Quality of care provided by Multiple Sclerosis Centers during Covid-19 pandemic: Results of an Italian multicenter patient-centered survey

Abstract

Background:
Covid-19 pandemic impacted on management of people with Multiple Sclerosis (pwMS). Level of satisfaction of pwMS regarding the care received by the staff of Multiple Sclerosis Centers (MSCs) during the pandemic was not fully investigated. In a large patient-centered multicenter study, the therapeutic adherence and quality of care of MSCs was assessed.

Methods:
In April-May 2021, an online survey was widespread by 16 Italian MSCs. Frequencies, percentages and/or means and standard deviations were calculated to describe the sample. ANOVAs were performed to evaluate the effect of sociodemographic and clinical variables on overall pwMS' rating of MSC assistance.

Results:
1670 pwMS completed the survey (67.3% women). During the pandemic, 88% did not change their disease modifying therapy schedule, and 89.1% reached their MSCs with no or little difficulties. Even if only 1.3% of participants underwent a tele-health follow-up visit with their MSC staff, the 80.1% believed that tele-health services should be improved regardless of pandemic. 92% of participants were satisfied of how their MSC took charge of their needs; ANOVAs revealed an effect of disease duration on pwMS' level of satisfaction on MSCs management during the pandemic.

Conclusions:
The results revealed an efficient MSCs response to Covid-19 pandemic and provided the basis for the implementing of tele-health services that would further improve the taking charge of patients, particularly those with longer disease, higher disability, and/or living far from their MSC.

Full text

Multiple Sclerosis and Related Disorders 77 (2023) 104870
2211-0348/© 2023 The Author(s). Published by Elsevier B.V. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).
Quality of care provided by Multiple Sclerosis Centers during Covid-19
pandemic: Results of an Italian multicenter patient-centered survey
Manuela Altieri
a
, Rocco Capuano
a
, Alvino Bisecco
a
, Alessandro d’Ambrosio
a
, Mario Risi
a
,
Paola Cavalla
b
, Marco Vercellino
b
, Pietro Annovazzi
c
, Mauro Zaffaroni
c
, Nicola De Stefano
d
,
Maria Laura Stromillo
d
, Emanuele D’Amico
e
, Aurora Zanghì
e
, Maria Chiara Buscarinu
f
,
Roberta Lanzillo
g
, Giovanna De Luca
h
, Massimiliano Calabrese
i
, Lorena Lorece
j
,
Massimiliano Di Filippo
k
, Paola Valentino
l
, Alberto Gajofatto
i
, Girolama Alessandra Mara
m
,
Aurora Fuiani
n
, Viviana Nociti
o
, Gioacchino Tedeschi
a
, Antonio Gallo
a
,
*
a
Multiple Sclerosis Center, Dept. of Advanced Medical and Surgical Sciences, University of Campania “Luigi Vanvitelli”, Naples, Italy
b
Dept. of Neuroscience and Mental Health, City of Health and Science University Hospital of Torino, Turin, Italy
c
Multiple Sclerosis Study Center, ASST Valle Olona, Gallarate, VA, Italy
d
Dept. of Medicine, Surgery and Neuroscience, University of Siena, Siena, Italy
e
Multiple Sclerosis Center, G.F. Ingrassia, University of Catania, Catania, Italy
f
Dept. of Neuroscience, Mental Health and Sensory Organs, Sapienza University, S. Andrea Hospital-site, Rome, Italy
g
Multiple Sclerosis Clinical Care and Research Centre, Dept. of Neuroscience, Reproductive Science and Odontostomatology, Federico II University of Naples, Naples,
Italy
h
Multiple Sclerosis Center, Policlinico SS. Annunziata, Chieti, Italy
i
Multiple Sclerosis Center, Dept. of Neuroscience, Biomedicine and Movement Sciences, University Hospital of Verona, Verona, Italy
j
Multiple Sclerosis Center, Dept. of Medical Sciences and Public Health, Binaghi Hospital, ASL Cagliari, University of Cagliari, Cagliari, Italy
k
Section of Neurology, Dept. of Medicine and Surgery, University of Perugia, Perugia, Italy
l
Institute of Neurology, University of Catanzaro “Magna Graecia”, Catanzaro, Italy
m
Dysimmune Neuropathies Unit, Dept. of Systems Medicine, Tor Vergata University of Rome, Rome, Italy
n
Dept. of Neuroscience, Riuniti Hospital of Foggia, Foggia, Italy
o
Institute of Neurology, Fondazione Policlinico Universitario “A. Gemelli”, IRCCS, Universit`
a Cattolica del Sacro Cuore, Rome, Italy
ARTICLE INFO
Keywords:
Multiple Sclerosis
Covid-19
Multiple Sclerosis Center
Patient centered study
Patient satisfaction
ABSTRACT
Background: Covid-19 pandemic impacted on management of people with Multiple Sclerosis (pwMS). Level of
satisfaction of pwMS regarding the care received by the staff of Multiple Sclerosis Centers (MSCs) during the
pandemic was not fully investigated. In a large patient-centered multicenter study, the therapeutic adherence
and quality of care of MSCs was assessed.
Methods: In April–May 2021, an online survey was widespread by 16 Italian MSCs. Frequencies, percentages and/
or means and standard deviations were calculated to describe the sample. ANOVAs were performed to evaluate
the effect of sociodemographic and clinical variables on overall pwMS’ rating of MSC assistance.
Results: 1670 pwMS completed the survey (67.3% women). During the pandemic, 88% did not change their
disease modifying therapy schedule, and 89.1% reached their MSCs with no or little difculties. Even if only
1.3% of participants underwent a tele-health follow-up visit with their MSC staff, the 80.1% believed that tele-
health services should be improved regardless of pandemic. 92% of participants were satised of how their MSC
took charge of their needs; ANOVAs revealed an effect of disease duration on pwMS’ level of satisfaction on MSCs
management during the pandemic.
Conclusions: The results revealed an efcient MSCs response to Covid-19 pandemic and provided the basis for the
implementing of tele-health services that would further improve the taking charge of patients, particularly those
with longer disease, higher disability, and/or living far from their MSC.
* Corresponding author.
E-mail address: antonio.gallo@unicampania.it (A. Gallo).
Contents lists available at ScienceDirect
Multiple Sclerosis and Related Disorders
journal homepage: www.elsevier.com/locate/msard
https://doi.org/10.1016/j.msard.2023.104870
Received 16 November 2022; Received in revised form 28 June 2023; Accepted 4 July 2023

Multiple Sclerosis and Related Disorders 77 (2023) 104870
2
1. Introduction
Covid-19 was considered a Public Health Emergency of International
Concern on January 30, 2020, and it rapidly spread all over the world,
being declared a pandemic by the World Health Organization on March
11, 2020 (WHO, 2020). To avoid and slow down the spreading of
Sars-CoV-2 and to make room for the necessary expansion of basic
healthcare and intensive care unit capacities (Goyal et al., 2021), most
of governments imposed access restrictions to the national health sys-
tems (NHS), except for non-deferrable clinical conditions.
Therefore, since the rst lockdown of early 2020, these restrictions
caused a reduction on volume of hospitalizations and accesses in several
essential clinical areas of NHS (Spadea et al., 2021). Neurology de-
partments were also impacted by Covid-19 pandemic, as reported by a
global survey that revealed a mild-to-complete disruption of neurolog-
ical community-based services, long-term residential care, interventions
for caregivers and neurorehabilitation (García-Azorín et al., 2021; Moss
et al., 2020). This might have had an impact on management of people
with chronic neurological diseases such as Multiple Sclerosis (MS) who
need regular visits and additional care for relapses, disease progression,
symptoms management and /or psychological support. In fact, studies
focusing on possible changes in treatment and management during the
Covid-19 pandemic of people with MS (pwMS) reported a signicant
reduction or delay in visits, access to MRI, laboratory tests and clinical
trial activity; moreover, changes in modalities of visits were imple-
mented, with an increase of tele-health services to overcome these dif-
culties (Portaccio et al., 2022; Chen et al., 2022).
The current literature on this topic, however, has not taken into
account the level of satisfaction of pwMS regarding the healing/care
received as well as information on Covid-19 provided by their neurol-
ogists and the staff of Multiple Sclerosis Centers (MSCs) after one year of
pandemic. Given the importance of setting the standard of care of MSCs
also considering the opinion of patients, the aim of the present patient-
centered outcome study was to assess, in a large sample of pwMS, by
means of a digital survey: (i) the impact of Covid-19 pandemic on access
to (and care of) MSC; (ii) disease modifying therapy (DMT) changes
during pandemic; (ii) the point of view of pwMS on psychological and/
or tele-health services; (iii) the overall satisfaction/rating of MSCs pro-
vided by pwMS after one year of Covid-19 pandemic.
2. Materials and methods
Between April and May 2021, an online survey developed on Google
Forms was widespread to a very large sample of pwMS throughout Italy.
Sixteen Italian MSCs agreed to participate in the study and sent the
survey to their MS patients; the complete list of MSCs involved is re-
ported in Table 1. The survey included items aimed at collecting:
I Socio-demographic and clinical characteristics (sex, age, referral
MSC, disease duration and course, ambulatory capability) of
pwMS.
II Data about Covid-19 infection (including impact on MS symp-
toms) and vaccination.
III Type/frequency of contacts with MSC since the start of Covid-19
pandemic in Italy (March 2020).
IV DMT management during the Covid-19 pandemic.
V Degree of satisfaction with MSCs activities and contacts during
the Covid-19 pandemic.
VI Opinions on psychological and tele-health services activated
during the Covid-19 pandemic.
All participants were informed on the purposes of the study and
agreed to complete the survey. The study was approved by Ethical
Committee of University of Campania “Luigi Vanvitelli” and it was
carried out in accordance with the Code of Ethics of the World Medical
Association (Declaration of Helsinki).
2.1. Statistical analyses
Descriptive analyses were performed by calculating frequencies,
percentages and/or means and standard deviations as appropriate. Pie
charts were generated to facilitate the readability of the results.
Aggregated data from all MSCs were considered.
Frequencies of Covid-19 infection, types of Covid-19 treatment, and
worsening of MS-related neurological symptoms during and after Covid-
19 infections were compared between pwMS on different DMTs by
means of chi square test. A comparison was performed on the following
groups: (a) pwMS under no DMTs, pwMS on anti-CD20 DMTs (Ocreli-
zumab and Rituximab), and pwMS on other DMTs; (b) participants
under no DMTs, on rst line and second line DMTs.
Moreover, several univariate analyses of variance (ANOVA) were
performed to evaluate the effect of sociodemographic and clinical var-
iables on overall pwMS’ rating of MSCs assistance, with pwMS’ rating of
MSC as dependent variable, and sex, age, geographical localization of
MSC, disease duration and ambulation capability added as independent
variables. Independent variables were added as categorical variables in
the following way: I. sex: men and women; II. age: young adults (18–35
years), adults (36–64 years), older adults (65+years); III. geographical
localization of MSCs: Northern Italy MSCs, Central Italy MSCs, Southern
Italy MSCs; IV. disease duration: short (<2 years), medium (3–5 years)
and long disease duration (≥6 years); V. ambulation capability: high
(pwMS who were able to walk without any limitations or more than 100
m without experiencing fatigue and without assistive devices), moderate
(pwMS who were able to walk without less than 100 m or needing as-
sistive devices, such as canes, crutches, walkers for most of the day) and
low-absent (pwMS on wheelchair) ambulation capability; VI. MS phe-
notypes: relapsing remitting MS, primary progressive MS, and secondary
progressive MS; VII. types of DMTs (no DMTs, rst line DMTs, second
line DMTs).
Finally, in pwMS who underwent a tele-health follow-up visit with
their MSC staff, the possible association between going to a tele-health
follow-up visit and socio-demographic and clinical variables was
assessed by means of chi square test. Socio-demographic and clinical
variables were coded as stated in the previous paragraph. Statistical
analyses were carried out with SPSS, version 25.
3. Results
3.1. Characteristics of the sample
A total number of 1670 pwMS completed the survey (see Table 2;
Table 1
Number of participants for each Italian Multiple Sclerosis Center (MSC).
MSC pwMS enrolled by MSC
(N)
Cagliari – Sardegna, Ospedale Binaghi 73
Catania – AOU Policlinico “G. Rodolico – San Marco” 108
Catanzaro – Universit`
a Magna Graecia 60
Chieti – Policlinico SS. Annunziata 90
Foggia – Ospedali riuniti di Foggia 44
Gallarate – ASST Valle Olona 210
Napoli – AOU “Federico II” 90
Napoli – AOU “Luigi Vanvitelli” 269
Perugia – Universit`
a degli Studi di Perugia 62
Roma – Policlinico Universitario “A. Gemelli” 43
Roma – Policlinico Tor Vergata (PTV) 50
Roma – Ospedale S. Andrea 96
Siena – Universit`
a di Siena 111
Torino – AOU Citt`
a della Salute e della Scienza
“Molinette”
228
Verona – AOUI, Borgo Roma 136
Notes. MSC =Multiple Sclerosis Center; pwMS =people with Multiple Sclerosis.
M. Altieri et al.

Multiple Sclerosis and Related Disorders 77 (2023) 104870
3
34.4%, 21.7% and 44% of the sample were from northern, central, and
southern Italy, respectively). The percentage of women in the whole
sample was 67.3%; 17.5% did not reach a high school diploma, whereas
50.4% possessed a high school diploma and 32.1% attended college.
Mean age at onset was 29.9 years, whereas the mean age at diagnosis
was 32.5 years. High ambulation capability was reported by 81.7% of
participants. As for DMT usage, 10.2% of the sample was not under
DMTs, 34.6% was on rst line DMTs, and 55.1% was on second line
DMTs; among participants who were on DMTs, dimethyl fumarate
(18.6%), ocrelizumab (14.4%) and natalizumab (13.9%) were the most
used DMTs.
3.2. Covid-19 infection and vaccines
Of the whole sample, 10.2% reported a diagnosis of Covid-19
infection (78.8% conrmed by a nasopharyngeal swab, 21.2% by a
general practitioner because of clinical presentation). In our sample, the
comparison between participants under no DMTs, on rst line and sec-
ond line DMTs on frequency of Covid-19 infection revealed no signi-
cant differences (
χ
2
=4.133, df =3, p =.127). Moreover, people on anti-
CD20 therapies (Ocrelizumab and Rituximab) were not more likely to be
affected by Covid-19 when compared to people on other DMTs (
χ
2
=
4.81, df =1, p =.488).
An asymptomatic course of Covid-19 was reported by 37% of pa-
tients who reported a Covid-19 diagnosis, whereas one or more symp-
toms suggestive of Covid-19 (dry cough, fever >37.5 ◦C, anosmia and/
or ageusia, new onset of muscle pain, asthenia) were reported by the
remaining 63%. At the time of the survey, 0.8% of the whole sample was
still tested positive for Covid-19.
As regards treatment for Covid-19, 50% of the patients stated that
they did not carry out any treatment, 37.2% took medications prescribed
by a doctor (e.g., antibiotics, corticosteroids, NSAIDs), 9.7% only took
supplements, multivitamins, or homeopathic remedies and only 3%
were hospitalized.
As for the impact of Covid-19 infection on MS-related neurological
symptoms, 69.3% of the patients stated that they remained stable,
whereas 21.5% reported a worsening of existing symptoms, 7.4%
afrmed that new neurological symptoms emerged, while only 1.8%
reported an improvement. Types of DMTs (anti-CD20 vs other DMTs vs
no DMTs:
χ
2
=15.900, df =10, p =.103; second line DMTs vs rst line
DMTs vs no DMTs:
χ
2
=6.165, df =10, p =.801) were not statistically
linked to a higher frequency of worsening or improvement of neuro-
logical symptoms.
At the time of the survey (April-May 2021), 60.6% of the patients
was inoculated at least one dose of Covid-19 vaccine. As shown in Fig. 1,
vaccination appointments were scheduled by MSC staff (44.9%), MSC
staff together with the general practitioner (17.5%), the general prac-
titioner alone (16.1%), or other institutions (12.1%; i.e., local health
authority and/or the Italian Multiple Sclerosis Association, AISM;), and
by themselves (9.3%). Among participants who did not receive any
doses of Covid-19 vaccine (39.4%), 40.8% had already booked an
appointment and were going to be vaccinated in the next few days/
weeks, 17.6% was willing to be vaccinated but they did not book an
appointment yet, while 19.3% was still undecided or they did not want
to be vaccinated at all. Full reasons for not being vaccinated yet are
reported in Fig. 1.
3.3. Changes in DMT compliance
Among participants who were on DMT (89.9%; 1501/1670) at the
beginning of the pandemic outbreak, 88% did not change their DMT
schedule, 7.8% reduced/delayed the intake of their DMT, and only the
4.2% skipped all scheduled doses of DMT during the Covid-19 outbreak.
Table 2
Socio-demographic and clinical characteristics of the sample.
Whole
sample
(N=
1670)
pwMS
from
northern
Italy
MSCs
(N=574)
pwMS
from
central
Italy
MSCs
(N=362)
pwMS
from
southern
Italy
MSCs
(N=734)
Age
a
42.9
(12.1)
46.4
(11.5)
43.3
(11.2)
40.1
(12.3)
Sex (Women)
b
67.3 69.3 72.5 63.2
Educational
attainment
b
No
qualication
0.4 0.2 0.6 0.5
Elementary
education
0.3 0.2 0 0.5
Inferior
middle license
16.8 21.3 9.1 17
High school
diploma
50.4 47.7 50.8 52.3
Bachelor’s
degree
10.4 8.7 11.6 11
Master’s
degree or
more
21.7 22 27.9 18.5
Age at onset
a
29.9
(10.7)
30.8
(11.3)
30.9
(10.2)
28.8
(10.3)
Age at diagnosis
a
32.5
(11)
33.7
(11.2)
32.9
(10.5)
31.2 (11)
Phenotype
b
RRMS 76.3 73.5 75.7 78.9
PPMS 10.8 11.7 11 9.9
SPMS 12.9 14.8 13.3 11.2
Ambulation
capability
b
High 81.7 81.2 80.9 82.4
Moderate 14.9 15 13.8 15.3
Low-absent 3.5 3.8 5.2 2.3
DMT
b
No therapy 10.1 8.7 14.1 9.5
Alemtuzumab 2.1 2.8 1.9 1.6
Azathioprine 0.6 0.5 0.9 0.3
Cladribine 3.1 2.1 3.9 3.5
Dimethyl-
fumarate
18.6 15.7 21.3 19.5
Fingolimod 13.4 13.2 10.8 14.9
Glatiramer
acetate
6.6 7.3 6.9 6
Interferon
beta
7.2 7.3 6.4 7.2
Natalizumab 13.9 15 10.8 14.7
Ocrelizumab 14.4 15.9 14.9 12.9
Ponesimod 0.1 0.2 0 0
Rituximab 1.4 1.9 1.7 0.8
Siponimod 0.5 0.2 0.6 0.7
Teriunomide 8 9.2 5.5 8.3
Symptomatic
treatment
b
No therapy 60 56.6 65.5 61.3
Yes, for
anxiety
7.2 6.6 7.2 7.8
Yes, for
depression
8.8 9.2 6.1 9.8
Yes, for
insomnia
8.7 10.5 6.4 8.6
Yes, for
fatigue
8.5 10.1 7.5 7.8
Yes, for
spasticity
11.7 14.5 10.8 10.1
Yes, for sexual
dysfunction
1.7 2.1 3 0.7
Yes, for
bowel/
bladder
dysfunction
8.3 11 8.6 6
Yes, for pain/
sensitive
disorders
11.5 12.4 11.9 10.8
Yes, but I
don’t know
why
0.9 0.9 1.1 0.8
Notes. pwMS =patient with Multiple Sclerosis; MSC =Multiple Sclerosis Center;
RRMS =Relapsing-Remitting Multiple Sclerosis; PPMS =Primary Progressive
Multiple Sclerosis; SPMS =Secondary Progressive Multiple Sclerosis; DMT =
Disease-modifying therapy.
a
=data reported as mean (standard deviation).
b
=data reported as %.
M. Altieri et al.

Multiple Sclerosis and Related Disorders 77 (2023) 104870
4
Participants reducing/discontinuing DMT during Covid-19 pandemic
did so for the following main reasons (see also Fig. 2): advice by their
MSC neurologist (47.5%), forgetting to take their DMT (11.9%), and
presence of co-pathologies that required a delay and/or stop of current
DMT (i.e., cancer) (10.9%).
3.4. Contacts and access to MSC
More than two thirds of the sample (68.3%) reported contacts with
their MSC or general practitioner regarding information and advice
about Covid-19 pandemic and disease as well as prophylactic behaviors
and vaccination. Specically, 35.7% of the patients contacted directly
the MSC, whereas 29.6% declared to have been contacted by the MSC
staff.
Almost 9 out of 10 pwMS (89.1%) were able to reach their MSC with
no or little difculties (see Fig. 3). During the pandemic, almost all
participants (68.6%) reported exchanges of information between
themselves and MSC staff with at least one of the following means of
communication: phone calls, messaging programs, emails, face-to-face
encounters, tele-health software (see Fig. 3). The most recurrent
means of communication included emails (68.6%), phone calls (59.3%)
and messaging programs (24.9%). Face-to-face encounters and visits
with tele-health software were reported by only 1.4% and 1.3% of
participants, respectively.
As regards the frequency of routine visits at MSC: (i) more than half
of the sample (63.5%) performed their check-up visits at the MSC with
the same frequency/schedule as the pre-pandemic period; (ii) 24.2% of
the sample stated that there were some derangement/difculties in their
check-up visits due to the impossibility of MSC to provide scheduled
follow-up visits, whereas (iii) 12.3% of the patients personally choose to
skip at least one scheduled visit (see Fig. 2).
Main reasons for voluntary skipping follow-up visits at MSC regarded
fear of getting Covid-19 (46%) and the sensation of feeling well without
absolute/urgent need of a check-up visit (16.8%; see also Fig. 2).
3.5. Tele-health services
As reported above, only 1.3% of participants underwent a tele-health
follow-up visit with their MSC staff by means of specic software during
the Covid-19 pandemic. Chi-square test showed that there was no sig-
nicant association between going to a tele-health follow-up visit and
sex (
χ
2
=0.004, df =1, p =0.947), geographical localization of MSC (
χ
2
=3.958, df =2, p =0.138), age (
χ
2
=1.065, df =2, p =0.587),
ambulation capability (
χ
2
=1.525, df =2, p =0.467), disease course (
χ
2
=5.046, df =2, p =0.08), and types of DMTs (
χ
2
=0.115, df =2, p =
0.944).
Fig. 1. Vaccination appointments and reasons for not being vaccinated against Covid-19.
Fig. 2. Disease modifying therapy (DMT) discontinuation.
M. Altieri et al.

Multiple Sclerosis and Related Disorders 77 (2023) 104870
5
All participants, regardless of whether they underwent a tele-health
follow-up visit with their MSC, were asked an opinion about utility of
tele-health services; the 80.1% of the sample believed that tele-health
services should be improved and that they could be a very useful tool
to perform follow-up visits (see Fig. 4).
3.6. Psychological services
75.2% of the sample was not aware if a remote/live psychological
service was available at their MSC during the Covid-19 pandemic. Only
4.6% of participants attended a live (1.5%) or remote (3.1%) psycho-
logical service (see Fig. 4). Among participants who took psychological
support sessions, 90.6% found the psychological sessions very or fairly
useful; instead, the 69.5% of people who not attended or were not aware
of the presence of a psychological service reported that it would have
been useful (see Fig. 4).
3.7. Overall satisfaction/rating of MSC during the Covid-19 pandemic
About 92% percent of participants reported to be very or fairly
satised of how their MSC took charge of their requests or needs during
the pandemic (see Fig. 5). The overall patients’ opinion regarding the
assistance provided by their MSC during Covid-19 outbreak was stable
(61.3%) or became more positive (31.9%). Contrariwise, only 6.8% of
the sample stated that they lost condence (fully or partially) in their
MSC (see Fig. 5).
The ANOVAs aimed at exploring whether sociodemographic/clinical
variables could predict the overall pwMS’ rating of MSC assistance
Fig. 3. Contacts with Multiple Sclerosis Centers (MSC) during Covid-19 pandemic.
Fig. 4. Psychological and telemedicine services during Covid-19 pandemic.
M. Altieri et al.

Multiple Sclerosis and Related Disorders 77 (2023) 104870
6
revealed a signicant effect of disease duration (F
(1667,2)
=7.190, p =
0.001) on pwMS’s overall rating of MSC, whereas sex (F
(1662,1)
=0.310,
p =0.578), geographical localization of MSC (F
(1667,2)
=1.141, p =
0.320), age (F
(1667,2)
=0.093, p =0.912), ambulation capability
(F
(1667,2)
=2.051 p =0.129), disease course (F
(1667,2)
=1.971, p =
0.140) and types of DMTs (F
(1667,2)
=0.611, p =0.543) were not sig-
nicant. Post-hoc Bonferroni corrected analyses revealed that pwMS
with a disease duration <2 years (X‾=3.58,
σ
=0.94) reported a sig-
nicant higher rating with respect to pwMS with a disease duration>6
years (X‾ =3.36,
σ
=0.885).
4. Discussion
The present study explores not only possible changes in management
and access to MSCs, but also the level of satisfaction of pwMS towards
clinical and management activities carried out by MSCs during the rst
year of Covid-19 pandemic according to a patient-centered perspective
and by employing a large sample of pwMS.
The results revealed that pwMS judged globally well the care and
information received by their MSCs during Covid-19 pandemic. In
particular, pwMS declared that MSCs were able to keep a high quality of
care and to provide information about protective behavior against
Covid-19 as well as support with Covid-19 vaccination. This nding may
highlight that, although the rst year of pandemic was characterized by
extreme uncertainty and access restrictions to healthcare facilities
(24.2% of the sample reported to have skipped at least one follow-up
visit due to reduced access to MSCs), MSCs were able to maintain an
adequate standard of care remaining in constant close contact, through
multimodal channels (telephone, emails, and messaging services), with
their patients. These results may also provide evidence of a quick
organizational response to the public health emergency of the well-
established Italian MSCs network. In fact, despite all pandemic re-
strictions and disruptions MSCs tried to preserve the patient-provider
relationship, which is a fundamental element for maintaining
Fig. 5. Levels of satisfaction of Multiple Sclerosis Centers (MSC) support during Covid-19 pandemic and changes in levels of trust.
M. Altieri et al.

Multiple Sclerosis and Related Disorders 77 (2023) 104870
7
treatment adherence and quality of life (Costello et al., 2008; Rieck-
mann et al., 2015).
In fact, when investigating DMT changes during Covid-19 pandemic,
most of pwMS from this sample did not change/stop their DMT intake,
and only 4% reported to have done so due to fear of possible collateral
effects or worries related to Covid-19 pandemic. It is possible that this
high treatment adherence might have been also supported by keeping a
consistent contact with pwMS, and by providing them with all available
information about Covid-19 and DMT. Current evidence on DMT
changes during the pandemic are discordant, with some studies
reporting slightly higher percentages on patients’ decision on dis-
continuing their DMT (e.g., 14.3% in Chertcoff et al. 2021 study),
whereas other surveys - investigating the MS specialist approach to DMT
prescription during the Covid-19 pandemic - revealed a higher rate of
DMTs switch during the pandemic period (Portaccio et al., 2022; Mor-
rison et al., 2021). This discrepancy may be ascribed to different study
design and heterogeneous geographic provenience of the samples. As
regards routine monitoring visits, our nding of 36.5% of missed visits is
in line with a previous study that revealed that 38 to 50% pwMS re-
ported missing or canceling an appointment or delays (Chen et al.,
2022). When investigating Covid-19 infection and related outcomes, we
also found that the type of DMT did not predict a higher rate of Covid-19
infection or negative outcomes in our sample. These analyses compared
pwMS on rst, second line DMT and no DMT; moreover, due to the
evidence that pwMS on anti-CD20 monoclonal antibodies may be at
higher risk of severe Covid-19 outcomes (Simpson-Yap et al., 2021;
Landtblom et al., 2021), an additional analysis was performed to
compare pwMS on anti-CD20 therapies (i.e., people on Ocrelizumab or
Rituximab), people on other DMTs, and pwMS with no pharmacological
therapy. However, in each analysis no differences were found between
groups. The inconsistency between our results and previous studies may
be explained by differences in socio-demographic and clinical data (i.e.,
time elapsed from last infusion, levels of humoral and cellular immunity,
treatment duration) in the samples. Data collection regarding these
clinical aspects was beyond the scope of the present study, so it was not
possible to fully analyze these possible differences and this aspect should
be taken into account.
The only variable that seemed to inuence the judgment of pwMS on
level of assistance provided by MSC was the disease duration, with
newly diagnosed pwMS that reported higher levels of satisfaction with
respect to pwMS with longer disease duration, and this difference could
not be explained by different levels of ambulatory ability among pwMS,
since it did not have an impact on levels of satisfaction regarding the
MSC activities; although it is difcult to provide an explanation of this
result, it has to be noted that newly diagnosed pwMS had just few or no
contacts with their MSC before the pandemic (because they just received
MS diagnosis or they were not diagnosed yet), so it is possible that, based
on their experience - which was mostly related to the pandemic period -
they did not perceive a reduction on access to MSC or an increase of
disruption of neurological services. Another explanation of this nding
may be that, since in this sample pwMS with lower disease duration
were also signicantly younger and with higher ambulation ability than
those with higher disease duration, they may have been able to get in
touch more easily (i.e., by employing multiple contact channels) with
respect with older and more disabled pwMS with longer disease
duration.
Moving on to the challenging modalities of support provided by MSC
during the Covid-19 pandemic, such as tele-health services or psycho-
logical support, some differences emerged on tele-health services: in our
study, only 1.3% of pwMS underwent a routine visit by means of tele-
health software, whereas in other studies tele-health use was reported
by a signicantly larger number of participants (Chen et al. 2022:
61–62%; Keszler et al. 2021: 75.8%; McGinley et al. 2021: 90%; Por-
taccio et al. 2022: 92%). This discrepancy might be explained by the fact
that, in these studies, all types of electronic communication were
regarded as tele-health (i.e., email, messaging services, video-calls). On
the other hand, in this study, we considered and analyzed each contact
modality separately, and the frequency of use of specic tele-health
software was considered a distinct outcome. In fact, when we
compared frequencies of usage of specic tele-health software/video-
calls, the discrepancy reduced signicantly: for example, Portaccio et al.
(2022) reported a frequency of 4%. Interestingly, most of pwMS
believed that tele-health services should be further ameliorated to pro-
vide better care and management to MS patients, in line with other
studies (Landi et al., 2022). Preliminary studies on telemedicine for
pwMS during Covid-19 pandemic demonstrated that it can be an
effective and suitable care method for MS (Corea et al., 2021), it is well
accepted by pwMS (Chen et al., 2022) and it can be employed not only as
a temporary method of care, but as a permanent one, when the Covid-19
pandemic will end. Indeed, tele-health can be benecial to both patients
and MSC since it reduces access difculties for pwMS, increases pro-
tection from exposure to infectious agents, reduces costs of travel for
patients and it is associated with higher pwMS and caregivers’ satis-
faction (Hatcher-Martin et al., 2020, 2021). However, not all studies
found a signicant benecial effect of telemedicine programs. For
example, a recent study (Landtblom et al., 2019) reported a negative
result in terms of better adherence or better health-related quality of life
when comparing a tele-health program with standard technical support.
Moreover, some concerns were raised by some neurologists on the ef-
cacy of this type of medical care in MS and tele-health has been
considered more suitable for other neurological patients, i.e., people
with epilepsy or migraine (Landtblom et al., 2021). Our study found that
frequency of follow-up tele-health visit did not depend on any
socio-demographic and/or clinical variable; therefore, there was no
specic category of pwMS who was more likely to undergo a telemed-
icine visit. However, due to the small number of pwMS who experienced
a telemedicine visit in our sample, no denite conclusions should be
made. Instead, it should be interesting to evaluate this issue with larger
samples, and also to investigate which clinical and socio-demographic
variables may predict a better efcacy of tele-health services, and
which specic clinical activity may be carried on with a tele-health
approach. Furthermore, future studies may further explore this inter-
esting topic by evaluating the possible increase of percentages of usage
of tele-health software over time. Our study only investigated the rst
year of pandemic, and it is possible that, in the subsequent Covid-19
pandemic waves, MSCs arranged novel tele-health services.
As for psychological services that were active or activated during the
pandemic, most of pwMS were not informed on whether they were
available or not at the time of the survey. Although pwMS did not show
an increase of psychological distress after the Covid-19 outbreak (Altieri
et al., 2022), prevalence rates of depression and anxiety are higher in
pwMS than their healthy peers (Boeschoten et al., 2017) and access to
mental health services should be facilitated in pwMS, independently
from the pandemic. The results from our survey may prompt MSC staff
to better communicate the presence of live or remote psychological
services to their patients– if they are already available – or to organize
psychological programs at pwMS’ disposal. The access to psychological
services within MSC may help increasing patients’ resilience, quality of
life, and trust in their healthcare providers: in fact, it has been high-
lighted that pwMS are more satised if psychological interventions are
provided by mental health providers with expertise in MS and within
their MSC (Rintell et al., 2012).
Of course, the results of this study should be interpreted in light of
some limitations. For example, this study was on a voluntary basis, so a
selection bias could not be excluded; moreover, since our survey was
available online only, pwMS with limited access to the Internet could
have been underrepresented. Moreover, geographical localization was
not homogeneous, and so our sample could not have been fully repre-
sentative of Italian MS population. Finally, since the sample was
composed only by Italian pwMS, we could not assess possible differences
among European and extra-European countries and the results may not
be generalizable to pwMS living in other countries.
M. Altieri et al.

Multiple Sclerosis and Related Disorders 77 (2023) 104870
8
4.1. Conclusions
This multicentric survey has important implications for future
management of MS, revealing not only an efcient MSC response to
Covid-19 pandemic as regards pwMS management, but also providing
the basis for future developments and improvement of care services,
such as the implementing of remote psychological and tele-health ser-
vices that would further improve the taking charge of patients, partic-
ularly those with longer disease, higher disability, and/or living far from
their MSC.
CRediT authorship contribution statement
Manuela Altieri: Conceptualization, Data curation, Formal analysis,
Investigation, Methodology, Project administration, Validation, Visual-
ization, Writing – original draft, Writing – review & editing. Rocco
Capuano: Conceptualization, Data curation, Investigation, Methodol-
ogy, Writing – original draft, Writing – review & editing. Alvino
Bisecco: Investigation, Methodology, Writing – review & editing.
Alessandro d’Ambrosio: Investigation, Methodology, Writing – review
& editing. Mario Risi: Investigation, Writing – review & editing. Paola
Cavalla: Investigation, Writing – review & editing. Marco Vercellino:
Investigation, Writing – review & editing. Pietro Annovazzi: Investi-
gation, Writing – review & editing. Mauro Zaffaroni: Investigation,
Writing – review & editing. Nicola De Stefano: Investigation, Writing –
review & editing. Maria Laura Stromillo: Investigation, Writing – re-
view & editing. Emanuele D’Amico: Investigation, Writing – review &
editing. Aurora Zanghì: Investigation, Writing – review & editing.
Maria Chiara Buscarinu: Investigation, Writing – review & editing.
Roberta Lanzillo: Investigation, Writing – review & editing. Giovanna
De Luca: Investigation, Writing – review & editing. Massimiliano
Calabrese: Investigation, Writing – review & editing. Lorena Lorece:
Investigation, Writing – review & editing. Massimiliano Di Filippo:
Investigation, Writing – review & editing. Paola Valentino: Investiga-
tion, Writing – review & editing. Alberto Gajofatto: Investigation,
Writing – review & editing. Girolama Alessandra Mara: Investiga-
tion, Writing – review & editing. Aurora Fuiani: Investigation, Writing
– review & editing. Viviana Nociti: Investigation, Writing – review &
editing. Gioacchino Tedeschi: Investigation, Writing – review & edit-
ing. Antonio Gallo: Conceptualization, Investigation, Methodology,
Project administration, Supervision, Validation, Visualization, Writing –
review & editing.
Declaration of Competing Interest
The authors declare the following nancial interests/personal re-
lationships which may be considered as potential competing interests:
Antonio Gallo reports a relationship with Biogen that includes:
consulting or advisory, speaking and lecture fees, and travel reim-
bursement. Antonio Gallo reports a relationship with Merck Serono that
includes: consulting or advisory, speaking and lecture fees, and travel
reimbursement. Antonio Gallo reports a relationship with Mylan ITALIA
Srl that includes: consulting or advisory, speaking and lecture fees, and
travel reimbursement. Antonio Gallo reports a relationship with
Novartis that includes: consulting or advisory, speaking and lecture fees,
and travel reimbursement. Antonio Gallo reports a relationship with
Roche that includes: consulting or advisory, speaking and lecture fees,
and travel reimbursement. Antonio Gallo reports a relationship with
Sano Genzyme that includes: consulting or advisory, speaking and
lecture fees, and travel reimbursement. Antonio Gallo reports a rela-
tionship with Teva Health that includes: consulting or advisory,
speaking and lecture fees, and travel reimbursement. Lorena Lorece
reports a relationship with Biogen that includes: consulting or advisory
and speaking and lecture fees. Lorena Lorece reports a relationship
with Novartis that includes: consulting or advisory and speaking and
lecture fees. Lorena Lorece reports a relationship with Sano that
includes: consulting or advisory and speaking and lecture fees. Lorena
Lorece reports a relationship with Sano Genzyme that includes:
consulting or advisory and speaking and lecture fees. Lorena Lorece
reports a relationship with Merck Serono that includes: consulting or
advisory and speaking and lecture fees. Lorena Lorece reports a rela-
tionship with Teva Health that includes: consulting or advisory and
speaking and lecture fees. Lorena Lorece reports a relationship with
Almirall Ltd that includes: speaking and lecture fees. Alvino Bisecco
reports a relationship with Biogen that includes: consulting or advisory
and speaking and lecture fees. Alvino Bisecco reports a relationship with
Roche that includes: consulting or advisory and speaking and lecture
fees. Alvino Bisecco reports a relationship with Merck & Co Inc that
includes: consulting or advisory and speaking and lecture fees. Alvino
Bisecco reports a relationship with Celgene Corp Los Angeles that in-
cludes: consulting or advisory and speaking and lecture fees. Alvino
Bisecco reports a relationship with Sano Genzyme that includes:
consulting or advisory and speaking and lecture fees. Massimiliano
Calabrese reports a relationship with Biogen that includes: speaking and
lecture fees. Massimiliano Calabrese reports a relationship with Bristol
Myers Squibb that includes: speaking and lecture fees. Massimiliano
Calabrese reports a relationship with Celgene Corp Los Angeles that
includes: speaking and lecture fees. Massimiliano Calabrese reports a
relationship with Sano Genzyme that includes: speaking and lecture
fees. Massimiliano Calabrese reports a relationship with Merck Serono
that includes: speaking and lecture fees. Massimiliano Calabrese reports
a relationship with Novartis that includes: speaking and lecture fees.
Massimiliano Calabrese reports a relationship with Roche that includes:
speaking and lecture fees. Massimiliano Calabrese reports a relationship
with International Progressive MS Alliance that includes: funding
grants. Massimiliano Calabrese reports a relationship with Ministry of
Health that includes: funding grants. Massimiliano Di Filippo reports a
relationship with Bayer AG that includes: speaking and lecture fees and
travel reimbursement. Massimiliano Di Filippo reports a relationship
with Biogen Italy that includes: speaking and lecture fees and travel
reimbursement. Massimiliano Di Filippo reports a relationship with
Sano Genzyme that includes: speaking and lecture fees and travel
reimbursement. Massimiliano Di Filippo reports a relationship with
Merck & Co Inc that includes: speaking and lecture fees and travel
reimbursement. Massimiliano Di Filippo reports a relationship with
Mylan ITALIA Srl that includes: speaking and lecture fees and travel
reimbursement. Massimiliano Di Filippo reports a relationship with
Novartis that includes: speaking and lecture fees and travel reimburse-
ment. Massimiliano Di Filippo reports a relationship with Roche that
includes: speaking and lecture fees and travel reimbursement. Massi-
miliano Di Filippo reports a relationship with Siemens Healthineers that
includes: speaking and lecture fees and travel reimbursement. Massi-
miliano Di Filippo reports a relationship with Teva Health that includes:
speaking and lecture fees and travel reimbursement. Gioacchino Tede-
schi reports a relationship with Teva Health that includes: board mem-
bership. Gioacchino Tedeschi reports a relationship with Roche that
includes: board membership. Gioacchino Tedeschi reports a relationship
with Eli Lilly Italy that includes: board membership. Gioacchino Tede-
schi reports a relationship with Allergan US that includes: board mem-
bership. Gioacchino Tedeschi reports a relationship with Sano-Aventis
US LLC that includes: speaking and lecture fees and travel reimburse-
ment. Gioacchino Tedeschi reports a relationship with Merck Serono Ltd
that includes: speaking and lecture fees and travel reimbursement.
Gioacchino Tedeschi reports a relationship with Bayer Schering Pharma
AG that includes: speaking and lecture fees and travel reimbursement.
Gioacchino Tedeschi reports a relationship with Biogen Italy that in-
cludes: speaking and lecture fees and travel reimbursement. Gioacchino
Tedeschi reports a relationship with Novartis that includes: speaking
and lecture fees and travel reimbursement.
M. Altieri et al.

Multiple Sclerosis and Related Disorders 77 (2023) 104870
9
Funding source
None.
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