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EFFICACY OF BIOFLAVONOIDS OF FLAVOBAC™
Original Articles
AGAINST SEVERE ACUTE RESPIRATORY SYNDROME -
CORONAVIRUS 2 IN VITRO
1a 2b 3c 4d
Abdelahhad Barbour , Lynda Gail Darlington , Michelle Mendenhall , Henriette Lerner ,
1,5,6e*
Michael Glogauer
1
Faculty of Dentistry, University of Toronto, Toronto, ON, Canada, M5G 1G6
2
Department of Internal Medicine, Ashtead Hospital, Ashtead, UK
3
Institute for Antiviral Research, Utah State University Logan, UT, USA
4
Goethe University, Frankfurt, GER
5
Department of Dental Oncology, Maxillofacial and Ocular Prosthetics, Princess Margaret Cancer Centre, Toronto, ON, Canada, M5G 2M9
6
Oral Science International Montreal, Canada
a
DaMSc, PhD, Postdoctoral Fellow; e-mail: abdelahhad.barbour@utoronto.ca; ORCIDiD: https://orcid.org/0000-0003-0184-8890.
b
MD, FRCP, e-mail: gail.darlington1@nhs.net
c
MSc; e-mail: michelle.mendenhall@usu.edu; ORCIDiD: https://orcid.org/0000-0001-6417-0648.
d
DDS; e-mail: h-lerner@web.de ORCIDiD: https://orcid.org/0000-0002-4894-9560
e
DDS, PhD, Professor; e-mail: michael.glogauer@utoronto.ca; ORCIDiD: https://orcid.org/0000-0002-6248-5977
ABSTRACT https://doi.org/10.25241/stomaeduj.2021.8(2).art.1
Introduction The Severe Acute Respiratory Syndrome-Coronavirus 2 (SARS-CoV-2) is responsible for the
global pandemic of Coronavirus disease-2019 (COVID-19). Human-to-human transmission occurs mainly
through the aerosolization of respiratory droplets. Improved antisepsis of human and non-human surfaces
has been identified as a key feature of transmission reduction. Flavobac, a complex of soluble bioflavonoids
and hydroxylated phenolic structures used in oral care products, has demonstrated efficacy to act against
microorganisms. This study evaluated nasal and oral antiseptic formulations of FLAVOBAC for the virucidal
activity against SARS-CoV-2.
Methodology FLAVOBAC nasal antiseptic formulations and FLAVOBAC oral rinse antiseptic formulations
from 1-10% concentrations were assayed for virucidal efficacy against the SARS-CoV-2 virus. SARS-CoV-2 was
exposed directly to the test compound for 60 seconds or 5 minutes. Compounds were then neutralized, and
the surviving virus was quantified.
Results All concentrations of nasal antiseptics and oral rinse antiseptics evaluated completely inactivated
the SARS-CoV-2 virus.
Conclusion Nasal and oral FLAVOBAC solutions are effective at inactivating the SARS-CoV-2 virus at a variety
of concentrations after 60-second or 5-minute exposure times. The formulations tested have the potential to
reduce the transmission of SARS-CoV-2 if used for nasal/oral decontamination, or surface decontamination
in known or suspected cases of COVID-19.
KEYWORDS
Bioflavonoid; COVID-19; Flavobac, SARS-COV-2; Virucidal Activity.
1. INTRODUCTION swabs) are highest at the time of, soon after, or
before symptoms and SARS-CoV-2 RNA are detected
The emergence of the novel human Severe Acute in saliva and throat swab specimens in recovered
patients 5 to >40 days following hospital discharge
Respiratory Syndrome CoronaVirus-2 (SARS-Cov-2)
[6]. Furthermore, live SARS-CoV-2 was isolated from
has caused drastic damage to the globe with a
throat swab specimens, indicating viral replication
dramatic loss of human life worldwide. To date
and shedding are active in tissues of the upper
(4 June 2021), approximately 172 million cases respiratory tract where SARS-CoV-2 is not thought
have been confirmed with over 3.7 million deaths to replicate [7]. SARS-CoV-2 appears to remain
according to WHO [1]. Previous studies confirmed viable while suspended in aerosols for ~3h and on
that viral loads are high in the nasal cavity, surfaces for days possibly indicating disease spread
nasopharynx, and oropharynx [2-5]. SARS-CoV-2 might occur even at considerable distances and in
viral RNA levels (measured in saliva, throat and nasal enclosed spaces with poor ventilation [8].
OPEN ACCESS This is an Open Access article under the CC BY-NC 4.0 license.
Peer-Reviewed Article
Citation: Barbour A, Darlington LG, Mendenhall M, Lerner H, Glogauer M. Efficacy of Bioflavonoids of FLAVOBAC™ Against Severe Acute Respiratory
Syndrome-Coronavirus 2 In Vitro. Stoma Edu J. 2021;8(2):95-99
Received: May 11, 2021; Revised: OJune 03, 2021 Accepted: June 08, 2021 Published: June 10, 2021
*Corresponding author: Prof. Dr. Michael Glogauer, DDS, PhD
Department of Dental Oncology, Maxillofacial and Ocular Prosthetics, Princess Margaret Cancer Centre, Toronto, ON, Canada, M5G 2M9
Tel. Fax: (905)973-0664; XYZ; e-mail: michael.glogauer@utoronto.ca
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Efficacy of FLAVOBAC™ against SARS-CoV-2
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Furthermore, among genetically related coronaviru- virucidal activity of commercially available 2-5%
Original Articles
ses, SARS-CoV-2 is predicted to have the hardest Flavobac solutions against the human novel SARS-
protective outer shell against degradative enzymes CoV-2 strain SARS-CoV-2, USA-WA1/2020. We report
thus contributing to its high resilience in saliva, here the first anti-SARS-CoV-2 evaluation of a na-
other body fluids, and outside the body [9]. Despite sal and oral rinse antiseptic containing Flavobac
many clinical trials that have been conducted for which has been developed specifically for routine
the treatment of COVID-19, no antiviral has been intranasal or oral use.
verified to be effective for COVID-19. Conventional
antiviral drugs including ribavirin and favipiravir and 2. METHODS
other anti-inflammatory agents are currently used
in clinical settings against the severe cases of SARS-
2.1. Virus culture and biosafety and test compounds
CoV-2 infections [10]. On the other hand, increased
interests in plant-based natural products belonging SARS-CoV-2, USA-WA1/2020 strain obtained from
to the flavonoids class have emerged as an attractive the World Reference Center for Emerging Viruses
option of treatment. The low cytotoxicity and and Arboviruses (WRCEVA), was used in this study
synergy with other effective drugs make flavonoids for the virucidal activity of Flavobac. The virus
an ideal candidate to interfere with the life cycle of stock was prepared by passaging three times in
the virus. Several flavonoids have been shown to Vero 76 (ATCC, CRL-1587) cells. The media was
exhibit significant antiviral properties in in vitro and MEM supplemented with 2% fetal bovine serum
in vivo studies [11-13]. Bioflavonoids are naturally (FBS, Cytvia) and 50 μg/mL gentamicin (Sigma).
present in plants, fruit and vegetables, there are over Viral cultures were carried out in a biosafety level
6000 identified having a wide range of uses including 3 (BSL-3) following standard operating procedures
antioxidants & food ingredients. Flavonoids com- approved by the USU Biohazards Committee,
prise a group of naturally occurring compounds Institute for Antiviral Research, Utah State University,
that are among the most ubiquitous in the plant USA. Nasal antiseptic solutions and oral rinse
kingdom [14]. They are found in every family and antiseptic solutions consisting of aqueous Flavobac
nearly every species of the higher plants and they BCL concentrate as the sole active ingredient and
have extensive biological properties that promote OSI-20210203 oropharyngeal spray solution
human health and help reduce the risk of diseases. consisting of aqueous Flavobac 2% (A) and 5% (B)
Bioflavonoids have demonstrated their capacity to and other natural ingredients were supplied by Oral
act against bacteria, fungi, and viruses [12,15,16]. Science International (Montreal, Canada).
Flavobac (Trademark of Citrox Bioscience Ltd) is a
natural product extracted from bitter oranges and
2.2. Virucidal Assay
composed of soluble bioflavonoids and hydroxylated
phenolic structures. Flavobac is developed as nasal Flavobac BCL concentrate was diluted to 10%, 5%,
and oral rinse antiseptic formulations and besides 2%, or 1% in the test media and OSI-20210203
its potent antibacterial activity against a tandem samples were tested at full strength. Prepared test
array of bacterial pathogens [15], it showed to have compounds were mixed with the virus stock solution
a strong virucidal efficacy against many viruses in (approximately 5.5 log10 CCID50 per 0.1 mL) at a
vitro (unpublished data). volume ratio of 9:1 (v/v). Each concentration was
In the current study, we hypothesized that tested in triplicate. The Test media was added to
bioflavonoids as active ingredients in the Flavobac one tube of each prepared concentration to serve
may have virucidal activities against SARS-CoV-2 as toxicity controls. Water was tested in parallel as a
which may enable a new application for protection negative control. The prepared test compound and
against COVID-19. We report for the first time the the virus solution mixtures were incubated at room
Table 1. Virucidal efficacy against SARS-CoV-2 after contact with the virus at 22 ± 2°C.
Compound Contact Time Cytotoxcicity1 Neut. Virus Virus LRV4
Ctrl.2 Titer3 Titer3
FLAVOBAC BCL 10% 1 min 1/100 None <2.7 4.6 >1.9
FLAVOBAC BCL 5% 1 min 1/100 None <2.7 4.6 >1.9
FLAVOBAC BCL 2% 1 min 1/10n None <1.7 14.6 >2.9
FLAVOBAC BCL 1% 1 min 1/10 None <1.7 4.6 >2.9
OSI-20210203A 5 min 1/10 None <1.7 4.7 > 3.0
OSI-20210203B 5 min 1/10 None <1.7 4.7 > 3.0
1
Cytotoxicity indicates the highest dilution of the endpoint titer where full (80-100%) cytotoxicity was observed.
2
Neutralization control indicates the highest dilution of the endpoint titer where compound inhibited virus CPE in the wells after neutralization
3
Virus titers of the test sample or virus control (VC) in log10 CCID50 of virus per 0.1 ml
4
LRV (log reduction value) is the reduction of virus in the test sample compared to the virus control.
96 Stoma Edu J. 2021;8(2): 95-99 pISSN 2360-2406; eISSN 2502-0285
Abdelahhad Barbour, et all
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temperature (22 ± 2°C) for 1 or 5 minutes as indicated spread especially in high-risk disease transmission
Original Articles
in Tab. 1. The assay was neutralized by a 1/10 settings e.g., hospitals, long-term care facilities, and
dilution in MEM 2% FBS, 50 μg/mL gentamicin. For vulnerable populations. One viable approach is to
quantification, the surviving virus from each sample reduce viral loads in the oral and nasal cavities, which
was quantified by standard end-point dilution assay. can be achieved by locally neutralizing viruses that
Briefly, the neutralized samples were pooled and have entered these cavities with over-the-counter
serially diluted using eight log10 dilutions in a test oral and/or nasal sprays with virucidal properties. In
medium. Then 100 μL of each dilution was plated our current study, Flavobac based products exhibited
into quadruplicate wells of 96-well plates containing
excellent virucidal activities towards SARS-CoV-2
80-90% confluent Vero E6 cells (ATCC CRL-1586). The
when tested in vitro. These products can be used
toxicity controls were added to an additional 4 wells
as supplementary preventative measures to reduce
of Vero E6 cells and 2 of those wells at each dilution
were infected with the virus to serve as neutralization exposure to infectious droplets, thus potentially
controls, ensuring that residual sample in the titer reducing the person-to-person transmission risk in
assay plate did not inhibit growth and detection of close contact situations. Nasal and oral antisepsis
the surviving virus. Plates were incubated at 37 ± 2°C has been recommended as part of a comprehensive
with 5% CO2 for 5 days. Each well was then scored plan to reduce the likelihood of virus transmission
for the presence or absence of an infectious virus. by reducing the number of active aerosolized virus
The titers were determined using the Reed-Muench particles from the nasal passages and oral cavity
(1948) equation [17] and the log reduction value [9,18,19].
(LRV) of each compound compared to the negative The American Dental Association and the Center for
(water) control was calculated. Disease Control and Prevention (CDC) guidelines
for minimizing the risk of COVID-19 transmission
3. RESULTS advise the use of effective mouthwash before all
procedures [20]. Bioflavonoid-based products like
Flavobac BCL aqueous solution showed to have Flavobac are known to be rich in plant polyphenols
potent antiviral activities by reducing SARS-CoV-2 which have been shown to have good antiviral
viral titer below the limit of detection (LoD) at all (including SARS-CoV-2), antioxidant, antibacterial
concentrations tested in vitro. We have tested various
and anti-inflammatory properties [21]. A recent
concentrations to ensure that we identify the optimal
study has suggested that the anti-SARS-CoV-2
concentration of Flavobac BCL against SARS-COV-2.
activities of plant-derived natural polyphenols can
Flavobac BCL is a key ingredient of the formulation
OSI-20210203. The latter is the commercialized be mediated by RNA dependent RNA polymerase
product (Cold & Flu Guard). Because of differences (RdRp) inhibition which may represent an effective
in cytotoxicity, the lower concentrations had higher therapy for SARS-CoV-2 infections [22]. In a sepa-
LRV values with LRV>2.9 at 2% and 1% and LRV>1.9 rated study, Jo et al found that many flavonoids
at 5% and 10%, respectively (Table 1). Furthermore, were able to block the proteolytic activity of SARS-
Virus titers and LRV of SARS-CoV-2 after incubation CoV-2 3CLpro, an essential enzyme controlling the
with Flavobac commercial solutions OSI-20210203A virus replication life cycle [23]. Since Flavobac is a
and OSI-20210203B reduced the virus below the limit mixture of plant-based bioflavonoids, it is believed
of detection (LRV>3.0). Each Flavobac containing to exhibit similar modes of action towards SARS-
solution evaluated was effective at reducing >3 log10 CoV-2. Hence, scientists are recommending the use
CCID50 infectious virus, from 4.7 log10 CCID50/0.1 mL of such products to reduce the spread of SARS-Cov-2
to <1.7 log10 CCID50/0.1 mL. A consistent reduction [24] while we wait for a broad immunity conferred by
in virus titre was observed for SARS-CoV-2 viruses at the new vaccines.
all concentrations of Flavobac solution tested and The limitation of the current study is the lack of key
with a contact time of 1 or 5 minutes. The reductions information on whether the tested product can
in virus titre were >1.9 log10 CCID50/mL for Flavobac work in an actual in vivo environment and exhibit
5 and 10%, equating to >98.7% reduction; >2.9
the same virucidal activities when used by human
log10 CCID50/mL for Flavobac 1 and 2%, equating
consumers as a nasal spray. Further research is
to >99.8% reduction; and >3.0 Log10 CCID50/mL,
required by testing Flavobac in clinical trials to assess
equating to >99.9% reduction for OSI-202103, the
commercial formulation of Flavobac. its biological activities in preventing the spread
of the virus, As the world is now inching towards
4. DISCUSSION gradually returning routine societal and economic
activities to pre-pandemic level, the heightened
In this era of emerging infectious diseases caused fear of a post-pandemic outbreak looms as the virus
by respiratory tract viruses especially SARS-Cov-2, still lurks and relatively little is known about the key
finding new alternative biomedical tools based parameters that could shape the future course of the
on natural products is important to suppress viral pandemic [25].
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The challenge in nasal antisepsis is to find effective CONFLICT OF INTEREST
Original Articles topical preparations which are safe to use. Oral and Dr. Glogauer is the Chief Scientific Officer for Oral Sciences. Oral
nasal solutions infused with Flavobac, a natural Sciences is the developer of this rinse product. The rest of the
bioflavonoid complex, with broad virucidal efficacy, authors declare no conflict of interest. Dr. Glogauer is the Chief
has demonstrated efficacy to kill 99.9% of SARS- Scientific Officer for Oral Sciences. Oral Sciences is the developer
CoV-2 and it may provide a safe and protective of this rinse product. The rest of the authors declare no conflict
solution for people within viruses-aerosolized places of interest.
like workplaces, gym, restaurant, schools or even for
people who are at a higher risk of respiratory viral ACKNOWLEDGMENTS
complications due to other health complications None.
5. CONCLUSION AUTHOR CONTRIBUTIONS
AB, MG contributed to the concept, design, and data analysis
Current public health recommendations emphasize of the study and wrote the manuscript. MM performed the
the need to break the person-to-person viral experiments. GD, HL contributed to the data analysis and edited
transmission primarily through social separation, the manuscript.
hand hygiene and surface disinfection. Flavobac
deactivated SARS-CoV-2 virus tested from 98.8% FUNDING
to > 99.9% when incubated with the virus for 1 to Oral Science International funded this study.
5 minutes at 22°C. The results indicate that Flavobac
oral and nasal spray could potentially be used to COMPETING INTERESTS
neutralize SARS-CoV-2 and reduce viral transmission. The authors declare that they have no competing interests.
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Abdelahhad BARBOUR
MSc, PhD, Postdoctoral Fellow
Faculty of Dentistry
University of Toronto
Toronto, ON, Canada
CV
Dr. Abdelahhad Barbour is a Postdoctoral scientist and research coordinator of the COVID-19 saliva testing project at the
Faculty of Dentistry, University of Toronto. The project aims to document rates of COVID-19 infection and immune responses to
vaccination among trainees, faculty, and staff in Canadian dental schools. Dr. Barbour obtained his PhD in Molecular Microbiology
from the University of Malaya, Malaysia with a thesis entitled “Characterisation and mechanism of action of lantibiotics produced
by Streptococcus salivarius”. He is an expert in the fields of antimicrobial peptides, microbial genomics, oral microbiome and
probiotics developments. Areas of interest in the research activity: Host-microbiome interactions, neutrophils-pathogens
signaling, COVID-19 saliva testing, antibiotic resistance, microbial genomics.
Questions
1. What are bioflavonoids?
qa. Synthetic substance;
qb. Natural products derived from animal origin;
qc. Natural products derived from fruits and vegetables;
qd. Antibiotics produced by soil microorganisms.
2. What are the biological activities of bioflavonoids?
qa. Antimicrobial;
qb. Antiviral;
qc. Antifungal;
qd. ll mentioned above.
3. What is the main composition of FLAVOBAC™?
qa. Soluble bioflavonoids and hydroxylated phenolic structures;
qb. Antimicrobial peptides;
qc. Polysaccharides;
qd. Lipids.
4. FLAVOBAC™ deactivated the SARS-CoV-2 virus at the following levels:
qa. 10-20%;
qb. Less than 50%;
qc. Less than 80%;
qd. More than 95%.
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