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Removal of Viruses in Membrane Bioreactors

Article in Journal of Environmental Engineering · July 2020

DOI: 10.1061/(ASCE)EE.1943-7870.0001743

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 State-of-the-Art Review

Removal of Viruses in Membrane Bioreactors

Evan O’Brien 1 and Irene Xagoraraki, M.ASCE 2

Abstract: This review seeks to summarize the current literature regarding the removal of viruses from wastewater using membrane
bioreactors (MBRs). Membrane bioreactors are an effective technology for the removal of viruses from wastewater and do so with greater
efficiency than conventional activated sludge treatment plants. However, much is unclear about the capabilities and mechanisms of this pro-
cess. Membrane pore size is commonly thought to be an important factor impacting virus removal, but this effect is primarily observed when
the pore size is smaller than the virus diameter, and the effects vary by virus. A variety of factors can impact the effectiveness of MBRs in virus
Downloaded from ascelibrary.org by Evan O'Brien on 04/25/20. Copyright ASCE. For personal use only; all rights reserved.

removal, with the presence of a biofilm foremost among them. Balancing the presence of a biofilm with regular membrane backwashing and
cleaning to maintain consistent flux remains a critical consideration in MBR operation. Differences in reported removal efficiencies of human
viruses compared to model viruses (such as bacteriophages) call into question the reliability of these model viruses in assessing the effective-
ness of virus removal in MBRs. More investigation, particularly with full-scale MBR systems, must be performed to further understand the
potential of MBRs in virus removal. DOI: 10.1061/(ASCE)EE.1943-7870.0001743. © 2020 American Society of Civil Engineers.

Introduction efficiently removed in MBR systems relative to CAS plants

Membrane bioreactors (MBRs) are a state-of-the-art technology
for municipal wastewater treatment involving a combination of
activated sludge process with biomass separation by membrane fil-
tration. There are two primary ways of integrating the membrane
modules into an activated sludge process (Cornel and Krause
2008): the submerged configuration, in which the membranes are
immersed in the mixed liquor and permeate is pumped mechani-
cally or by gravity flow, and the sidestream configuration, in which
the activated sludge is pumped through the membrane module and
then recycled in order to maintain a constant sludge concentration.
Three membrane modules are available for MBRs: hollow fiber,
flat sheet, and tubular, of which hollow fiber and flat sheet are more
prevalent (Asano 2007).
Compared to conventional activated sludge (CAS) reactors,
MBRs present a number of advantages, including better effluent
quality, less performance variability, and a smaller footprint due
to the membrane unit being responsible for filtration and clarifica-
tion, eliminating the need for a clarifier (Choi et al. 2002). Activated
sludge is a component in both CAS and MBR systems, but different
microbial community structures have been observed between the
two systems in many previous studies (Gao et al. 2004; Li et al.
2005; Munz et al. 2008; Silva et al. 2010), and sludge floc size
in MBR systems is smaller compared to CAS systems (Çiçek
et al. 1999; Holbrook et al. 2005), which implies a higher oxygen
transfer rate (Liu et al. 2001).
It is widely accepted that MBRs typically exhibit superior
and more stable performance in pollutant removal compared to
CAS plants. A variety of pollutants, including COD, nitrogen, am-
monium, and total suspended solids have been found to be more
1
Graduate Student, Dept. of Civil and Environmental Engineering,
Michigan State Univ., A10 Engineering Research Complex, East Lansing,
MI 48824 (corresponding author). Email: obrienev@msu.edu
2
Associate Professor, Dept. of Civil and Environmental Engineering,
Michigan State Univ., A124 Engineering Research Complex, East Lansing,
MI 48824. Email: xagorara@msu.edu
Note. This manuscript was published online on April 25, 2020. Discus-
sion period open until September 25, 2020; separate discussions must be
submitted for individual papers. This paper is part of the Journal of En-
vironmental Engineering, © ASCE, ISSN 0733-9372.
(González et al. 2007; Munz et al. 2008; Soriano et al. 2003).
Most full-scale MBRs can also achieve high removal efficiency
for bacteria, and membrane pore size appears to be an important
factor. MBRs are regularly reported to achieve removal in excess
of 6 logs for bacteria (Yin and Xagoraraki 2014). One study (Aidan
et al. 2007) reported that an MBR equipped with an 0.8-μm
ceramic membrane could only remove 39% of coliform bacteria,
whereas high or complete removal was achieved by using mem-
branes with smaller pore sizes in the range of 0.01–0.1 μm
(Herrera-Robledo et al. 2010; Hirani et al. 2010; Saddoud et al.
2007). Another study (Gallas-Lindemann et al. 2013) also reported
high removal efficiencies for Giardia (99.4%) and Cryptosporidium
(94.2%) in a full-scale MBR.
Viruses, meanwhile, are small compared to other pathogens,
making them less susceptible to membrane filtration. Even the larg-
est viruses, such as adenovirus, are only 70–90 nm in diameter,
while bacteria are typically larger than 1 μm with protozoa larger
still. Viruses are the most abundant microorganisms on the earth
(Madigan and Martinko 2006). It has been suggested that more than
150 types of enteric viruses are excreted in human feces and may be
present in contaminated waters (Havelaar et al. 1993; Leclerc et al.
2000; Wong et al. 2012). Wastewater is one of the most concen-
trated sources of infectious viruses (Castignolles et al. 1998;
Puig et al. 1994). The estimated mean concentration of enteric
viruses in wastewater in the United States has been said to be ap-
proximately 7,000 infectious viruses per liter (Melnick et al. 1978),
and the highest concentrations of viral particles can reach 109 per
liter (Kuo et al. 2010; da Silva et al. 2007; Simmons et al. 2011).
Wastewater utilities may release viruses to environmental waters
via treated effluent discharge and biosolids that are land applied.
Removal of viruses from wastewater is critical for potential waste-
water reuse purposes.
Table 1 presents a summary of characteristics of human viruses
and bacteriophages regularly studied in wastewater (USEPA 2015;
Xagoraraki et al. 2014). Many of these viruses are similar in size
and structure, and most viruses have negative surface charge. The
most commonly used methods for quantification of viruses are
quantitative polymerase chain reaction (qPCR) for enteric viruses
and via plaque assay for bacteriophages. qPCR has the advantage
of being rapid, sensitive, and reliable (O’Brien et al. 2017b);

© ASCE 03120007-1 J. Environ. Eng.

J. Environ. Eng., 2020, 146(7): 03120007

 Table 1. Summary of characteristics of human viruses and bacteriophages regularly studied in wastewater
Virus Group Family Examples Approximate size (nm) Structure
Adenoviruses dsDNA Adenoviridae human adenovirus 90–100 Nonenveloped, icosahedral
Caliciviruses ssRNA(+) Caliciviridae norovirus, sapovirus 30–40 Nonenveloped, icosahedral
Enteroviruses ssRNA(+) Picornaviridae poliovirus, coxsackievirus, echovirus 22–30 Nonenveloped, icosahedral
F-specific coliphages ssRNA(+) Leviviridae MS2, F2 27 Nonenveloped, icosahedral
Somatic coliphages dsDNA Myoviridae T4 90 Nonenveloped, tailed
Podoviridae P22 60 Nonenveloped, tailed
Microviridae phiX174 30 Nonenveloped, icosahedral
Note: dsDNA = double-stranded DNA; and ssRNA(+) = positive-sense single-stranded RNA.

however, it will quantify viruses that are both infective and non- Virus Removal in Full-Scale MBRs
infective. Plaque assay, meanwhile, will only quantify infective
Many studies have investigated the removal of viruses by full-
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viruses, but it is more laborious (Guo et al. 2015).

While membrane bioreactors are an effective technology for the
removal of viruses from wastewater, much is still unclear about
the capabilities and mechanisms of this process as well as which
viruses are removed most efficiently and why. This review seeks to
present an overview of the current literature regarding the removal
of viruses from wastewater using membrane bioreactors, summa-
rize findings from studies investigating full-scale treatment plants,
analyze factors that may contribute to virus removal efficiency, and
offer suggestions for future research to improve the understanding
and performance of virus removal in MBRs.
scale membrane bioreactors in wastewater treatment plants. Table 2
summarizes these studies. It is important to acknowledge that
the log removal values listed in Table 2 are attributed to removal
by primary and secondary treatment, given that all of the studies
listed quantified viral concentration at the WWTP influent and
membrane effluent and determined log removal based on those
measurements [except for two studies, Francy et al. (2012) and
Chaudhry et al. (2015b), which measured membrane influent in
favor of raw influent]. The values reported in these studies, there-
fore, represent the membrane permeate and do not take disinfection

Table 2. Summary of prior studies investigating virus removal in full-scale membrane bioreactors
Membrane Removal
pore Capacity Detection efficiency
size (um) Location (m3 =d) MBR type Virus methods (logs) Reference
0.4 Northwest France 390 DNS Norovirus I qPCR 0–5.3 da Silva et al. (2007)
Norovirus II 0–5.5
0.1 Traverse City, MI 32,000 Submerged Human adenovirus qPCR 4.1–5.6 Kuo et al. (2010)
0.4 Bologna, Italy 1,935.36 Submerged F-specific coliphage Plaque assay 6.0 Zanetti et al. (2010)
Somatic coliphage 4.0
0.45 Northwest France 270 Submerged Norovirus qPCR 3.3–6.8 Sima et al. (2011)
Sapovirus 1.8–4.1
0.1 Traverse City, MI 32,000 Submerged Human adenovirus qPCR 3.4–4.5 Simmons and
Enterovirus 2.9–4.6 Xagoraraki (2011)
0.1 Traverse City, MI 32,000 Submerged Human adenovirus qPCR 4.1–6.3 Simmons et al. (2011)
Enterovirus 4.1–6.8
Norovirus II 3.5–4.8
0.4 Northern OH 12,900 DNS F-specific coliphage Plaque assay 4.58–6 Francy et al. (2012)
Somatic coliphage 2.67–4.04
Human adenovirus qPCR 2.38–4.86
Enterovirus 2.2–4.74
Norovirus I 1.51–3.32
0.4 Bologna, Italy 1,935.36 Submerged F-specific coliphage Plaque assay 5.77 De Luca et al. (2013)
Somatic coliphage 4.35
0.04 American Canyon, CA 5,700 Submerged Human adenovirus qPCR 3.9–5.5 Chaudhry et al. (2015b)
Norovirus II 4.6–5.7
F-specific coliphage 5.4–7.1
0.04 London, UK 574 Submerged Somatic coliphage Plaque assay 5.3 Purnell et al. (2015)
F-specific coliphage 3.5
Human-specific coliphage 3.8
DNS Southern CA 105,992 Side-stream Total viruses Flow cytometry 4.0 Huang et al. (2016)
0.4 Thuwal, Saudi Arabia 1,600 Submerged Human adenovirus dPCR 3.7 Jumat et al. (2017)
Enterovirus 1.7
0.4 Northwest France 1,800 Submerged Sapovirus qPCR 3.0 Miura et al. (2018)
Rotavirus 2.0
Norovirus 3.0
0.05 Sao Paulo, Brazil 164,160 Submerged Norovirus I qPCR 1.1 Prado et al. (2019)
Norovirus II 1.2
Note: DNS = did not specify.

© ASCE 03120007-2 J. Environ. Eng.

J. Environ. Eng., 2020, 146(7): 03120007

 into account regarding the treated wastewater effluent released into
the environment.
Several of these studies have utilized bacteriophages as viral
indicators to model the removal of viruses, and these studies have
reported removal of viral indicators ranging from 1.7 log removal to
7.1 log removal, demonstrating the capability of MBRs to effec-
tively remove viruses from wastewater (De Luca et al. 2013;
Francy et al. 2012; Purnell et al. 2015; Zanetti et al. 2010). Other
studies have investigated the removal of human viruses in full-scale
MBR wastewater treatment facilities. These studies have shown
that MBRs are also effective in the removal of human viruses from
wastewater, with efficiencies ranging up to 6.8 log removal. MBRs
have been shown to remove human viruses from wastewater with
greater efficiency than conventional activated sludge treatment
plants (Xagoraraki et al. 2014; Xiao et al. 2019).
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Despite the effectiveness of MBR systems and disinfection tech-
nologies such as chlorine and ultraviolet light, human viruses have
still been detected in wastewater effluent after these treatment steps
by many of these studies (Francy et al. 2012; Huang et al. 2016;
Jumat et al. 2017; Simmons and Xagoraraki 2011). Other studies
investigating treated effluent of MBR plants have reached the same
conclusion, detecting human viruses in effluent with both molecu-
lar and metagenomic methods (O’Brien et al. 2017a).
Parameters That Affect Virus Removal
In addition to the study of full-scale utilities, bench- and pilot-scale
MBR systems can assist in the evaluation of different factors on the
removal efficiency of viruses from water and wastewater. Numer-
ous studies have investigated a variety of factors that can impact
removal efficiency of viruses, and these factors are summarized
in the subsequent section.
Membrane Pore Size
One point of differentiation among the various full-scale studies is
the pore size of the membrane used in the MBR facilities. A chart
summarizing removal of viruses in relation to pore size is presented
in Fig. 1. While the studies are limited in number, for some viruses,
studies utilizing smaller pore sizes led to higher log removal values
than studies with larger pore sizes. Log removal of adenovirus has
been reported in the range of 2.38–4.86 with a membrane pore size
of 0.4 μm (Francy et al. 2012; Jumat et al. 2017), whereas ranges
from 4.1–6.3 have been reported with a pore size of 0.1 μm (Kuo
et al. 2010; Simmons et al. 2011). These studies find the same for
enterovirus; log removal of 1.7–4.74 is reported for membranes
with a pore size of 0.4 μm (Francy et al. 2012; Jumat et al.
2017), while another study reports log removal of 4.1–6.8 with
a pore size of 0.1 μm (Simmons et al. 2011). Norovirus, mean-
while, does not follow this trend; for example, one study using
a membrane pore size of 0.45 μm reported log removal from
3.3–6.8 (Sima et al. 2011), with another study utilizing a membrane
pore size of 0.05 μm reporting log removal of 1.1 (Prado et al.
2019). To confirm this observation, reported log removal values
of norovirus by a membrane pore size of 0.4 μm or greater were
compared with those by a pore size of 0.1 μm or less using a t-test.
No significant difference was found between the two groups
(p-value ¼ 0.62).
Other full-scale studies report similarly inconsistent log removal
values for model bacteriophages with regards to pore size. For in-
stance, one study investigating somatic coliphages reported a log
removal from 2.67–4.04 using a membrane with a 0.4-μm pore size
(Francy et al. 2012), and two other studies reported log removal
results of 4.0 (Zanetti et al. 2010) and 4.35 (De Luca et al. 2013).
© ASCE 03120007-3
J. Environ. Eng., 2020, 146(7): 03120007
Another study that utilized a membrane pore size of 0.04 μm
instead reported log removal of 5.3 for somatic coliphage (Purnell
et al. 2015), slightly higher than the studies with a larger pore size.
However, these same studies report opposite results for that of
F-specific coliphages. The studies with a pore size of 0.4 μm report
log removal values of 4.58–6.0, 6.0, and 5.77 for F-specific coli-
phage, while the study using a pore size of 0.04 μm reported a log
removal value of 3.5 for the same indicator. It is worth noting that
when comparing studies utilizing different full-scale utilities, other
operational parameters may vary aside from pore size. These other
operational variables [such as flow rate, mixed liquor suspended
solids (MLSS) concentration, and frequency of membrane cleaning
or backwash] among the utilities could be one explanation for the
inconsistencies regarding pore size.
Several bench-scale studies have also investigated the effects of
membrane pore size on removal efficiency of viruses. One study
measured removal of bacteriophage MS2 (size of 0.025 μm) in
membranes with pore sizes of 0.1, 0.08, 0.05, 0.04, and 0.03 μm.
No significant differences in removal efficiency of indigenous MS2
were observed among the different membranes (Hirani et al. 2010).
Other studies also showed no significant difference in the removal
of bacteriophage T4 (size of 0.11 μm) between two membranes
with pore sizes of 0.1 and 0.22 μm (Lv et al. 2006; Zheng et al.
2005). Another study, however, produced different results, with
removal efficiency of bacteriophage T4 reported as 2.1 logs for
a membrane with 0.22 μm pore size and 5.8 logs for a membrane
with 0.1 μm pore size. Furthermore, removal efficiency of bacte-
riophage f2 (size of 0.025 μm) was reported as 0.3 and 0.5 logs for
the 0.22 μm and 0.1 μm membranes, respectively (Zheng and
Liu 2007).
Membrane Biofilm
The role of the membrane biofilm in virus removal by MBRs has
been studied in several bench-scale experiments. One such experi-
ment (Wu et al. 2010) found that a clean membrane with a pore size
of 0.4 μm contributed only approximately 0.5 logs removal of so-
matic coliphages. However, when covered with a biofilm, the same
membrane could remove 1.8 to 2.6 logs of the virus. Similarly,
another study (Shang et al. 2005) observed that an MBR with
the nominal pore size of 0.4 μm could initially (i.e., prior to mem-
brane fouling) remove just 0.4 logs of MS-2 coliphage. After
21 days of operation, the removal efficiency increased to 2.3 logs;
the study concluded that membrane biofilm played an important
role in removing the virus. However, another study indicated that
the presence of a biofilm was not necessarily a reliable indicator in
removal efficiency of adenovirus (Yin et al. 2015).
Different elements of the MBR biofilm have been found to have
different contributions to the removal of viruses from wastewater.
One bench-scale study (Lv et al. 2006) determined that the cake
layer and gel layer of the membrane that develops during operation
make major contributions to virus removal. In the study, the oper-
ation of the membrane with developed gel and cake layers was per-
formed, followed by destruction of the cake layer and operation of
the membrane with the gel layer, and finally removal of the gel
layer and operation of the membrane itself. The experiment resulted
in 1.7 log, 3.1 log, and 6.3 log removal of bacteriophage T4 for the
0.22 μm membrane itself, the membrane with the gel layer, and the
membrane with the gel and cake layers, respectively. This study
also found that for the 0.1 μm membrane investigated, the mem-
brane alone was responsible for complete virus removal, implying
that pore size can also impact which membrane components
become responsible for removal. Another study observed that the
permeability of the cake layer can determine whether the removal
J. Environ. Eng.
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(a) (b)

(c) (d)

(e)

Fig. 1. Summary of studies reporting log removal of viruses in full-scale MBR systems in relation to pore size for (a) adenovirus; (b) enterovirus;
(c) norovirus; (d) F-specific coliphage; and (e) somatic coliphage. Values are represented as the maximum, central tendency, and minimum as reported
by the references. *Reference only reported an average value. ^Reference only reported minimum and maximum values.

efficiency of viruses increases or decreases due to cake formation
(Yin et al. 2015).
Membrane Cleaning
While membrane fouling leads to development of a biofilm that
aids in virus removal, fouling also decreases flux through the
membrane and therefore lowers flow rate and efficiency of the
treatment plant. Because of this, cleaning of the membrane via
backwashing and chemicals is important to treat sufficient quan-
tities of water. Numerous bench-scale studies have investigated
the effects of membrane cleaning on virus treatment, often leading
to lower levels of removal of bacteriophages (Hirani et al. 2010;
Lv et al. 2006; Tam et al. 2007; Zheng et al. 2005). Another study

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J. Environ. Eng., 2020, 146(7): 03120007

 specifically looking at the effects of backwashing (Yin et al.
2016) determined similar results; backwashing and pressure relax-
ation increased membrane flux but decreased removal of human
adenoviruses.
Gas sparging is commonly used to control membrane fouling in
MBR systems. One bench-scale study (Fox and Stuckey 2015)
investigated the impact of different sparging rates on the removal
efficiency of MS2 and T4 bacteriophages using a 0.4-μm pore size
membrane with a surface area of 0.1 m2 . Sparging rates from 10 to
2 liters per minute were evaluated, and the experiment found that
higher sparging rates yielded lower removal of the bacteriophages.
For sparging rates between 4 and 10 L=min, log removal ranged
from 1.75–2.10 for MS2 and 5.1–5.3 for T4, whereas a sparging
rate of 2 L=min increased log removal to 3.0 for MS2 and yielded
complete removal of T4. This increased removal was again attrib-
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uted to increased fouling levels at lower sparging rates.
Membrane Flux
One aforementioned bench-scale study (Wu et al. 2010) also sub-
jected a clean membrane to different operational fluxes and mea-
sured the efficiency of the membrane in the removal of somatic
coliphage. The 0.4-μm clean membrane was subjected to fluxes
of 12.5, 10.0, and 7.5 L m−2 h−1 and yielded log removal values
of 0.7, 0.5, and 0.6 logs, respectively. Therefore, operational flux
was not found to have a significant impact on removal efficiency of
somatic coliphage. However, when applying different fluxes to a
continuously operating membrane with developed cake and gel
layers, the experiment found that the removal efficiency of the
gel layer increased with increased flux. The study claims that
higher flux leads to higher rate of fouling, enhancing the develop-
ment of the gel layer and its ability to entrap viral particles. Mem-
brane flux may also impact virus removal in other ways. One study
(Hirani et al. 2010) found that changes in flux can affect the MLSS
concentration in an MBR, and another study found that MLSS
concentration is related to removal efficiency of certain viruses
(Miura et al. 2015).
Membrane Coatings
Photocatalytic coatings have been found to improve removal effi-
ciency of viruses when paired with ultraviolet (UV) disinfection.
One bench-scale study (Guo et al. 2015) investigated the removal
of bacteriophage P22 using a membrane with a pore size of 0.8 μm
in which the membrane was coated with a photocatalyst (TiO2 ).
The coated membrane was coupled with UV to make a hybrid
MF-UV treatment process. This process was considerably more ef-
fective at inactivating P22 (log removal of 5.0) than the membrane
without the photocatalytic coating (log removal of 2.4) or micro-
filtration and UV disinfection applied in series (log removal of 2.0).
Similar results were observed when measuring the inactivation of
human adenovirus (HAdV) in a subsequent study again utilizing a
TiO2 -coated 0.8-μm membrane (Guo et al. 2018), with removal of
infectious HAdV being a full log greater for the hybrid photoca-
talytic process than the membrane alone or the hybrid nonhotoca-
talytic process.
Mechanical Failure
Various mechanical failures can impact MBR operation, including
aeration failure, washout of biomass, compromised membranes via
fiber abrasion, and breakage of membrane fibers. One bench-scale
study investigated the effects of these events (Branch et al. 2016).
A control experiment was first performed with normal operation
of the 0.04-μm membrane to determine log removal of FRNA
© ASCE 03120007-5
J. Environ. Eng., 2020, 146(7): 03120007
bacteriophage, and log removal values of 4.1–7.3 were reported.
Aeration failure was modeled by switching off aeration to the bio-
mass and membrane compartment for 24 h. FRNA removal was not
affected in this trial, which was described as unexpected by the
authors. Biomass washout was modeled by the direct membrane
filtration of wastewater. Upon startup without biomass, FRNA re-
moval significantly declined to 4.0 logs, but recovered to 4.8 logs
after 3 days of operation. To model compromised membranes, one
of the four minimodules on the MBR rack contained 5–50 μm de-
fects in the membrane fibers resulting from sharp foreign objects in
situ during operation as detected by scanning electron microscopy.
In this case, log removal of phage fell to 3.5 but recovered within
1 day. For breakage of membrane fibers, 4% of the fibers in the
membrane were cut. Immediately upon the cutting of fibers, log
removal of FRNA would decline, but would recover to typical lev-
els within minutes.
Virus Type and Concentration
Certain human viruses appear to be more easily removed by full-
scale MBRs than others. Studies measuring the removal of both
human adenovirus and enterovirus reported log removal values that
were higher for adenovirus compared to enterovirus within the
same study, sometimes to a large degree (Francy et al. 2012;
Jumat et al. 2017; Simmons and Xagoraraki 2011), although one
study reported the two viruses as having approximately equivalent
log removal values (Simmons et al. 2011). Other studies that did
not investigate both viruses together reported consistent log re-
moval values, on the order of 4 log removal. Norovirus, meanwhile,
was sometimes reported to have lower log removal values com-
pared to adenovirus and enterovirus (Francy et al. 2012; Simmons
et al. 2011), while one study reported log removal values equal or
higher than adenovirus (Chaudhry et al. 2015b). Other studies in-
vestigating norovirus report conflicting values as well, with one
reporting 1.1–1.2 log removal (Prado et al. 2019) and others rang-
ing from 3.3 to 6.8 log removal (Sima et al. 2011). Another study
surveying an MBR plant over the course of several months found a
relatively constant effluent concentration of norovirus regardless of
influent concentration (da Silva et al. 2007).
Bench-scale studies also show that certain viruses are often
found to undergo higher removal efficiencies in MBR systems than
others. One study (Ottoson et al. 2006) compared the removal ef-
ficiency of four viruses (enterovirus, norovirus, somatic coliphage,
and F-specific coliphage) with a 0.4-μm membrane. Somatic col-
iphages and F-specific coliphages were found to have mean log
removal values of 3.08 and 3.78, respectively, while enterovirus
and norovirus were determined to have mean log removal of
1.79 and 1.14, respectively. Not only does this difference show
a distinction between removal of different human viruses, but it also
brings into question the use of bacteriophages as models for human
viruses. Another study (Miura et al. 2015) using a 0.4-μm MBR
system also investigated removal of enterovirus and norovirus,
as well as sapovirus, via monthly sampling over a period of
16 months. Similar results were found, with enterovirus and nor-
ovirus having log removal values in the range of 0.3–3.2 (mean of
1.6) and 0.2–3.4 (mean of 1.3), respectively. The two viruses were
nearer in log removal for this study, but removal of enterovirus still
outpaced that of norovirus. Sapovirus, meanwhile, had higher re-
moval efficiency than both of the other viruses, with log removal
values in the range of 1.3–4.1, again demonstrating that virus
type can impact removal efficiency in MBRs. The study suggested
that the differences observed among the three viruses could be
attributed to how well the virus associates with MLSS, with
J. Environ. Eng.
 sapovirus most readily associating with MLSS of the three viruses
studied.
A different bench-scale study (Chaudhry et al. 2015a) appears to
support this notion. The removal of three bacteriophages of similar
size and shape by an MBR system with a pore size of 0.04 μm was
investigated. While each virus type was removed at similar rates by
the membrane and cake layer, removal associated with attachment
to biomass was largely different despite the similar structures of the
three phages. The study stated that electrostatic interactions could
not explain these differences.
Another bench-scale study (Lu et al. 2016) investigated the
effect of virus concentration in wastewater on removal efficiency
by a 0.2 μm membrane. The study found that as virus concentration
increased, so did the removal efficiency of human adenovirus
by the membrane. HAdV concentrations of 1.3e7, 5.2e7, and 3.
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4e8 copies=mL corresponded to log removal values of 0.5, 1.1,
and 1.8 respectively. This effect was attributed to a more rapid de-
velopment of an irreversible fouling layer on the membrane. It is
noteworthy, however, that this trend implies that the effluent con-
centration was independent of the influent concentration of HAdV
in this experiment.
Wastewater Characteristics
Characteristics of the wastewater influent itself have also been
found to impact removal efficiency of viruses in MBRs. Another
bench-scale study (Branch et al. 2016) investigated the impact of
high concentrations of salt (NaCl), ammonia (NH3 ), and COD on
the removal efficiency of FRNA bacteriophages by a 0.04-μm
membrane. To establish baseline log removal, normal operation
of the membrane with no chemical additives yielded log removal
values in the range of 4.1–7.3. The addition of 20 g=L NaCl low-
ered the removal efficiency from 5.4 logs before NaCl addition to
3.9 logs 1 day following NaCl addition; this reduction was theo-
rized to be attributed to a reduction of virus adsorption to activated
sludge flocs due to increased ionic strength. A concentration of
0.7 g=L NH3 also depressed removal efficiency to from 5.6 logs
to 4.4 logs, and this change was attributed to the increase in pH
limiting FRNA aggregation. A 5 g=L COD concentration, mean-
while, significantly increased removal of FRNA to >6.9 logs, sig-
nifying complete removal of the virus. This change was attributed
to the reduction in pH inducing higher degrees of phage adsorption
to other phages and flocs.
The addition of coagulants has been found to improve the re-
moval of viruses. One bench-scale study (Fiksdal and Leiknes
2006) investigated removal of bacteriophage MS2 with a 0.2-μm
membrane and found little to no removal with no coagulants added
to the influent stream. Addition of aluminum-based coagulants
improved removal efficiency to log removal ranges of 6.7–7.5, a
dramatic increase compared to that with no coagulation.
Discussion
It is clear that membrane bioreactors are highly efficient at remov-
ing viruses from wastewater. What remain unclear in the current
literature are the precise mechanisms and factors that contribute
to this removal. The review of studies investigating full-scale MBR
systems shows conflicting information about which viruses are
most efficiently removed in MBRs. Some studies that compared
multiple human viruses within the same experiment report higher
log removal values for adenovirus compared to others, such as
enterovirus, while others show no marked difference between the
two. Moreover, removal efficiency for norovirus appears to vary
from study to study, with log removal ranging from 1.1 to 6.8
© ASCE 03120007-6
J. Environ. Eng., 2020, 146(7): 03120007
depending on the study. Additionally, the observation from one
study that effluent concentration was constant regardless of influent
concentration implies that for some viruses (in this case norovirus)
it may not be feasible to reduce the effluent concentration below a
certain value.
Membrane pore size is one factor that is often cited as an ex-
planation for these differences. Smaller pore sizes often lead to
higher removal efficiencies in full-scale systems for some viruses,
such as adenovirus and enterovirus, as observed in Fig. 1. However,
this is not always the case, because pore size does not appear to
have a conclusive relationship with the removal efficiency of nor-
ovirus in full-scale MBRs based on the available data. While
virus size could potentially explain the relationship of pore size
with the relatively large adenovirus (d ¼ 90–100 nm), enterovirus
(d ¼ 25–30 nm) and norovirus (23–40 nm) are both approximately
the same size yet exhibit different trends of log removal with re-
gards to membrane pore size. The same is true when investigating
the removal of bacteriophages in full-scale systems; Fig. 1 shows
that while the removal of somatic coliphage may be impacted by
pore size, removal of F-specific coliphages does not appear to have
any relationship with pore size. This difference is also observed in
studies investigating the effects of pore size utilizing bench-scale
systems. Removal of bacteriophages in bench-scale MBR systems
often do not exhibit any relationship with pore size, although some
studies indicate that pore size may matter when it is smaller than
virus size. A previous paper summarized removal of bacteriophages
in relation to pore size and reached similar conclusions (Xagoraraki
et al. 2014). Ultimately, though, the available data is limited, and
more studies are needed to better establish the relationship between
pore size and removal of different viruses.
Further complicating the use of bench-scale systems to study
virus removal is the fact that bacteriophages used to model enteric
human viruses often exhibit log removal values considerably higher
than the human viruses, even within the same study. For example,
one study (Ottoson et al. 2006) reported much higher log removal
for bacteriophages (3.08 for somatic coliphage, 3.78 for F-specific
coliphage) compared to human viruses (1.79 for enterovirus, 1.14
for norovirus). Based on the available data from the reference, a
two-tailed t-test determined that the phage removal values were sig-
nificantly different from the human virus removal values to >99%
confidence (p-value ¼ 0.002). The same is true in studies that have
quantified both bacteriophages and human viruses in full-scale
MBR systems. Fig. 1 shows that somatic coliphage may appropri-
ately model human viruses in full-scale systems, but this is not the
case for F-specific coliphage; one full-scale study (Chaudhry
et al. 2015b) reported removal of F-specific coliphage at higher
levels than that of adenovirus and norovirus. Both of the studies
mentioned in this paragraph noted that the observed disparities
could arise from differences in quantification methods between
phages and human viruses. Nonetheless, this discrepancy compli-
cates comparisons between removal of phages and human viruses.
Until there is adequate reconciliation of these quantification meth-
ods, the use of phages as model organisms may overestimate the
actual effectiveness of MBR systems to remove human viruses.
Moreover, the variation in removal efficiency observed among dif-
ferent virus types makes it a challenge to determine the use of a
single model virus.
Nonetheless, model bacteriophages are still useful on the
bench-scale as predictors of the efficiency of full-scale operation.
While direct comparisons are difficult to perform due to the variety
of confounding variables, comparisons of studies utilizing the
same virus and membrane pore size tend to show similar results
between bench- and full-scale operation of MBRs. For example,
a bench-scale study reported 4.1–7.3 log removal of F-specific
J. Environ. Eng.
 coliphage with a 0.04 um membrane (Branch et al. 2016), while a
full scale study reported 5.4–7.1 log removal with those same con-
ditions (Chaudhry et al. 2015b). Likewise, 3.08 log removal of
somatic coliphage by a 0.4 um membrane was reported in a
bench-scale study (Ottoson et al. 2006), with several full-scale
studies reporting similar values under those same conditions (De
Luca et al. 2013; Francy et al. 2012; Zanetti et al. 2010).
Model bacteriophages are also useful when assessing factors
that can impact virus removal by MBR systems on the bench-scale.
Of all factors explored in the literature, it is clear that membrane
fouling is the factor that has the most important impact on removal
efficiency of viruses by MBRs. Numerous studies have reported
that the clean membrane does not contribute to virus removal
nearly as much as that of the cake and gel layers that are developed
through membrane operation and fouling. As such, methods of
Downloaded from ascelibrary.org by Evan O'Brien on 04/25/20. Copyright ASCE. For personal use only; all rights reserved.
membrane cleaning, including backwash and gas sparging, have
been determined to lessen the efficiency of the membrane to re-
move viruses from wastewater. This naturally introduces a conun-
drum in which plant operators must decide between maintaining
sufficient flux through the membrane and achieving adequate re-
moval of viral pathogens from wastewater. Some studies have
sought to explore this problem by investigating how to optimize
membrane fouling mitigation with respect to virus removal, finding
that longer backwashes at a lower flowrate can minimize the neg-
ative impact on virus removal (Yin et al. 2016). Still, more inves-
tigation is necessary to determine how best to achieve fouling
mitigation while maintaining peak efficiency for virus removal.
Additionally, much remains unclear as to the precise mechanisms
which cause viruses to adhere to the biofilm surface. Given that the
evidence shows that this is the primary removal process in an MBR,
more research must be done as to what virus structures, virus sur-
face characteristics, and other chemical entities most readily pro-
mote this mechanism in order to fully optimize virus removal
by MBRs.
Moreover, while it is clear that MBRs are effective at meeting
regulations for virus removal in wastewater treatment, the studies
available in the literature do not present a clear picture as to the true
potential of full-scale MBR systems in the removal of human en-
teric viruses from wastewater. A variety of factors, such as virus
type, water quality, membrane characteristics (e.g., pore size, coat-
ings, etc.), and operational parameters have been shown at the
bench-scale to impact performance of MBR systems in virus re-
moval, but many of these factors have not been sufficiently inves-
tigated in full-scale MBR treatment plants. Even among current
full-scale studies, it remains unclear which viruses are most suscep-
tible to removal from wastewater by MBRs. More experiments
applying these variables to full-scale MBR systems can help to
elucidate how MBRs can most optimally treat viral pathogens in
wastewater.
Conclusions
MBRs remain the most efficient choice in full-scale treatment
plants for the removal of viruses from wastewater, but it is unclear
which human enteric viruses are most effectively removed by
MBRs and why differences in removal efficiency exist among dif-
ferent viruses. Membrane fouling is the most important factor in
determining removal efficiency of viruses by MBR systems, and
the removal of the fouling layer via the cleaning of membranes
is the greatest hindrance to virus removal. The balance of sufficient
membrane flux with sufficient removal of viruses is a critical opera-
tional decision in the use of MBRs. Membrane pore size may have
an effect on virus removal when the pore size is smaller than virus
© ASCE
J. Environ. Eng., 2020, 146(7): 03120007
diameter and the effects vary by virus. Bacteriophages used to
model human viruses often exhibit higher removal efficiencies than
that of human viruses, so their use in the investigation of full-scale
MBR systems may overestimate the effectiveness of virus removal.
A great deal of progress has been made in the development of MBR
technologies to remove viruses from wastewater, but more inves-
tigation is still required to fully understand the capability of MBRs
in wastewater treatment with regards to viral pathogens.
Data Availability Statement
All data, models, and code generated or used during the study
appear in the published article.
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