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\begin{document}

\title{A longitudinal study of unilateral M\selectlanguage{ngerman}énière's disease and clinical
evolutionary models Ménière's based on the vertigo episodes.\selectlanguage{english}}



\author[1]{Tomàs Pérez-Carbonell}%
\author[1]{Miguel Orts-Alborch}%
\author[2]{Vanesa Pérez-Guillen}%
\author[3]{José María Tenías-Burillo}%
\author[1]{Ignacio Pla-Gil}%
\author[4]{Jaime Marco Algarra}%
\author[2]{Herminio Pérez-Garrigues}%
\affil[1]{Hospital Clínico Universitario}%
\affil[2]{La Fe University and Polytechnic Hospital}%
\affil[3]{Pare Jofrè Hospital. Conselleria de Sanitat Universal i Salut Pública}%
\affil[4]{University of Valencia}%


\vspace{-1em}



  
  \date{May 25, 2024}


\begingroup
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\selectlanguage{english}
\begin{abstract}
INTRODUCTION: The variability in symptomatic evolution of vertiginous
crisis in M\selectlanguage{ngerman}énière's disease (MD) is just one more fact that indicates
the great heterogeneity attributed to MD. Recently, these variations and
differences between patients are being defined by different subtypes of
MD. OBJECTIVES: We have defined subtypes of MD based on the evolution of
vertigo crisis in the first 10 years of the disease, in addition to
defining the natural history of Unilateral MD (UMD) in our environment.
DESIGN: A longitudinal descriptive study of patients with UMD was
carried out. In a subgroup of patients followed from the onset of the
disease, three subtypes or models of UMD were defined according to the
individual review and our experience according to the vertiginous crisis
suffered the first 10 years of the disease. In these models a
differential behavior has been studied attending to different variables
analyzed. RESULTS: Data were collected from 327 patients with UMD, of
which 87 were followed from the onset of the disease. In this subgroup,
patients were grouped in 3 models. Model No. 3 was associated with a
worse auditory prognosis, a greater number of Tumarkin crisis, the need
for surgery, and a more frequent mononymptomatic debut. Model No. 1
presented a lower hearing loss compared to the rest of the models.
CONCLUSION: Several studies tried to define subtypes of MD. In our study
we have defined 3 models of behavior in UMD based on the number of
crisis suffered, which present a differential behavior according to
different aspects.%
\end{abstract}\selectlanguage{ngerman}%



\sloppy


A longitudinal study of unilateral M\selectlanguage{ngerman}énière's disease and clinical
evolutionary models Ménière's based on the vertigo episodes.

Abstract:

INTRODUCTION: The variability in symptomatic evolution of vertiginous
crisis in Ménière's disease (MD) is just one more fact that indicates
the great heterogeneity attributed to MD. Recently, these variations and
differences between patients are being defined by different subtypes of
MD.

OBJECTIVES: We have defined subtypes of MD based on the evolution of
vertigo crisis in the first 10 years of the disease, in addition to
defining the natural history of Unilateral MD (UMD) in our environment.

DESIGN: A longitudinal descriptive study of patients with UMD was
carried out. In a subgroup of patients followed from the onset of the
disease, three subtypes or models of UMD were defined according to the
individual review and our experience according to the vertiginous crisis
suffered the first 10 years of the disease. In these models a
differential behavior has been studied attending to different variables
analyzed.

RESULTS: Data were collected from 327 patients with UMD, of which 87
were followed from the onset of the disease. In this subgroup, patients
were grouped in 3 models. Model No. 3 was associated with a worse
auditory prognosis, a greater number of Tumarkin crisis, the need for
surgery, and a more frequent mononymptomatic debut.

Model No. 1 presented a lower hearing loss compared to the rest of the
models.

CONCLUSION: Several studies tried to define subtypes of MD. In our study
we have defined 3 models of behavior in UMD based on the number of
crisis suffered, which present a differential behavior according to
different aspects.

Keywords: ``Meniere Disease'', ``vestibular diseases'', ``longitudinal
studies'', ``vestibular disorders'', ``inner ear'', ``clinical models'',
``Subgroups'', ``neurotology''.

Five succinct points:

\begin{enumerate}
\tightlist
\item
  In most of uMD patients after the first four years of follow-up, there
  is a reduction and stabilization of the average annual number of
  vertigo crises
\item
  An exhaustive medical follow-up from the onset of the disease may
  reduce the need for a future surgical intervention.
\item
  Unilateral MD patients can be classified according the number of
  vertigo crises suffered the first ten years of the disease, on three
  clinical evolutionary models.
\item
  Significant differences has been observed when the extent of hearing
  loss has been considered in association with the different clinical
  models.
\item
  Patients included in model three had a worse disease prognosis in
  terms of the number of vertigo episodes, Tumarkin crises and need for
  surgical intervention.
\end{enumerate}

\textbf{2.Body of text}

1.INTRODUCTION

After the first episode, episodes of vertigo are recurrent in MD.
However, how the behaviour of the disease evolves as a function of the
number of vertigo episodes it still not absolutely clear. From the first
year of the disease, there is a gradual decrease in the number of
vertigo episodes over the first eight years of the disease, which is
followed by a subsequent stabilization, and then by a mild and
progressive decrease in the following 10 years (1). However, there are
reports of an increase in the number of seizures/year in those patients
who have experienced episodes for more than 10-15 years (2,3). In
contrast, MD is also associated with periods of remission in which the
individual does not experience any episode of vertigo, with a variable
duration between the episodes of vertigo (4,5) that may ultimately lead
to a complete cessation of the episodes of vertigo. We do not know how
or when these periods of remission arise, yet it has been proposed that
70\% of patients who do not have episodes of vertigo for one year will
not experience any episode during the following year (1).

Although the course of the vertigo episodes in MD is well-defined for
the general population of MD patients, \emph{it} does not accommodate
the wide clinical variability presented by each individual patient. In
addition, there is considerable heterogeneity regarding the evaluation
of these episodes of vertigo, their duration and intensity. The
heterogeneity among patients with MD, not only in the course of vertigo
episodes but in several other aspects of the disease, makes us think
that there are different subtypes of MD. In recent years, new studies
have emerged that attempt to explain this variation or the heterogeneous
behaviour of the disease, attempting to identify clinical subgroups to
help explain the different forms of the disease (6--8).

2. OBJECTIVES

After analyzing the course of the disease in a very large series of
patients who have been followed since the onset of the disease, we found
that the evolution of the symptoms in patients differed based on the
annual number of vertigo episodes in the first 10 years of the disease.
Therefore, we wanted to assess the possible existence of ``subtypes'' of
MD based on the frequency of vertigo episodes in the initial years of
the disease, and help to define the natural evolution of unilateral MD
(uMD).

3. MATERIALS AND METHODS

A longitudinal descriptive study was carried out on patients from two
referral centres with UMD. The patients' data was collected and stored
from 1977 to 2018, after which the data collected was processed and
analysed. All the patients data were revised to confirm that they met
updated criteria for complete MD.

At their first visit to each of the centers, the patients were advised
to consult the Otorhinolaryngology (ENT) specialist every six months. At
the first and subsequent visits, different variables were registered:
clinical - onset of each symptom, date of the first visit, follow-up
time, number of vertigo episodes in the last 6 months, type and date of
the different surgical interventions undertaken, associated diseases,
presence of Tumarkin crisis; audiometric - hearing parameters according
to liminal pure tone audiometry at frequencies of 250, 500, 1,000, 2,000
and 4,000 Hz.

After recording the different variables, we analysed the evolution of
the vertigo episodes in each patient during the period in which they
were followed. This period was defined as the time elapsed between the
first and the last visit, or in the case of those who underwent a
surgical intervention, the date of this intervention was taken as the
end of the follow-up for our study. We consider the following as
surgical procedures that can modify the natural evolution of the
disease: chemical labyrinthectomy, surgical labyrinthectomy,
endolymphatic sac decompression, vestibular neurectomy, or cochlear
implantation.

Many of the patients came to seek care a few months or years after the
onset of disease symptoms. Thus, we could not precisely define the exact
evolution of their disease before they were attended at the care
centers. For this reason, a subgroup of patients who had been followed
from the onset of the disease was defined. This subgroup included those
patients in whom the time elapsed from the onset of the first symptom
and the first visit to the ENT service was \selectlanguage{english}[?]365 days.

In this group, for which we have reliable information on the evolution
of the disease, the number of annual vertigo episodes was revised
individually and accordingly, 3 clinical evolutionary models were
defined according to the evolutionary behaviour of the episodes in the
first 10 years of the disease.

All patients gave their written consent that they wanted to participate
in this work.

\emph{Analytic strategy}

\begin{itemize}
\tightlist
\item
  Univariate analysis: Descriptive statistics appropriate to the nature
  of each variable were estimated, including the measures of central
  tendency, dispersion, and tables of the absolute and relative
  frequencies of each variable.
\item
  Bivariate analysis: a contrast analysis was used to test the
  relationship between the variables, employing Chi-squared tests to
  examine relationships between categorical variables, correlation tests
  to examine relationships between quantitative variables, and a
  comparison of means using Student's t-tests, Analysis of variance
  (ANOVA) or their non-parametric equivalents (Mann-Whitney U test and
  Kruskall-Wallis H test).
\item
  The evolution of the episodes over time was modelled out using the
  mean episodes suffered during each year of the follow-up, reflecting
  this evolution in a similar way to routine clinical practice. On some
  occasions, the incidence rate was the parameter used in each follow-up
  period (number of episodes suffered/time elapsed since the last
  visit).
\end{itemize}

The statistical package SPSS(r) \emph{v.22} was used for the statistical
analysis.

4.RESULTS

During the course of the longitudinal study, data were collected from
327 patients with unilateral UMD, of which 87 (26.6\%) were followed up
from the onset of the disease.

\emph{Evolution of vertigo episodes and clinical models}

In the UMD group of patients, the mean incidence of annual episodes
reached a maximum value of 7.56 in the first year (SD +-13.68), 4.36
(+-7.44) in the second year, and 2.94 (+- 5.47) in the third and fourth
years of follow-up. Subsequently, the number of episodes stabilized to a
value of less than 2 episodes per year until the tenth year, and they
reduced until there was a cessation in the episodes in subsequent years
(figures 1 and 2).

In the subgroup of patients followed from the onset of the disease,
after analysing each case individually, specific criteria were defined
by which all these patients can be grouped into 3 behavioural or
evolutionary models based on the number of vertigo episodes/year
experienced during the first 10 years of the disease (Figure 3).

Model 1: Sudden onset with no further episodes from the fourth year
after disease onset. These patients experience episodes of vertigo in
consecutive years during the first four years of the disease (N=39,
44.8\%).

Model 2: Sudden onset followed by a period of relapse. Episodes of
vertigo are experienced in the first four years of the disease followed
by a period with no episodes that lasted for at least one-year, with a
subsequent relapse or occurrence of episodes of vertigo in one or more
consecutive years (N=30, 34.5\%).

Model 3: Multiple relapses throughout the course of the disease or with
a worst evolution. During the first 10 years of disease, episodes of
vertigo are recorded in at least 7 years, whether consecutively or
followed by intercritical periods of one or two years with no episodes
(N=18, 20.7\%).

\emph{General descriptive data}

Table 1 shows the results for the different variables analysed in each
group.

\emph{Timeline of the symptoms}

In most of the subgroups analysed, there was a slight predominance in
the occurrence of a single symptom at disease onset relative to
individuals with a bi-symptomatic onset or that involving a triad of
symptoms. This was not the case in model 3 of clinical evolution, where
the difference between the occurrence of a single symptom and the
occurrence of the triad of symptoms at disease onset was much
greater.(Table 1).

\emph{Hearing outcomes}

All groups of patients with UMD exhibited a mean tonal threshold
corresponding to moderate hearing loss, with a greater degree of
low-frequency hearing loss at the beginning of the disease. These
thresholds evolved to a more severe degree of hearing loss by the end of
follow-up.

Significant differences were observed when the extent of hearing loss
was considered in association with the different clinical models (Table
2).

4.DISCUSSION

\emph{Evolution of vertigo episodes} \emph{and clinical models}

Understanding the general evolution of vertigo episodes and taking into
account our clinical experience and the individual revision of each
case, we observed that the evolution of vertigo episodes differed
considerably between cases during the first 10 years of the disease. We
decided to define a series of criteria according to which the whole
cohort of patients could be assigned to different subgroups.

We defined a series of subgroups based on the evolution and behaviour of
vertigo episodes, although there are many ways of grouping the clinical
variations typical of MD (6--8).

In our view, the most relevant work in this regard is that in which five
subgroups of patients were defined (7): classic MD, delayed MD, familial
MD, MD associated with migraine and MD associated with autoimmune
disorders. In our models, familial association and a history of
autoimmune diseases are not taken into account, although some
hypothetical associations and comparisons could be made with these
groups. Our model number 2 was that in which patients most frequently
also suffered from migraine and that in which there was an earlier
disease onset, as previously reported for the subgroup of patients with
MD associated with migraine. Model number 3 had the highest proportion
of patients that suffered a Tumarkin crisis and no patient with
migraines, and it was the model in which the patients experienced the
largest number of vertigo episodes, as reported previously(7), as the
subgroup of patients with MD associated with autoimmune diseases.

Accordingly, in different studies in this field groups of patients have
been classified based on specific criteria(6,7). However, as they share
common features, it would appear that there are different forms of MD
that can be distinguished on the basis of the criteria used in these
studies.

\emph{Migraine and Tumarkin Crisis}

In our series, a smaller proportion of patients in the group of patients
followed from the onset of the disease reported migraines relative to
the total group of patients with UMD. Thus, early care and a close
follow-up of the disease may be associated with a better management of
this type of headaches. Taking into account that approximately 12\% of
the general population suffers from migraine (9), and 10 to 51\% of
patients with MD (10--12), this may be underestimated in our sample. The
reason for this may be that we were not sufficiently cautious in
assessing the presence of migraine in the initial years of data
collection, as the migraine-MD relationship was not as relevant at that
time as it is at present. However, these would be non-differential
biases equally distributed throughout the sample and that would not lead
to an incorrect estimate of the associations but rather, to a reduction
in the existing estimates.

In our series 12,2\% patients reported the presence of Tumarkin crises,
that is consistent with the published, 5-15\% of patients (13--16).
Patients within model number 3 are those that experienced the highest
proportion of Tumarkin crises between episodes (17.7\%), which augmented
the perceived severity of MD in these patients.

\emph{Surgical treatments}

Around 10-20\% of patients with MD require surgical treatments (17),
those have been reduced to those patients with a worse evolution and
less symptomatic control. As all surgical procedures can modify the
disease course, we classified the patients as ''operated'' or ''not
operated'' and we performed the analysis irrespective of the surgical
procedure undertaken.

In our series the proportion of patients operated for their UMD is 16\%,
increasing to 27\% in model number 3.

The 16\% of the MD patients followed from the onset of the disease that
required a surgical intervention was lower than the whole group of
patients with UMD. As such, carrying out an exhaustive medical follow-up
from the onset of the disease may reduce the need for a future surgical
intervention aimed at controlling the symptoms of MD.

\emph{Timeline of the symptoms}

In our series, 34.1\% of patients with UMD presented with the triad of
symptoms at disease onset, which is consistent with many studies
(18--20). We observed a different behaviour of patients included in
model number 3 in this sense, half of patients has a monosymptomatic
onset.

\emph{The evolution of hearing}

During the first years of the disease, the greatest degree of hearing
loss coincides with a higher prevalence of vertigo episodes (1), even
though these subsequently diminish or disappear while hearing loss
persists (21,22). In this regard, our results show that patients within
model number one, who suffer from vertigo episodes for a shorter time,
experience less hearing loss. This could be explained by the fact that,
experiencing episodes of vertigo for a shorter period of time is
associated with better preservation of hearing. However, model number
two presented greater mean hearing loss than those in model number
three, which is that in which there was a worse severity in the temporal
evolution of vertigo episodes.

\emph{Limitations and strengths}

The present study suffers from biases typical of an observational study,
although these would be non-differential biases whereby all patients
would be equally affected, regardless of the subgroup they belong to. As
such, the estimated associations would tend towards a null value (no
association). Furthermore, we have not taken into account variables such
as the association with autoimmune diseases or any family history of the
disease, which are now considered as variables defining possible
subtypes of MD.

Conversely, we provide data from a longitudinal study carried out on a
large number of patients with a long follow-up. Moreover, we have
performed an analysis of variables related to MD and their outcomes in
different subgroups. To date, no study has yet attempted to explain the
existence of different evolutionary models of the disease in this sense
and hence, we believe that our study may offer a new perspective to
define the existence of different subtypes of uMD.

5.CONCLUSIONS

In most of the uMD patients, after the first four years of disease
follow-up, there is a reduction and a stabilization in the mean number
of annual episodes of vertigo. An in depth analysis of the number of
episodes of vertigo over the first 10 years of disease evolution has
enabled us to define 3 clinical models based on the evolution of the
episodes of vertigo suffered in the first 10 years of the disease.
Patients included in model number one showed significantly less hearing
loss at the end of follow-up. The patients included in model three had a
worse disease prognosis in terms of the number of vertigo episodes,
number of Tumarkin crises, a greater need for surgical intervention and
a mono-symptomatic onset.

The data presented here offer criteria that may help to predict the
evolution of MD in different subsets of patients, enabling their
treatment to be better personalized, while encouraging a close follow up
of the episodes of vertigo in UMD patients.

8. REFERENCES

1. Perez-Garrigues H, Lopez-Escamez JA, Perez P, Sanz R, Orts M, Marco
J, et al. Time course of episodes of definitive vertigo in Meniere's
disease. Arch Otolaryngol Head Neck Surg. 2008 Nov 17;134(11):1149--54.

2. Tokumasu K, Fujino A, Yoshio S, Hoshino I. Prognosis of Meniere's
disease by conservative treatment: retrospective study on the time
course of the disease. Acta Otolaryngol Suppl. 1995;519(March):216--8.

3. Tokumasu K, Fujino A, Naganuma H, Hoshino I, Arai M. Initial symptoms
and retrospective evaluation of prognosis in Meniere's disease. Acta
Otolaryngol Suppl. 1996;524:43--9.

4. Havia M, Kentala E. Progression of Symptoms of Dizziness in Meniere's
Disease. Head Neck. 2004;130(Md):431--5.

5. Friberg U, Stahle J, Svedberg A. The natural course of Meniere's
disease. Acta Otolaryngol Suppl. 1984;406:72--7.

6. Montes-Jovellar L, Guillen-Grima F, Perez-Fernandez N. Cluster
analysis of auditory and vestibular test results in definite meniere's
disease. Laryngoscope. 2011;121(8):1810--7.

7. Frejo L, Martin-Sanz E, Teggi R, Trinidad G, Soto-Varela A,
Santos-Perez S, et al. Extended phenotype and clinical subgroups in
unilateral Meniere disease: A cross-sectional study with cluster
analysis. Clin Otolaryngol. 2017;(January):1--9.

8. Frejo L, Soto-Varela A, Santos-Perez S, Aran I, Batuecas-Caletrio A,
Perez-Guillen V, et al. Clinical subgroups in bilateral meniere disease.
Front Neurol. 2016;7(OCT):1--10.

9. Swaminathan A, Smith JH. Migraine and Vertigo. Curr Neurol Neurosci
Rep. 2015;15(2).

10. Clemmens C, Ruckenstein M. Characteristics of Patients With
Unilateral and Bilateral Meniere's Disease. Otol Neurotol. 2012
Sep;33(7):1266--9.

11. Ray J, Carr SD, Popli G, Gibson WP. An epidemiological study to
investigate the relationship between Meniere's disease and migraine.
Clin Otolaryngol. 2016;41(6):707--10.

12. Ghavami Y, Mahboubi H, Yau AY, Maducdoc M, Djalilian HR. Migraine
features in patients with Meniere's disease. Laryngoscope.
2016;126(1):163--8.

13. Baloh RW, Jacobson K, Winder T. Drop attacks with Meniere's
syndrome. Ann Neurol. 1990;28(3):384--7.

14. Black FO, Effron MZ, Burns DS. Diagnosis and Management of Drop
Attacks of Vestibular Origin: Tumarkin's Otolithic Crisis. Otolaryngol
Neck Surg. 1982 Mar;90(2):256--62.

15. Viana LM, Bahmad F, Rauch SD. Intratympanic gentamicin as a
treatment for drop attacks in patients with Meniere's disease.
Laryngoscope. 2014;124(9):2151--4.

16. Gurkov R, Jerin C, Flatz W, Maxwell R. Clinical manifestations of
hydropic ear disease (Meniere's). Eur Arch Oto-Rhino-Laryngology. 2018
Oct 10;

17. Kitahara T. Evidence of surgical treatments for intractable
Meniere's disease. Auris Nasus Larynx. 2018;45(3):393--8.

18. Havia M, Kentala E, Pyykko I. Hearing loss and tinnitus in Meniere's
disease. Auris Nasus Larynx. 2002 Apr;29(2):115--9.

19. Pyykko I, Nakashima T, Yoshida T, Zou J, Naganawa S. Meniere's
disease: a reappraisal supported by a variable latency of symptoms and
the MRI visualisation of endolymphatic hydrops. BMJ Open. 2013 Feb
14;3(2):e001555.

20. Belinchon A, Perez-Garrigues H, Tenias JM. Evolution of symptoms in
Meniere's disease. Audiol Neurotol. 2012;17(2):126--32.

21. Katsarkas A. Hearing loss and vestibular dysfunction in Meniere's
disease. Acta Otolaryngol. 1996 Mar;116(2):185--8.

22. Thomas K, Harrison S. long-therm follow upof 610 cases of meniere's
disease. Proc R Soc Med. 1971;64(8):856--7.

9. FIGURE CAPTIONS

\textbf{Fig 1.} Average incidence according to year of follow-up of the
disease in UMD patients.

\textbf{Fig 2.} Average incidence according to five-year follow-up of
the disease in UMD patients.

\textbf{Fig 3.} Course of disease for each subtype expressed in the mean
annual number of vertigo episodes suffered in the first ten years.\selectlanguage{english}
\begin{figure}[H]
\begin{center}
\includegraphics[width=0.70\columnwidth]{figures/Figure-1/Figure-1}

\end{center}
\end{figure}\selectlanguage{english}
\begin{figure}[H]
\begin{center}
\includegraphics[width=0.70\columnwidth]{figures/Figure-2/Figure-2}

\end{center}
\end{figure}\selectlanguage{english}
\begin{figure}[H]
\begin{center}
\includegraphics[width=0.70\columnwidth]{figures/Figure-3/Figure-3}

\end{center}
\end{figure}

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