\documentclass[10pt]{article}

\usepackage{fullpage}
\usepackage{setspace}
\usepackage{parskip}
\usepackage{titlesec}
\usepackage[section]{placeins}
\usepackage{xcolor}
\usepackage{breakcites}
\usepackage{lineno}
\usepackage{hyphenat}





\PassOptionsToPackage{hyphens}{url}
\usepackage[colorlinks = true,
            linkcolor = blue,
            urlcolor  = blue,
            citecolor = blue,
            anchorcolor = blue]{hyperref}
\usepackage{etoolbox}
\makeatletter
\patchcmd\@combinedblfloats{\box\@outputbox}{\unvbox\@outputbox}{}{%
  \errmessage{\noexpand\@combinedblfloats could not be patched}%
}%
\makeatother


\usepackage{natbib}




\renewenvironment{abstract}
  {{\bfseries\noindent{\abstractname}\par\nobreak}\footnotesize}
  {\bigskip}

\titlespacing{\section}{0pt}{*3}{*1}
\titlespacing{\subsection}{0pt}{*2}{*0.5}
\titlespacing{\subsubsection}{0pt}{*1.5}{0pt}


\usepackage{authblk}


\usepackage{graphicx}
\usepackage[space]{grffile}
\usepackage{latexsym}
\usepackage{textcomp}
\usepackage{longtable}
\usepackage{tabulary}
\usepackage{booktabs,array,multirow}
\usepackage{amsfonts,amsmath,amssymb}
\providecommand\citet{\cite}
\providecommand\citep{\cite}
\providecommand\citealt{\cite}
% You can conditionalize code for latexml or normal latex using this.
\newif\iflatexml\latexmlfalse
\providecommand{\tightlist}{\setlength{\itemsep}{0pt}\setlength{\parskip}{0pt}}%

\AtBeginDocument{\DeclareGraphicsExtensions{.pdf,.PDF,.eps,.EPS,.png,.PNG,.tif,.TIF,.jpg,.JPG,.jpeg,.JPEG}}

\usepackage[utf8]{inputenc}
\usepackage[english]{babel}



\usepackage{float}








\begin{document}

\title{Severe oropharyngeal dysphagia following COVID-19: a case report}



\author[1]{Giulia De Vincentis}%
\author[1]{Chiara Ferrari}%
\author[1]{Dario Guerini Rocco}%
\affil[1]{ASST Bergamo Est}%


\vspace{-1em}



  
  \date{May 26, 2024}


\begingroup
\let\center\flushleft
\let\endcenter\endflushleft
\maketitle
\endgroup





\selectlanguage{english}
\begin{abstract}
This case report describes the clinical history of a COVID-19 patient
with a non-immediate diagnosis of severe dysphagia that required a
gastrostomy positioning. A vocal folds paresis was observed for the
first time in the course of a Sars-CoV-2 infection. Thanks to intensive
rehabilitation treatment, the outcome was favourable.%
\end{abstract}%



\sloppy


\textbf{Severe oropharyngeal dysphagia following COVID-19: a case
report}

Giulia De Vincentis\textsuperscript{1}*, Chiara
Ferrari\textsuperscript{1}, Dario Guerini Rocco\textsuperscript{1}

\textsuperscript{1} Rehabilitation Unit, ASST Bergamo Est, Briolini
Hospital, Gazzaniga, Bergamo, Italy

*Corresponding author: Giulia De Vincentis, Rehabilitation Unit, ASST
Bergamo Est, Briolini Hospital, Via Manzoni 130, 24025, Gazzaniga,
Bergamo, Italy. E-mail: giulia.devincentis@asst-bergamoest.it

\textbf{ABSTRACT}

This case report describes the clinical history of a COVID-19 patient
with a non-immediate diagnosis of severe dysphagia that required a
gastrostomy positioning. A vocal folds paresis was observed for the
first time in the course of a Sars-CoV-2 infection. Thanks to intensive
rehabilitation treatment, the outcome was favourable.

\textbf{KEY CLINICAL MESSAGE}

Dysphagia may occur after a prolonged intubation due to Covid-19 but it
is usually mild. Case reports on severe dysphagia following Covid-19 are
infrequent. Diagnosis can be difficult because international indications
recommend avoiding instrumental assessments as far as possible because
of the infection risk. An early rehabilitation treatment is recommended.

\textbf{Key words}

COVID-19, swallowing disorders, dysphagia rehabilitation, vocal fold
paresis, case report.

\textbf{Introduction}

Many patients who underwent prolonged intubation {[}1{]} develop
dysphagia after extubation, with an occurrence varying between 3\% and
62\%. The prevalence of swallowing disorders increases as the intubation
period is extended {[}2{]}. Dysphagia predisposes to prolonged
hospitalizations and to a worse prognosis due to the high risk of
complications such as aspiration pneumonia, malnutrition and
dehydration. The origin of post-intubation dysphagia derives from
several factors: the endotracheal tube can cause trauma at pharynx or
larynx {[}1{]} and can generate muscle atrophy due to disuse, aggravated
by long sedation and the use of neuromuscular blockers. Such disuse of
the swallowing mechanism may diminish its cortical representation and
delay functional recovery in the long term. To these factors can be
added changes in sensitivity, gastroesophageal reflux and
breath-swallowing incoordination {[}3{]}. Recovery after post-intubation
dysphagia is usually possible in a short period of time {[}2{]}. In
patients with Acute Respiratory Distress Syndrome (ARDS), however,
swallowing improvement appears slower, even longer than 6 months. The
reason may lie in the severity of the pathology that often requires
prolonged mechanical ventilation and long stays in intensive care unit.

A recent case-control study compared the trend of swallowing disorders
after endotracheal tube removal in 101 Covid-19 patients and in 150
non-Covid-19 patients undergoing prolonged intubation. Although Covid-19
patients were intubated longer, they showed less swallowing disorders
after extubation and required fewer re-education sessions {[}4{]}.
However, there is no data about the incidence of dysphagia in these
patients also owing to the reduction of diagnostic procedures such as
Fiberoptic Endoscopic Evaluation of Swallowing (FEES) during Covid-19
pandemic because of the aerosol generating risk {[}5{]}. In May 2020 the
first case report on oropharyngeal dysphagia associated with Sars-CoV-2
was published: the patient, a 70-year-old man, after an 11-day
intubation developed dysphagia and a subsequent aspiration pneumonia.
The instrumental evaluations evidenced bilateral absent GAG reflex,
pyriform and vallecular salivary stagnation and silent aspiration. The
patient received rehabilitative treatment with noticeable improvement of
symptoms, without the need for nasogastric tube or Percutaneous
Endoscopic Gastrostomy (PEG) positioning. The authors hypothesized the
presence of a glossofaringeal and vagal neuropathy underlying the
development of dysphagia {[}6{]}. Another newest Italian case report
highlighted the possible involvement of the cranial nerves in dysphagia
development during Covid-19 {[}7{]}.

The purpose of the present case report is to describe the clinical
history and the rehabilitation of a patient coming from Bergamo, Italy.
Patient's informed consent was obtained for data treatment.

\textbf{Case presentation}

This patient, a 66-year-old man, developed a severe dysphagia of not
immediate diagnosis during hospitalization for Covid-19. He suffered
from diabetes mellitus for about 10 years and chronic obstructive
pulmonary disease (COPD). His drug therapy only consisted of metformin.
He has never been hospitalized before. He accessed the Emergency Room on
9\textsuperscript{th} March 2020 due to persistent fever for several
weeks and worsening dyspnea. Nasopharyngeal swab for the detection of
Sars-CoV-2 was positive. Chest computed tomography (CT) scan showed
extensive inflammatory areas with ground-glass opacities. Due to
worsening respiratory pattern, the patient was placed on Continuous
Positive Airway Pressure (CPAP) and started therapy with antibiotics,
antivirals and hydroxychloroquine. In the following days, despite the
use of CPAP, the clinical picture worsened up to ARDS and required
tracheal intubation (on 12\textsuperscript{th} March). On
24\textsuperscript{th} March tracheotomy tube was placed. In the
following weeks there was a slow but progressive improvement in
respiratory exchanges that allowed a gradual weaning from the
ventilator. At the end of April, a neurological evaluation was required
due to loss of strength affecting the left lower limb. Brain CT showed
no acute lesions. Because of abundant secretions in the airways,
tracheal tube was not removed. Initial assessment of swallowing (nursing
screening with Evan's Blue dye test) performed at the beginning of May
did not detect signs or symptoms of dysphagia, so parenteral nutrition
was stopped and the patient started eating with modified diet and
thickened liquids (honey-thick and spoon-thick). The texture of food was
gradually modified from pureed diet to solid food. At the beginning of
May nasopharyngeal swabs for detecting Sars-CoV-2 were negative and on
22\textsuperscript{th} May the patient moved from the acute care
hospital to the Rehabilitation Unit.

\textbf{Differential diagnosis, investigations and treatment}

In the new hospital ward nursing screening test for dysphagia and
specific evaluation of swallowing performed by speech and language
pathologist (SLP) were carried out, as it is usually performed on
tracheotomy patients at the beginning of the recovery. The tracheotomy
tube was in place, the patient breathed in ambient air, using
fenestrated inner cannula with decannulation plug. Evaluation of
secretion management, Evan's Blue dye test, test with gel-water and
methylene blue were negative. For preventive purposes, however, a pureed
diet was recommended. In addition, evaluation during lunch was performed
in order to detect any signs or symptoms of dysphagia: at the end of the
meal, some traces of bolus in the aspirate were found in association to
wet voice. That same evening, while taking dinner with pureed diet under
supervision, the presence of food material in the tracheal tube without
reflex cough and desaturation (pulse oximeter readings from 99\% to
94\%) were observed. The meal was interrupted and the material was
aspirated with rapid recovery of oxygen saturation. Subsequently, after
the placement of the decannulation plug, wet voice was noticed. Since
similar findings were also obtained by the SLP in the following days
during daily evaluation at meal, oral feeding was interrupted due to the
high risk of pulmonary complications. For this reason, on
25\textsuperscript{th} May, after an unsuccessful attempt to place
nasogastric tube, the medical team decided to feed the patient with
parenteral nutrition. On 1\textsuperscript{st} June gastroscopy was
performed to exclude mechanical obstructions but it showed no notable
alterations. On 3\textsuperscript{rd} June the patient underwent FEES,
which revealed a complete paresis of the right hemilarynx and a partial
paresis of the left hemilarynx, in absence of heteroproductive lesions.
The right paretic vocal fold was in paramedian position, the left vocal
fold, with partial paresis, was in median position. There was sufficient
breathing space. Swallowing was characterized by vallecular and
retrocricoid salivary stagnation. A similar situation occurred during
spoon-thickened liquid swallowing test with stagnation and late
inhalation. Reduced laryngeal sensibility and late and poor reflex cough
were also observed. On 5\textsuperscript{th} June the patient underwent
head and neck CT scan to detect the possible causes of the vocal folds
paresis. The CT scan showed a structural inhomogeneity just above the
cricoarytenoid joints, sclerosis of the upper portion of the cricoid and
of both arytenoids. The Radiologist reported that the alteration
described was not purely characteristic for neoplasia, but more
correlated to a chronic inflammatory event. For this reason steroid
therapy was introduced using intravenous methylprednisolone 20 mg twice
a day for 15 days, followed by methylprednisolone 20 mg/day for a
further 25 days. After FEES and CT, the medical team considered
appropriate to position PEG (on 10\textsuperscript{th} June). The
patient underwent one-hour speech therapy re-education sessions from
Monday to Friday, with the following objectives: prevention of arytenoid
ankylosis, improvement of glottic closure, strengthening of the basis of
the tongue. FEES, on 13\textsuperscript{th} July, showed a clear
improvement of glottic muscle: the right hemilarynx paresis remained but
the left hemilarynx had a normal motility. Salivary stagnation was not
present. Swallowing tests were normal with all consistencies. Therefore,
it was indicated to start an oral nutrition re-education, under
supervision of a SLP. The patient started nutrition per os with pureed
diet and spoon-thickened liquid and constant training for compensatory
posture under the SLP supervision. Daily calories requirement was
guaranteed by lunch per os and two other meals by PEG. Administration of
drug therapies was by PEG. The patient's weight was measured daily. The
oral intake was gradually increased and solid foods and liquids were
introduced. On 16\textsuperscript{th} July there was no more secretion
or need to aspirate the patient, so tracheostomy tube was removed.

\textbf{Outcome and follow-up}

On hospital discharge (30\textsuperscript{th} July) the patient was fed
with a diet without limitations in food consistencies and liquids with
compensatory posture (head turned to the right). He took drug therapy
orally. SLP gave guidance to perform independently daily exercises at
home. PEG was no more necessary but the medical team decided to maintain
the gastrostomic access until the Ear, Nose and Throat (ENT) visit
scheduled two months after the hospital discharge. On
25\textsuperscript{th} September the patient underwent ENT visit with
FEES which showed no more paresis of the right hemilarynx and a full
recovery. The ENT specialist allowed the PEG removal. The main steps of
the patient's course are summarised in the timeline (figure 1).

\textbf{Discussion}

Since the beginning of the 2020, about 130 others patients with Covid-19
have been hospitalized in our Rehabilitation Unit. Among them, 17 were
diagnosed with mild dysphagia, with a fast recovery. None of them needed
enteral nutrition or prolonged speech therapy. Due to the severe
respiratory failure, they also had a prolonged intubation, a tracheotomy
(but for a maximum of one month) and were affected by a Critical Illness
Myopathy and Neuropathy, but they did not develop a severe dysphagia.
The patient of this case report was the only one who was still carrying
the tracheotomy tube on his arrival and had to keep the tracheal tube
because of abundant secretions in the airways, which were probably a
result of many factors: the previous history of COPD, the recent
pneumonia and the irritation of the airways due to inhalation.

This late inhalation was challenging to identify because the quality of
the voice was already altered by the presence of the tracheotomy
(despite the decannulation plug). Moreover, his voice was euphonic, not
breathy and he breathed well in ambient air with the decannulation plug.
It is already known that vocal fold paresis is often misdiagnosed
especially if the symptoms are non-specific {[}8{]}. For these reasons
it was difficult to guess a vocal fold paresis.

As it is documented in literature, swallowing with tracheotomy is more
difficult due to reduced sensitivity stimulation, attenuated tracheal
reflexes, inability to generate adequate under-glottal pressure and
reduced reflex cough. However, the presence of the tracheal tube has
allowed us to directly establish inhalation since during these episodes
there was not reflex cough as a result of a reduced laryngeal
sensibility. These issues were confirmed by FEES, which was performed
after observing the patient's performance at meal for several days.
According to the ESSD commentary, the instrumental assessment has not
been previously performed because of high infection risk {[}5{]}.

\textbf{Conclusions}

In summary, in this patient dysphagia lasted longer than expected after
an intubation but the source seems neither the intubation nor the
Sars-CoV-2 but an interaction of both. Investigating the possible
aetiology of vocal fold paresis, the instrumental exams allowed us to
exclude vascular events, neoplasms and degenerative diseases {[}8{]}. It
has not been possible to exclude post-intubation, post-viral and
idiopathic aetiology. Regarding viral aetiology, in literature there are
studies that correlate respiratory viral infections to vocal fold
paresis due to the virus neurotropism {[}9{]} and there is an increasing
evidence that the nervous system is frequently involved in patients with
Covid-19 {[}10{]}. It was therefore not possible to identify with
certainty the origin of vocal fold paresis in our patient.

Concerning the prognosis, there are no specific studies on recovery but
the data suggests a good recovery within a year. Furthermore, this
patient benefited from corticosteroid treatment, which targeted the
hyperinflammation caused by the virus {[}10{]}, and from intensive
rehabilitation therapy with a good result in approximately 50 days.

At present in literature there are not many studies about Covid-19 and
severe and prolonged dysphagia with the need of gastrostomy positioning.
Moreover, vocal fold paresis during Covid-19 was not described yet and
for this reasons a comparison is difficult.

The present case report shows that dysphagia in Covid-19 is not always
mild and may cause serious complications. Therefore, we advise not to
rely on a single evaluation and screening tests alone, but to monitor
meal performance, especially in patients at high risk of dysphagia (such
as those with long intubation or tracheotomy). Considering that
sometimes the diagnosis of dysphagia is not obvious and the gold
standard instrumental evaluations are limited due to the high risk of
aerosol-generating, awareness about dysphagia in this patient population
should be increased.

Moreover it seems important to start an appropriate and intensive
rehabilitation treatment early with high-specialized professionals.

We hope that the history of this patient will help other healthcare
professionals during their clinical practice.

\textbf{Declaration of interest}

The authors certify that there is no conflict of interest with any
financial organization regarding the material discussed in the
manuscript.

\textbf{Authorship}

GD: acquired and analysed the data, drafted the manuscript. CF: acquired
and analysed the data, drafted the manuscript. DGR: revised critically
the manuscript and supervised the project.

\textbf{Acknowledgement}

The authors acknowledge all department staff and colleagues for their
collaboration in patient management during this difficult emergency
period.

The authors acknowledge Silvia Acerbi who helped with the design of the
timeline.

\textbf{REFERENCES}

{[}1{]} - Sassi FC, Medeiros GC, Zambon LS, Zilberstein B, Andrade CRF.
Evaluation and classification of post-extubation dysphagia in critically
ill patients. \emph{Rev Col Bras Cir.} 2018;45(3):e1687.

{[}2{]} - Brodsky MB, Levy MJ, Jedlanek E, Pandian V, Blackford B, Price
C, Cole G, Hillel AT, Best SR, Akst LM.~ Laryngeal Injury and Upper
Airway Symptoms After Oral Endotracheal Intubation With Mechanical
Ventilation During Critical Care: A Systematic Review. \emph{Crit Care
Med} . 2018;46(12):2010-2017.

{[}3{]} - Frajkova Z, Tedla M, Tedlova E, Suchankova M, Geneid A.
Postintubation Dysphagia During COVID-19 Outbreak-Contemporary
Review.\emph{Dysphagia} . 2020;35(4):549-557.

{[}4{]} - Lima MS, Sassi FC, Medeiros GC, Ritto AP, Andrade CRF.
Preliminary results of a clinical study to evaluate the performance and
safety of swallowing in critical patients with COVID-19. \emph{Clinics}
. 2020;75:e2021.

{[}5{]} - Schindler A, Baijens LWJ, Clave P, Degen B, Duchac S, Dziewas
R, Farneti D, Hamdy S, Michou E, Pokieser P, Speyer R, Walshe M, Verin
E, Rommel N. ESSD Commentary on Dysphagia Management During COVID
Pandemia. \emph{Dysphagia} . 2020 Oct 27. doi:
10.1007/s00455-020-10194-z. Epub ahead of print.

{[}6{]} - Aoyagi Y, Ohashi M, Funahashi R, Otaka Y, Saitoh E.
Oropharyngeal Dysphagia and Aspiration Pneumonia Following Coronavirus
Disease 2019: A Case Report. \emph{Dysphagia} . 2020;35(4):545-548.

{[}7{]} - Cavalagli A, Peiti G, Conti C, Penati R, Vavassori F, Taveggia
G. Cranial nerves impairment in post-acute oropharyngeal dysphagia after
COVID-19: a case report. \emph{Eur J Phys Rehabil Med} . 2020 Sep 17.
doi: 10.23736/S1973-9087.20.06452-7. Epub ahead of print.

{[}8{]} - Chandra MI. Vocal fold paresis. \emph{Otolaryngol Clin N Am} .
2019; 52: 637-648.

{[}9{]} - Bhatt NK, Pipkorn P, Paniello RC. Association between Upper
Respiratory Infection and Idiopathic Unilateral Vocal Fold
Paralysis.\emph{Ann Otol Rhinol Laryngol} . 2018 Oct;127(10):667-671.

{[}10{]} - Iadecola C, Anrather J, Kamel H. Effects of COVID-19 on the
Nervous System. \emph{Cell} . 2020 Oct 1;183(1):16-27.

\textbf{Figures}

Figure 1. - \emph{Timeline}\selectlanguage{english}
\begin{figure}[H]
\begin{center}
\includegraphics[width=0.70\columnwidth]{figures/Timeline/Timeline}

\end{center}
\end{figure}

\selectlanguage{english}
\FloatBarrier
\end{document}

