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\begin{document}

\title{Salivary detection of SARS-CoV-2 (COVID-19) and implications for oral
healthcare providers}



\author[1]{Mark S. Chambers, DMD, MS}%
\affil[1]{The University of Texas MD Anderson Cancer Center,}%


\vspace{-1em}



  
  \date{May 17, 2024}


\begingroup
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\selectlanguage{english}
\begin{abstract}
The coronavirus disease 2019 (COVID-19) pandemic has become a major
public health crisis. The diagnostic and containment efforts for the
disease have presented significant challenges for the global healthcare
community. In this brief report, we provide perspective on the potential
use of salivary specimens for detection and serial monitoring of severe
acute respiratory syndrome coronavirus 2 (SARS-CoV-2), based on current
literature. Oral healthcare providers are at an elevated risk of
exposure to COVID-19 due to their proximity to nasopharynx of patients,
and the practice involving the use of aerosol-generating equipment. Here
we summarize the general guidelines for oral healthcare specialists for
prevention of nosocomial transmission of COVID-19, and provide specific
recommendations for clinical care management.%
\end{abstract}%



\sloppy


\subsection*{\texorpdfstring{Nimit Bajaj, BDS, MPH,\textsuperscript{1}
Bruno P. Granwehr, MD, MS,\textsuperscript{2} Ehab Y. Hanna,
MD,\textsuperscript{3} Mark S. Chambers, DMD,
MS\textsuperscript{3}}{Nimit Bajaj, BDS, MPH,1 Bruno P. Granwehr, MD, MS,2 Ehab Y. Hanna, MD,3 Mark S. Chambers, DMD, MS3}}

{\label{939559}}

~

\textsuperscript{1}Department of Radiation Oncology, The University of
Texas MD Anderson Cancer Center, Houston, Texas

\textsuperscript{2}Department of Infectious Diseases, The University of
Texas MD Anderson Cancer Center, Houston, Texas

\textsuperscript{3}Department of Head and Neck Surgery, The University
of Texas MD Anderson Cancer Center, Houston, Texas

\textbf{~}

\textbf{Corresponding Author:}

Dr. Mark S. Chambers, Department of Head and Neck Surgery, The
University of Texas MD Anderson Cancer Center, 1515 Holcombe Boulevard,
Unit 1445, Houston, TX 77030 USA. Telephone: (713) 745-2672

Email address: mchamber@mdanderson.org

\textbf{Running title:} Diagnostic potential of saliva for COVID-19 and
implications for oral healthcare specialists

\textbf{Keywords:} COVID-19, SARS-CoV-2, saliva, nosocomial infection,
head and neck

\textbf{Acknowledgment:} The authors would like to thank Sarah Bronson,
Department of Scientific Publications at MD Anderson Research Medical
Library, for help in editing of this article.

\textbf{~}

\textbf{Abstract}

The coronavirus disease 2019 (COVID-19) pandemic has become a major
public health crisis. The diagnostic and containment efforts for the
disease have presented significant challenges for the global healthcare
community. In this brief report, we provide perspective on the potential
use of salivary specimens for detection and serial monitoring of severe
acute respiratory syndrome coronavirus 2 (SARS-CoV-2), based on current
literature. Oral healthcare providers are at an elevated risk of
exposure to COVID-19 due to their proximity to nasopharynx of patients,
and the practice involving the use of aerosol-generating equipment. Here
we summarize the general guidelines for oral healthcare specialists for
prevention of nosocomial transmission of COVID-19, and provide specific
recommendations for clinical care management.\textbf{{}}

\par\null

\textbf{Introduction}

An outbreak of pneumonia of unknown etiology was detected in Wuhan,
Hubei Province of China, in late December,
2019.\textsuperscript{1,2}Since then, the disease has rapidly spread
around the globe. The causative agent of the disease was identified to
be a novel coronavirus of bat origin,\textsuperscript{3} later termed
severe acute respiratory syndrome coronavirus 2
(SARS-CoV-2),\textsuperscript{4} and the disease was named coronavirus
disease 2019 (COVID-19).\textsuperscript{5} The World Health
Organization (WHO) designated the COVID-19 outbreak as a pandemic on
March 11, 2020.\textsuperscript{6} As of May 19, 2020, there have been
over 4,731,458 laboratory confirmed cases and 316,169 deaths reported
globally. In the United States alone, more than 1,477,516 COVID-19 cases
and 89,272 deaths have been reported, and the numbers continue to
rise.\textsuperscript{7,8}

Many patients infected with SARS-CoV-2 are asymptomatic, however the
most common symptoms at the onset of illness are fever, cough, dyspnea,
and myalgia.\textsuperscript{9,10} Some patients may also experience
headache, dizziness, loss of taste and/or smell,\textsuperscript{11} and
gastrointestinal symptoms such as nausea, vomiting and
diarrhea.\textsuperscript{10,12} Chest computed tomography (CT) findings
of COVID-19 patients show multifocal bilateral ground-glass opacities
and areas of consolidation.\textsuperscript{10,13} Severe-onset disease
may lead to acute respiratory distress syndrome and
death.\textsuperscript{12} SARS-CoV-2 is thought to spread primarily
through respiratory droplets and from close person-to-person contact
with an infected individual.\textsuperscript{14} The virus has also been
shown to survive on surfaces such as plastic and stainless steel for up
to 72 hours.\textsuperscript{15} Currently, the recommended mode of
diagnostic specimen collection is from the upper respiratory tract using
nasopharyngeal and oropharyngeal swabs. However, this requires close
contact between the healthcare worker and individual, and may induce
sneezing and coughing which can lead to aerosol generation, and cause
transmission of the virus. This method of sample collection may also
cause discomfort and bleeding in some people.\textsuperscript{16} In
addition, there is an acute shortage of swabs and protective gear, and
an overburdening of the testing centers. Thus, there is a need to
explore other evidence based modalities of specimen collection for mass
testing and monitoring of COVID-19.

\textbf{Diagnostic potential of saliva for SARS-CoV-2}

It has been reported that the angiotensin converting enzyme II (ACE2) is
the host cell receptor to which the SARS-CoV-2 binds to gain entry into
cells, same as SARS-CoV.\textsuperscript{9,17} Xu et al have
demonstrated that the receptor binding domain of SARS-CoV-2 spike
protein supports strong interactions with the human ACE2
receptor.\textsuperscript{18} The ACE2 protein is present in most organs
of the human body, and is abundantly expressed in the vascular
endothelial cells, heart, alveolar epithelial cells of lungs and
enterocytes of the intestine.\textsuperscript{19} These findings
indicate that these organs may potentially be at high risk for COVID-19
infection.\textsuperscript{20} Recently, RNA sequencing studies from The
Cancer Genome Atlas database have identified that there is a high
expression of the ACE2 receptors on the epithelial cells of oral
mucosa.\textsuperscript{21} Among oral sites, the highest expression was
seen in the epithelial cells of tongue, followed by buccal and gingival
tissues. These findings may provide clues for further investigation of
oral routes of infection, pathogenesis and detection of COVID-19.

Previous studies have demonstrated that salivary specimens have a higher
than 90\% concordance rate with nasopharyngeal specimens in the
detection of respiratory viruses.\textsuperscript{22} In an initial
pilot study by To et al.,\textsuperscript{23} SARS-CoV-2 was detected in
the salivary specimens of 11 out of 12 patients with
laboratory-confirmed COVID-19, and all 33 individuals who tested
negative for nasopharyngeal specimens also tested negative for salivary
specimens. In another recently published study, posterior oropharyngeal
saliva samples were collected for 23 patients with laboratory-confirmed
COVID-19 for nasopharyngeal specimens.\textsuperscript{24} Of these, 20
patients (87\%) tested positive for SARS-CoV-2 in their saliva. Serial
viral load was ascertained using reverse transcriptase quantitative
polymerase chain reaction (RT-qPCR). It was found that the salivary
viral load was highest during the first week after symptom onset and it
declined over time. The salivary sample was self-collected by patients
by coughing up saliva from the posterior oropharynx. Therefore it is
possible that these specimens included secretions from the nasopharynx
or the lower respiratory tract, rather than being completely salivary.
In a study by Williams et al.,\textsuperscript{25} 622 individuals were
tested for COVID-19 using nasopharyngeal specimens, of which 522 also
provided salivary specimens. For salivary specimen collection, they were
instructed to pool saliva in their mouth for 1-2 minutes, and gently
spit into a collection pot. 33 of the 39 patients (84.6\%) who tested
positive for nasopharyngeal specimens, also had SARS-CoV-2 detected in
their saliva.\textsuperscript{25} A study of 44 COVID-19 inpatients
noted a high correlation between nasopharyngeal and salivary samples,
with higher viral titers in saliva.\textsuperscript{26} It was found
that the salivary specimens yielded higher detection sensitivity and
consistency throughout the course of disease. This study also enrolled
98 asymptomatic healthcare workers, who self-collected nasopharyngeal
and salivary specimens every three days for a period of two weeks.
SARS-CoV-2 was detected in saliva from two healthcare workers who tested
negative for matching nasopharyngeal samples.\textsuperscript{26} These
data, although limited, suggest that saliva may be more sensitive in
detection of asymptomatic or pre-symptomatic infections.

Researchers from Rutgers University evaluated the use of salivary
specimens for SARS-CoV-2 detection in symptomatic patients from three
ambulatory care centers.\textsuperscript{27} They found 100\% positive
and negative concordance between results obtained from testing of saliva
and those obtained from nasopharyngeal and oropharyngeal swabs {[}saliva
vs nasopharyngeal swab: (26/26) positive agreement, (27/27) negative
agreement; saliva vs oropharyngeal swab: (4/4) positive agreement, (3/3)
negative agreement{]}. The U.S. Food and Drug Administration (FDA) has
since issued them an emergency use authorization for the use of salivary
specimens, in addition to the nasopharyngeal and oropharyngeal swabs,
for detection of SARS-CoV-2 RNA in individuals suspected of
COVID-19.\textsuperscript{27} A salivary diagnostic test would allow for
a noninvasive self-administered sample collection under healthcare
providers' directive for individuals in quarantine, and would circumvent
the issues regarding global shortage of swabs and personal protective
equipment (PPE) needed for conventional COVID-19 testing. Specific
guidelines are needed to standardize the method for collection of
salivary specimens, and implement the use of appropriate assays, and
processing methods. The presence of SARS-CoV-2 in the saliva of infected
patients also bears implications for a high potential of transmission in
the dental operatory, and underscores the need for awareness and use of
effective PPE practices.

\textbf{Implications for oral healthcare providers}

Healthcare workers such as physicians, nurses, respiratory therapists,
dentists, oral healthcare specialists, speech pathologists,
ophthalmologists, and otolaryngologists are at an elevated risk of
exposure to COVID-19. Oral healthcare providers (OHCP) are at a high
risk in particular for nosocomial transmission of respiratory infectious
diseases owing to their proximity to the nasopharynx and oral cavity of
patients. The general consensus in dental medicine is that the greatest
threat of airborne infection is from aerosols (particles smaller than
50\selectlanguage{greek}µ\selectlanguage{english}m in diameter) due to their ability to stay suspended in the air and
contaminate the mucous membranes of the mouth and respiratory
passages.\textsuperscript{28,29} Fine aerosols of usually 0.5 to 10 \selectlanguage{greek}µ\selectlanguage{english}m
in diameter have an even higher potential for transmitting infections.
The practice of dental treatment involves the use of surgical and dental
equipment, such as aerosol-generating ultrasonic scalers, air-water
syringes and handpieces. These instruments create a visible spray of
water droplets, salivary spatter, debris, blood and microorganisms, and
have the potential to spread nosocomial infections such as tuberculosis
and SARS in the exam rooms.\textsuperscript{28-30}

Currently there are no data available to assess the risk of transmission
of SARS-CoV-2 in the office settings of dental and specialty practices;
however, the Occupational Safety and Health Administration (OSHA) has
categorized oral healthcare providers under the ``very high exposure
risk'' category for SARS-CoV-2.\textsuperscript{31} OSHA has also
recommended the use of powered air-purifying respirators (PAPRs) or
supplied air respirators (SARs) for procedures involving aerosol
generation. The Centers for Disease Control and Prevention (CDC) has
laid out interim infection control guidance for dental
settings,\textsuperscript{14} which includes postponement of all
elective procedures, surgeries, and non-urgent visits. These guidelines
advise the use of highest level of PPE available, such as a gown,
gloves, eye protective gear (goggles or face shields that cover the
front and sides of the face), and N95 or higher-level respirator during
emergency procedures.

The CDC and the American Dental Association (ADA) have recommended that
all dentists and oral specialists keep their offices closed and postpone
all elective procedures except for urgent and emergency care
particularly those in hospital-based practices, although new guidelines
are expected for non-urgent care.\textsuperscript{32} They have put
forth interim guidelines for triaging patients for emergency procedures.
The ADA has highlighted special considerations for clinical procedures,
such as the use of extraoral radiographs, including panoramic
radiographs and cone beam CT over intraoral radiographs, minimizing the
use of aerosol-generating instruments and prioritizing the use of hand
instruments, using rubber dams and high-volume saliva evacuators, and
placing resorbable sutures to eliminate the need for follow-up
appointments.\textsuperscript{32} Likewise, the American Association of
Oral and Maxillofacial Surgeons (AAOMS) has recommended that non-aerosol
generating procedures and emergent treatments such as antibiotic therapy
should be handled in a manner that is as minimally invasive as possible,
with the use of adequate PPE.\textsuperscript{33} Previous studies have
investigated the virucidal efficacy of pre-procedural mouthrinse such as
0.23\% povidone iodine and 1\% hydrogen peroxide, and found them to be
highly effective against viruses, including
SARS-CoV.\textsuperscript{34,35} Currently there are no clinical studies
supporting the use of such agents against SARS-CoV-2. However due to its
vulnerability to oxidation, topical mouthrinse containing oxidative
agents such as povidone iodine may be effective in reducing the salivary
viral load of SARS-CoV-2.\textsuperscript{30}

Special considerations are needed for oral and maxillofacial specialists
working in an oncology practice. Initial screening of patients should be
conducted via telemedicine consults, and short-term deferment should be
considered. Patients who report a recent travel history to any of the
designated COVID-19 hotspots, and the presence of any symptoms of
respiratory illness should be instructed to self-quarantine for 14 days
and report to their physician for COVID-19 testing. Cancer patients are
considered as highly vulnerable to COVID-19 due to their
immunocompromised status. The MD Anderson head and neck surgery
consortium has devised guidelines for triaging patients based on
site-specific head and neck cancers.\textsuperscript{36} All elective
oral surgical procedures should be deferred, however procedures such as
planned dental extractions, surgery for patients with early and
intermediate malignant disease, and fabrication of oral stents for
radiation therapy are to continue. The management of these patients
requires a needs assessment on a case-by-case basis with patient's
primary oncologist, and the interdisciplinary team; and more in depth
considerations are beyond the scope and purpose of this report.

Due to the disruption of all major supply chains and increasing global
demands, there is a critical shortage of PPE for healthcare personnel.
Such an unprecedented situation demands for innovative ideas to address
these concerns. Many academic institutions, researchers and private
organizations have come up with creative solutions such as open-source
designs for 3D-printed respirators and face
shields.\textsuperscript{37,38} Customized face shields allow for a more
secure fit of the headband, and longer shields are suitable for
protection from splatter during dental and surgical procedures. COVID-19
is now a widespread and constant presence in our community. As we adapt
to this rapidly evolving situation and make adjustments based on new
information, revised guidelines from the regulatory authorities will be
critical in ensuring the safe reopening of oral healthcare operations.
Development and implementation of a rapid COVID-19 diagnostic test at
the point-of-care will be vital in safeguarding the health of both
patients and OHCP, and minimizing the burden of disease in our
community. The American Medical Association (AMA) as of May 1, 2020
stated ``as public health experts determine that it is safe to see
patients and stay-at-home restrictions are relaxed, physician practices
should strategically plan when and how best to reopen.'' In parallel,
the Centers for Medicare and Medicaid Services (CMS) published a Phase 1
guide for reopening facilities to provide non-emergent, non-COVID care.
The AMA and CMS guidance include pre-visit screening template and
checklists of criteria for reopening private and hospital-based
practices.\textsuperscript{39,40}

\textbf{Conclusions}

Saliva may be a viable alternative to nasopharyngeal specimen collection
for COVID-19 testing. Further studies are needed to investigate the
efficacy, feasibility and scalability of using salivary specimens for
SARS-CoV-2 detection and surveillance on a nationwide basis. It is
imperative that OHCP stay abreast of the latest developments surrounding
the pandemic, follow guidelines from the CDC, ADA, the federal and state
governments, and make informed decisions regarding clinical care.
Telemedicine efforts can be an excellent adjunct in triaging patients
and determining urgency of need.

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