10.14639/0392-100X-N1017
Objective. This prospective study aimed to investigate the role of migraine in favouring the onset of persistent postural perceptual dizziness (PPPD) following paroxysmal positional vertigo (PPV). Methods. A group of patients who came to our attention suffering of PPV with or without migraine and/or vestibular migraine (VM) was examined. Three months after the resolution, an anamnestic research was conducted aimed at establishing whether any patientrelated dizziness could meet the diagnostic criteria for PPPD. Results. 12 of the 240 patients recruited met the diagnostic criteria for PPPD for an overall incidence of 5%, with 3 (1.85%) belonging to the non-migraine group and 9 (11.5%) to the migraine group. In the latter, 6 (28.6%) patients with VM and 3 (5.26%) without VM were affected. Conclusions. The study shows a significant increase of PPPD diagnosis in migraine compared to patients without migraine (p = 0.003). Within migraine there was a significant increase in those with VM compared to patients without VM (p = 0.0016). No difference emerged between patients without migraine and migraine patients without VM (p &gt; 0.05). The presence of VM in patient’s history, but not migraine without VM, appears to significantly increase the incidence of PPPD in patients with PPV.
text/xml
1827-675X
1017
en
Mario Faralli
https://creativecommons.org/licenses/by-nc-nd/4.0
ACTA Otorhinolaryngologica Italica
dizziness
Persistent postural perceptual dizziness following paroxysmal positional vertigo in migraine
Text.Serial.Journal
https://www.actaitalica.it/
41
Vestibology
2021-07-07
2020-07-24
2021-07-08
2021-07-08
263-269
1
Mario Faralli
2021/07/07
10.14639/0392-100X-N1017
263
Section of Otolaryngology-Head and Neck Surgery, Department of Surgical and Biomedical Sciences, University of Perugia, Perugia, Italy
1827-675X
dizziness
269
Persistent postural perceptual dizziness following paroxysmal positional vertigo in migraine
https://www.actaitalica.it/article/download/1017/625
41
ACTA OTORHINOLARYNGOLOGICA ITALICA 2021;41:263-269; doi: 10.14639/0392-100X-N1017




Vestibology


Persistent postural perceptual dizziness following
paroxysmal positional vertigo in migraine
La dizziness posturale percettiva persistente dopo vertigine posizionale parossistica
nell’emicrania
Paolo Tropiano, Luca Maria Lacerenza, Giovanni Agostini, Annalisa Barboni, Mario Faralli
Section of Otolaryngology-Head and Neck Surgery, Department of Surgical and Biomedical Sciences, University of Perugia,
Perugia, Italy


SUMMARY
Objective. This prospective study aimed to investigate the role of migraine in favouring the
onset of persistent postural perceptual dizziness (PPPD) following paroxysmal positional
vertigo (PPV).
Methods. A group of patients who came to our attention suffering of PPV with or without
migraine and/or vestibular migraine (VM) was examined. Three months after the resolu-
tion, an anamnestic research was conducted aimed at establishing whether any patient-
related dizziness could meet the diagnostic criteria for PPPD.
Results. 12 of the 240 patients recruited met the diagnostic criteria for PPPD for an overall
incidence of 5%, with 3 (1.85%) belonging to the non-migraine group and 9 (11.5%) to the
migraine group. In the latter, 6 (28.6%) patients with VM and 3 (5.26%) without VM were
affected.                                                                                       Received: July 24, 2020
Conclusions. The study shows a significant increase of PPPD diagnosis in migraine com-          Accepted: November 27, 2020
pared to patients without migraine (p = 0.003). Within migraine there was a significant
increase in those with VM compared to patients without VM (p = 0.0016). No difference           Correspondence
emerged between patients without migraine and migraine patients without VM (p > 0.05).          Paolo Tropiano
The presence of VM in patient’s history, but not migraine without VM, appears to signifi-       Otorhinolaryngology Clinic, S.M. della Misericor-
cantly increase the incidence of PPPD in patients with PPV.                                     dia Hospital
                                                                                                via G. Dottori 1, 06100 S. Andrea delle Fratte,
KEY WORDS: PPPD, vestibular migraine, vestibular disorders, dizziness                           Perugia, Italy
                                                                                                E-mail: tropianopaolo@gmail.com
RIASSUNTO
Obiettivo. Questo studio prospettico indaga il ruolo favorente dell’emicrania nell’insor-       Funding
genza della dizziness percettiva posturale persistente (PPPD) dopo vertigine posizionale        None.
parossistica (PPV).
Metodi. È stata esaminata una popolazione consecutiva di pazienti affetti da PPV, con o         Conflict of interest
                                                                                                The Authors declare no conflict of interest.
senza emicrania e/o emicrania vestibolare (VM). Tre mesi dopo la risoluzione della PPV, è
stata condotta una anamnesi volta a stabilire se una dizziness residua correlata al paziente
potesse soddisfare i criteri diagnostici per la PPPD.                                             How to cite this article: Tropiano P, Lacer-
Risultati. 12 di 240 pazienti reclutati soddisfacevano i criteri diagnostici per la PPPD          enza LM, Agostini G, et al. Persistent postural
con un’incidenza complessiva del 5%, 3 (1,85%) appartenenti al gruppo non emicranico              perceptual dizziness following paroxysmal
e 9 (11,5%) a quello emicranico. Nello specifico, 6 pazienti (28,6%) con VM e 3 senza VM          positional vertigo in migraine. Acta Otorhi-
(5,26%) erano interessati.                                                                        nolaryngol Ital 2021;41:263-269. https://doi.
                                                                                                  org/10.14639/0392-100X-N1017
Conclusioni. Lo studio mostra un aumento significativo della diagnosi di PPPD nell’emi-
crania rispetto ai pazienti senza (p = 0,003). Nell’emicrania c’è stato un aumento signifi-
                                                                                                © Società Italiana di Otorinolaringoiatria
cativo in quelli con VM rispetto ai pazienti senza (p = 0,0016). Nessuna differenza è emersa    e Chirurgia Cervico-Facciale
tra i pazienti senza emicrania e pazienti emicranici senza VM (p > 0,05). La presenza di VM
nella storia del paziente sembra aumentare significativamente l’incidenza di PPPD che si
                                                                                                               OPEN ACCESS
verifica in pazienti con PPV.
                                                                                                This is an open access article distributed in accordance with
PAROLE CHIAVE: PPPD, emicrania vestibolare, disordini vestibolari, dizziness                    the CC-BY-NC-ND (Creative Commons Attribution-Non-
                                                                                                Commercial-NoDerivatives 4.0 International) license. The
                                                                                                article can be used by giving appropriate credit and mentio-
                                                                                                ning the license, but only for non-commercial purposes and
                                                                                                only in the original version. For further information: https://
                                                                                                creativecommons.org/licenses/by-nc-nd/4.0/deed.en




                                                                                                                                                        263
P. Tropiano et al.




Introduction                                                      immediately with repositioning procedures after positional
                                                                  tests that led to the diagnosis of the disease. Positional tests
Persistent postural perceptual dizziness (PPPD) is classi-
                                                                  were repeated 3-4 days later to verify the possible disappear-
fied as a chronic functional vestibular disorder 1. It is not
                                                                  ance of the nystagmus and resolution of PPV (1st control).
a structural or psychiatric condition, although both can
                                                                  If the control was negative, the diagnostic manoeuvres were
coexist with the syndrome. Functional changes in postural
                                                                  re-programmed 7 days later to confirm the absence of the
control strategies 2,3, shifts in multi-sensory information
                                                                  nystagmus (2nd control). On this occasion, patients in whom
processing 4 and reduced cortical integration of spatial ori-
                                                                  the resolution of the PPV was confirmed again, were asked
entation and threat assessment networks 5 can be invoked in
                                                                  if there was a new condition of dizziness that arose after the
the pathophysiologic processes underlying PPPD. Recent-
                                                                  disappearance of the nystagmus and currently present (Re-
ly, the diagnostic criteria for PPPD have been formulated
                                                                  sidual Dizziness: RD) 15. In all patients, on the other hand,
in a consensus paper by the Barany society 1. Although the
                                                                  where diagnostic manoeuvres revealed the nystagmus at the
term is new, PPPD collects aspects already described in
                                                                  1st or 2nd control, repositioning manoeuvres were repeated
various previous syndromes such as phobic postural ver-
                                                                  and a new control was scheduled at 3-4 days until the nys-
tigo 6, space motion discomfort 7, visual vertigo 8 and sub-
                                                                  tagmus disappeared, according to our protocol (Fig. 1). A 3rd
jective chronic dizziness 9. PPPD may be precipitated by
                                                                  control, three months after the 2nd control, was performed in
conditions that disrupt balance or cause vertigo, unsteadi-
                                                                  all patients who in the meantime had no other documented
ness, or dizziness. These conditions include peripheral
                                                                  episodes of PPV. Confirmed the absence of nystagmus and
or central disorders, panic attacks or anxiety, concussive
                                                                  the resolution of PPV by performing positional tests, pa-
brain injuries, whiplash of the neck, autonomic disorders
                                                                  tients who had reported RD were asked again if this con-
and medical illnesses 9,10. The majority of conditions that
                                                                  dition was still present. To complete the investigation, an
precede PPPD are acute or episodic in nature and patients
                                                                  anamnestic research was conducted aimed at establishing
report the onset of chronic symptoms of PPPD following
                                                                  whether any patient-related dizziness, not identifiable in
their acute illness 1. Paroxysmal positional vertigo (PPV)
is the most common peripheral vestibular disorder and is          the typical vertigo crisis of PPV, could meet the diagnostic
typically a recurrent vertigo with alternating active phases      criteria for PPPD 1 (Tab. I). The time interval established
of the disease with intercritical periods of variable duration.   in this protocol is justified by the minimum duration of the
Migraine is also often present in the history of a patient        required dizziness according to the diagnostic criteria for
with recurrent vertigo. Migraine can even play a decisive         PPPD. All patients who, in the time interval between the
pathogenetic role as it happens by definition in vestibular       2nd and 3rd control, had a new episode of PPV confirmed by
migraine 11 or, alternatively, be a significant comorbidity       the repetition of the diagnostic manoeuvres, were excluded
as in Ménière’s disease 12. In PPV, in particular, migraine       from the study. Patients with a history of vestibular neuritis
seems to condition a higher incidence 13,14 and an earlier on-    and suffering from Ménière’s disease and central vestibular
set of the disease 14. Therefore, if PPPD can be precipitated     disorders were excluded. Patients over the age of 65 were
by an acute event in the course of a recurrent vestibulopa-       also excluded. The latter criterion has been adopted as it is
thy, it is conceivable that migraine, if present, could condi-    considered a less likely influence of the pathogenetic mech-
tion this evolution. The initial purpose of this study was to     anism of migraine with advancing age 16. Finally, patients
ascertain the real existence of a clinical entity, which arose    with post-traumatic PPV were excluded, as the injury itself
in the evolutionary stages of a recurrent vestibulopathy, ca-     can cause PPPD 1. To avoid an inclusion of pre-existing PP-
pable of satisfying the diagnostic criteria for PPPD. Subse-      PD, only patients without persistent dizziness, unsteadiness
quently, the investigation was aimed at verifying a possible      or non-spinning vertigo in the three months preceding the
influence of migraine in determining the clinical feature.        PPV attack were recruited. Of the five criteria that define
For this reason, a group of consecutive patients, who came        PPPD, we only considered the quality of the symptom at
to our attention suffering of PPV with or without migraine        the first observation 1. Since all criteria must be fulfilled for
(M) and/or vestibular migraine (VM), was examined.                a diagnosis of PPPD, the absence of one symptom conse-
                                                                  quently excludes the diagnosis. Based on the natural history
                                                                  of the disease, patients were divided into 2 groups: Group
Materials and methods                                             A and Group B. Group A includes patients in whom PPV,
277 consecutive patients (167 F, 110 M), between 18 and           documented in the study, was the first and only episode in
65 years of age (age 46 ± 12.4), with a diagnosis of PPV          life. Group B includes patients in whom PPV, documented
made at our clinic in the period between 31 July 2017 and         in the study, did not represent the first and only episode,
31 January 2020 were evaluated. All patients were treated         and therefore having a recurrent trend. This definition indi-



264
                                                                                                                                              PPPD following PPV




Figure 1. Inclusion criteria in the study of patients with paroxysmal positional vertigo (PPV).


Table I. Criteria for the diagnosis of persistent postural-perceptual dizziness (PPPD): all five criteria must be fulfilled to make the diagnosis.
 A. One or more symptoms of dizziness, unsteadiness, or non-spinning vertigo are present on most days for 3 months or more:
    1. Symptoms last for prolonged (hours long) periods of time, but may wax and wane in severity
    2. Symptoms need not be present continuously throughout the entire day
 B. Persistent symptoms occur without specific provocation, but are exacerbated by three factors:
    1. Upright posture
    2. Active or passive motion without regard to direction or position, and
    3. Exposure to moving visual stimuli or complex visual patterns
 C. The disorder is precipitated by conditions that cause vertigo, unsteadiness, dizziness, or problems with balance including acute, episodic, or chronic
    vestibular syndromes, other neurologic or medical illnesses, or psychological distress:
    1. When the precipitant is an acute or episodic condition, symptoms settle into the pattern of criterion A as the precipitant resolves, but they may occur
    intermittently at first, and then consolidate into a persistent course
    2. When the precipitant is a chronic syndrome, symptoms may develop slowly at first and worsen gradually
 D. Symptoms cause significant distress or functional impairment
 E. Symptoms are not better accounted for by another disease or disorder



cates a PPV with at least two documented active phases of                           nPPV). The study was conducted at the Department of Sur-
the disease with a free interval lasting at least three months.                     gical and Biomedical Sciences, Section of Otolaryngology-
In all patients recruited, the number of therapeutic sessions                       Head and Neck Surgery of the University of Perugia (Italy).
necessary to obtain the disappearance of the nystagmus and                          The authors assert that all procedures contributing to this
the resolution of the PPV was calculated. Based on whether                          work comply with the ethical standards of the relevant na-
or not a current or previous history of migraine (M) with or                        tional and institutional guidelines on human experimenta-
without aura according to the International Classification of                       tion and with the Helsinki Declaration of 1975, as revised in
Headache Disorders (ICHD) 17, patients were divided into                            2008. Informed consent was obtained from all participants
group M and group nM respectively. Group M patients were                            in the study.
in turn divided into group VM/M if the diagnostic criteria
of the VM defined by the Barany Society 11 were met, and                            Statistical analyses
group nVM/M if the same criteria were not fulfilled. The re-                        The incidence of PPPD in the population of patients with
sults emerged were compared with those of a control group                           PPV examined in the study was calculated and the preva-
of 52 consecutive patients (average age 44.5 ± 7.2) affected                        lence of PPPD within the groups considered. The statisti-
by VM of our database without history for PPV (group VM/                            cal comparison between the percentage values was carried



                                                                                                                                                                 265
P. Tropiano et al.




out by means of chi-square test alone and with Yates cor-
rection where considered necessary. Parametric t-test was
performed for the comparison between means and standard
deviations. The significance level was set at p < 0.05.

Results
Of the 277 patients initially evaluated, 12 were excluded
because they suffered from Ménière’s disease (MD) (6 pa-
tients), neuritis vestibularis (NV) (2 patients) and central
vestibular disorders (4 patients). 17 patients were excluded
as they presented a new episode of PVV between the 2nd and
3rd control. Finally, 8 patients did not show up for the final
evaluation on the occasion of the 3rd control. Therefore, 240
                                                                                Figure 3. Incidence of persistent postural perceptual dizziness (PPPD) in
patients were definitively recruited in the present survey,                     groups with or without migraine.
124 (51.7%) in group A and 116 in group B (48.3%). 78
patients belonged to the M group and 162 to the nM group.
Within group M, 21 patients were affected by VM (group                          to M was as follows: 3 patients (1.85%) in group nM and 9
VM/M) and 57 patients, on the contrary, did not meet the di-                    patients (11.5%) in group M. In the latter, the distribution
agnostic criteria for VM (group nVM/M). The patients who                        of PPPD with reference to VM was as follows: 3 patients
reported RD were 97 (40.4%) at the 2nd control. 34 of these                     (5.26%) in the nVM/M group and 6 (28.6%) patients in the
patients continued to report RD on the 3rd control. 12 of the                   VM/M group. Chi-square test showed a significant increase
240 patients recruited met the diagnostic criteria for PPPD                     of PPPD diagnosis in group M compared to group nM
for an overall incidence of 5% (Fig. 2). In any case, the diag-                 (p = 0.0016). With Yates correction the p-value is 0.0046,
nosis of PPPD concerned patients who reported RD during                         thus significant at p < 0.05. Within group M there was a
the 2nd and 3rd control. Within these, the incidence of the                     significant increase in PPPD in group VM/M compared to
PPPD was 12.4% (12/97) and 35.3% (12/34), respectively                          group nVM/M. The chi-square statistic test is 7.22556391.
(Fig. 2). This difference is significant (p < 0.05) both by                     The p-value is 0.0072, and significant at p < 0.05. Even with
the chi-square test alone (p = 0.000000272) and by the chi-                     Yates correction (5.35) the p-value is 0.021. Equally very
square test with Yates correction (p = 0.000001353). In 10                      significant was the increase in the incidence of PPPD in the
cases (8.1%), the diagnosis of PPPD concerned group A and                       VM/M group compared to the nM group with or without
in 2 cases (1.72%) patients in group B. The chi-square test                     Yates correction (p < 0.000003). No significant difference
(p = 0.040) showed a significantly higher incidence of PP-                      emerged from comparison with the chi-square test be-
PD in group A compared to group B (p < 0.05). The distri-                       tween group nM and group nVM/M (p > 0.05). 4 patients
bution of PPPD within the groups considered with reference                      (7.7%) belonging to the VM/ nPPV group (control group)
                                                                                met the diagnostic criteria for PPPD (Fig. 3). In this group,
                                                                                the incidence of PPPD was significantly higher (p = 0,043)
                                                                                compared to the nM group (chi-square) and significantly
                                                                                lower (p = 0.03) compared to the VM/M group. No signifi-
                                                                                cant difference emerged between VM/nPPV and nVM/M
                                                                                (p > 0.05). The number of therapeutic sessions necessary
                                                                                to obtain the resolution of PPV was 1.54 ± 0.87. No signifi-
                                                                                cant difference (p > 0.05) emerged between patients fulfill-
                                                                                ing PPPD criteria (1.56 ± 0.76) and those not fulfilling it
                                                                                (1.53 ± 0.71) (Tab. II).

                                                                                Discussion
                                                                                The data from our study confirms that the vertigo attacks
Figure 2. Incidence of persistent postural perceptual dizziness (PPPD) in all   that characterise the PPV can constitute precipitating con-
groups.                                                                         ditions that precede the PPPD 18, although the overall inci-



266
                                                                                                                              PPPD following PPV




Table II. The incidence of persistent postural perceptual dizziness (PPPD) within the groups examined.
 Groups                                                          PPPD               % PPPD           χ2 (chi- square value)   p value (< 0.05)
 Group A                                                         10               8.10%                      4.82                  0.04
 Group B                                                          2               1.72%
 Group M                                                          9              11.50%                      9.88                 0.0016
 Group nM                                                         3               1.85%
 Group VM/M                                                       6              28.60%                      7.22                 0.0072
 Group nVM/M                                                      3               5.26%
 Group VM/M                                                       6              28.60%                     26.99              0.00000020
 Group nM                                                         3               1.85%
 Group nVM/M                                                      3               5.26%                      1.79                  0.18
 Group nM                                                         3               1.85%
 Group VM/nPPV (control group)                                    4               7.70%                      4.76                  0.03
 Group VM/M                                                       6              28.60%
 Group VM/nPPV (control group)                                    4               7.70%                      4.11                  0.043
 Group nM                                                         3               1.85%
 Group VM/nPPV (control group)                                    4               7.70%                      0.25                  0.62
 Group nVM/M                                                      3               5.26%
 Group RD 2nd control                                            97              12.40%                      26.4              0.00000027
 Group RD 2nd and 3rd control                                    34              35.30%



dence is low. However, some features are worthy of further                      of PPPD. The main goal of our study was to verify the in-
analysis. First of all, the incidence of PPPD is more relevant                  fluence of migraine as a trigger for the PPPD onset, fol-
when referring to post-PPV RD. Although repositioning                           lowing vertigo attacks induced by cupulo-canalolithiasis.
procedures are usually very effective in improving vertigo,                     For this purpose, we investigated patients affected by PPV
some patients report, for a certain period afterward, imbal-                    and migraine, with or without VM. It should be noted that
ance without positional vertigo, named RD. The pathogen-                        patients suffering from VM have different clinical features
esis of the RD is still debated 19,20. In most cases there is                   from those with PPV with or without migraine. At the same
a spontaneous resolution in a variable time, from days to                       time, however, migraine seems to condition a higher inci-
weeks 21, which is also confirmed by our study. In presence                     dence of PPV 14 and VM undeniably accounts for a large
of long-term dizziness, when PPPD is suspected, the diag-                       share in migraine women 11. Therefore, it is common to
nosis can be made by targeted and accurate medical history,                     find patients with migraine presenting distinct episodes of
and investigating the elements that meet the diagnostic cri-                    PVV or attacks of VM over the course of their life. As-
teria. The diagnosis of PPPD concerned patients who re-                         suming a greater involvement of the vestibular system in
ported a dizziness of at least three months, after resolution                   these patients, they represent an ideal study group in which
of a PPV episode, representing 30% of these cases. Another                      to test the influence of migraine in the induction of PPPD
interesting aspect concerning the natural history of the PPV                    after PPV. On the other hand, a control study was carried
is that the PPPD mainly involved patients who had the first                     out with a group of patients suffering from VM without
episode of PPV. This probably represents a completely new                       previous or current history of PPV. The data from the study
experience for the patient, with a strong emotional impact.                     clearly indicate a significant role of migraine in its glo-
In recurrent PPV, on the contrary, the patient undergoes a                      bality. In particular, patients who suffer from VM appear
weaker surprise effect and appears more reassured in case                       to be more prone to the pathogenetic mechanism triggered
of recurrence of the vertigo. Moreover, being aware of the                      by migraine that lead to PPPD. In other words, migraine
symptom and its modality of appearance, the patient tends                       alone does not seem to exert a significant influence, but a
to avoid critical situations and movements capable of caus-                     concomitant weakness of the vestibular system is required.
ing vertigo. On the contrary, a greater resistance to thera-                    To confirm this finding is the evidence of a significantly
peutic manoeuvres, expressed by the number of sessions                          higher incidence of PPPD in VM/ nPPV group compared
that are necessary to obtain the resolution of the nystagmus,                   to nM group, which in turn is not different from the nVM/
does not imply a favourable condition for the appearance                        Mgroup. If patients who suffer from VM have a higher



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P. Tropiano et al.




probability of experiencing PPPD, there is no doubt that in       a visual dependence has also been hypothesised in PPV in
these patients the probability of experiencing PPPD is even       the phases following the disappearance of the nystagmus 26,
higher if there is a concomitant PPV. The appearance of a         it is reasonable to assume that this may be responsible for
vertigo with different characteristics from those to which        many cases of RD with spontaneous resolution, while a fur-
the patient suffering from VM is used to, probably consti-        ther evolution towards the PPPD requires enhancement of
tutes an element of novelty and alarm that is able to trigger     the same by migraine mechanisms.
a new condition of uncertainty that leads to PPPD. Several
mechanisms could explain this diversity.                          Conclusions
Referring to the definition of PPPD, there are two aspects
that emerge from the literature: anxiety and visual depend-       PPPD may be precipitated by PPV, especially following the
ence. Previous studies have indicated the importance of           first crises. Careful anamnestic history aimed at identify-
anxious personality traits as possible risk factors 6. Two ele-   ing the diagnostic criteria of PPPD is required in patients
ments show relevant importance for the initial pathological       with long-term post-PPV RD. The presence of VM appears
response: a high level of anxiety and a mental status char-       to significantly increase the incidence of PPPD in patients
acterised by an exaggerate vigilance towards acute symp-          with PPV. Anxiety and visual dependence, worsened by
toms generated by the precipitating events of PPPD 1,4. In        migraine, may be the main factors that increase this risk.
1995, Bronsteim described the symptom of VV in a portion
of patients in his tertiary otoneurologic clinic 8. People with   References
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