as human noroviruses and enteroviruses. More recently, a
number of high-profile outbreaks such as Ebola virus, measles, Zika virus, avian
influenzas, SARS, MERS, and the ongoing COVID-19 pandemic have been caused by
enveloped viruses. In addition to the RNA or DNA genomes and protective protein
capsids that are common to all viruses, enveloped virus structures are also
wrapped in bilipid membranes.
The primary mode of transmission for many enveloped viruses is by close contact with
infected individuals. Some enveloped viruses, however, are released to the
environment by the host and persist on surfaces (i.e., fomites), in the air, or in
water, long enough to come into contact with another host for further onward
transmission (i.e., indirect transmission). This includes viruses responsible for
influenza and measles. The primary transmission routes for SARS-CoV-2 (the virus
that causes COVID-19) are believed to be person-to-person contact and by exposure
to large droplets produced from sneezing, coughing or talking, but indirect
transmission routes may also play a role.
1
This potential role
of the environment in the spread of COVID-19 highlights the multitude of applied
research needs that must be addressed to effectively control outbreaks and
pandemics as novel enveloped viruses emerge. Environmental engineers and
scientists are well positioned to apply their unique skill sets and experience
with interdisciplinary research to address these needs.
Virus particles in the air and on fomites are exposed to a range of environmental
conditions that influence their persistence. Relative humidity, fomite material,
and air temperature can greatly impact enveloped virus inactivation
rates.
2−5
Even the medium in which the
virus is suspended can greatly impact persistence.
6
For
example, chlorine-based solutions and hydrogen peroxide gas are effective at
inactivating the enveloped virus surrogate Phi6 on fomites,
7,8
but the presence of
blood requires much higher hydrogen peroxide gas doses.
8
Future
mechanistic studies should probe how specific constituents in the matrix,
temperature, humidity, and solar radiation each impact inactivation. Furthermore,
research quantifying the transfer of enveloped viruses between fomites and skin,
and determining effective hand washing and surface sanitizing methods, is needed
to inform agent-based risk assessment models.
Viruses have a direct connection to wastewater and drinking water purification when
they are excreted in feces or urine (Table 1
),
9
but there is limited data on the
concentration of enveloped viruses in feces and urine. The human coronavirus
responsible for the 2003 SARS outbreak was able to replicate in the human GI tract
and infective particles were detected in stool samples.
10
In
fact, aerosolized fecal particles are believed to have played a major role in
spreading the virus at a Hong Kong apartment complex.
11
Similarly, SARS-CoV-2 genomic RNA has been detected in feces.
12,13
Although infective
SARS-CoV-2 has not yet been confirmed in stool samples, the SARS-CoV-2 RNA
shedding pattern suggests viruses are replicating in the GI tract.
13
Other human enveloped viruses, such as cytomegalovirus (CMV),
are excreted in urine. Research so far on enveloped viruses in wastewater,
including coronaviruses, suggest these viruses are inactivated at faster rates
than most nonenveloped viruses,
14−18
that they partition to
wastewater solids to a greater extent than nonenveloped viruses,
15
and that wastewater temperature is positively associated with
their inactivation rates.
15,18
In water purification processes, they are generally more
susceptible to oxidant disinfectants than nonenveloped
viruses.
19,20
The presence of an envelope does not appear to impact
virus susceptibility to ultraviolet C (UVC) light,
15
likely
because UVC targets virus genomes and lipid membranes do not shield the genomes
from UVC radiation.
Table 1
Mean or Median Viral Loads in the Feces and Urine of Infected
Individuals for Three Enveloped Viruses and Two Nonenveloped
Virusesa
virus
enveloped?
urine (gc/mL)
feces (gc/g)
feces (gc/swab)
source
SARSb
yes
101.3
106.1
NA
(21)
cytomegalovirus (CMV)c
yes
104.5
NA
NA
(22)
SARS-CoV-2d
yes
ND
NA
105
(13)
human norovirus GIIe
no
NA
108.5
NA
(23)
JC polyomavirusf
no
104.6
NA
NA
(24)
a
“gc” is gene copy. NA = not analyzed in study, ND =
analyzed, but not detected in study.
b
Samples from approximately 100 patients with lab-confirmed illness,
mean.
c
Samples from 36 children with lab-confirmed illness, median.
d
Rectal swab samples from 9 patients with lab-confirmed illness
during first week of illness, mean.
e
Samples from 627 patients with gastroenteritis symptoms, median
f
Samples from 71 health blood donors that tested positive or JC
polyomavirus, median.
What does this mean for the SARS-CoV-2 virus and the ability of our water
purification plants to produce safe water? Our drinking water treatment plants,
including those used to produce drinking water from wastewater, were designed
using microbial risk assessments and process performance data with nonenveloped
enteric viruses. Based on the facts that (1) the closely related 2003 SARS was
excreted in feces at lower levels than enteric human noroviruses (Table 1
), (2) model coronaviruses are inactivated
at faster rates in wastewater and other waters than nonenveloped viruses, (3) the
enveloped viruses studied to-date are more susceptible to oxidant disinfectants
than nonenveloped viruses, and (4) the large single-stranded RNA (ssRNA) genome
(∼29.8 kb) of SARS-CoV-2 likely renders it more susceptible to UVC
inactivation than enteric ssRNA viruses, the multibarrier wastewater and drinking
water treatment systems are likely effective in protecting against SARS-CoV-2.
Nonetheless, there may still be water-related exposures that need to be considered
if infectious SARS-CoV-2 viruses are present in urine or feces. Such exposures may
occur in communities that experience combined sewage overflows, that do not have
sewage infrastructure, or that use wastewater for irrigation, as well as buildings
that have faulty plumbing systems and occupational exposures to wastewater and
excrement.
Despite the research outlined above, enveloped viruses are extremely diverse, with
a
range of genome types, structures, replication cycles, and pathogenicities. For
example, of the 158 identified human RNA viruses species as of 2018, 122 species
from 11 virus families were enveloped and 36 species from 6 families were
nonenveloped.
25
Consequently, enveloped viruses likely
display a diverse range of environmental behavior, persistence, and fate.
26
The limited studies on enveloped-virus fate, transport, and
inactivation have focused on only a small fraction of human viruses or their
proxies including animal coronaviruses and bacteriophage phi6. Although studies
using animal coronaviruses have been valuable for the current COVID-19
outbreak,
3,15,27
it is essential to consider an
expanded set of enveloped viruses that better represent human enveloped virus
diversity.
Future studies on enveloped viruses should seek to carefully characterize and even
standardize the conditions under which measurements are conducted. Media
composition, the purity of virus stock, and when possible, virus concentrations in
both gene copies and infective units, should be described. When studying oxidants,
the demand of the solution and change in oxidant concentration through the
experiment should be provided. When studying radiation (UVC and/or sunlight),
attenuation through the experimental solution should be well-characterized
incorporated into reported doses. Researchers should include a well-studied
surrogate virus in their experiments in addition to the enveloped virus of
interest to facilitate cross-study comparisons. We recommend using the
nonenveloped bacteriophage MS2 for this purpose, as it is one of the most studied
viruses in environmental systems.
Finally, there are emerging research areas in our field that we believe can inform
the current COVID-19 outbreak and future novel viral outbreaks. For example,
predictive models based on the underlying mechanisms controlling the persistence
of enveloped viruses, and other characteristics, may reduce the need to study
every virus under every condition.
14
Another promising area of
research involves using sewage to monitor virus circulation in communities and
detect outbreaks before clinical cases are identified. Recently applied to
pathogenic bacteria
28
and nonenveloped viruses,
29
this will necessitate a better understanding of which
enveloped viruses are excreted in urine and feces and at what levels.
SARS-CoV-2 will certainly not be the last novel virus to emerge and seriously
threaten global public health. Researchers and funding agencies have a tendency to
focus intensely on a specific virus during its outbreak, but then move on to other
topics when the outbreak subsides. Given the historical contributions from our
field, and the grand challenges that lie ahead,
30
environmental
science and engineering researchers should take a broader, long-term, and more
quantitative approach to understanding viruses that are spread through the
environment. Similar to how we approach chemical pollutants in the environment, we
should aim to understand and communicate to our colleagues in medicine and public
health the specific characteristics that drive transport and inactivation of
enveloped viruses in solutions, on surfaces, and in the air. Likewise, we should
seek to understand how environmental factors shape possible virus transmission
routes. That way, regardless of the identity of the enveloped virus that causes
the next major outbreak, we can provide more informed descriptions of its
persistence and recommendations on how to mitigate its spread.