Author’s Accepted Manuscript

Comparative study of quality of life, anxiety,

depression, and fatigue among patients with
neuromyelitis optica spectrum disorder and
multiple sclerosis: the first report from Iran

Mahdi Barzegar, Shervin Badihian, Omid

Mirmosayyeb, Fereshteh Ashtari, Maryam Jamadi,
Shohreh Emami, Leila Jahani, Armaghan Safavi, www.elsevier.com/locate/msard

Vahid Shaygannejad

PII: S2211-0348(18)30127-5
DOI: https://doi.org/10.1016/j.msard.2018.04.009
Reference: MSARD826
To appear in: Multiple Sclerosis and Related Disorders
Received date: 19 December 2017
Revised date: 7 March 2018
Accepted date: 13 April 2018
Cite this article as: Mahdi Barzegar, Shervin Badihian, Omid Mirmosayyeb,
Fereshteh Ashtari, Maryam Jamadi, Shohreh Emami, Leila Jahani, Armaghan
Safavi and Vahid Shaygannejad, Comparative study of quality of life, anxiety,
depression, and fatigue among patients with neuromyelitis optica spectrum
disorder and multiple sclerosis: the first report from Iran, Multiple Sclerosis and
Related Disorders, https://doi.org/10.1016/j.msard.2018.04.009
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Comparative study of quality of life, anxiety, depression, and fatigue among patients with

neuromyelitis optica spectrum disorder and multiple sclerosis: the first report from Iran

Mahdi Barzegar1,2, Shervin Badihian1,2, Omid Mirmosayyeb1,2, Fereshteh Ashtari1, Maryam

Jamadi1,2, Shohreh Emami1, Leila Jahani1, Armaghan Safavi1, Vahid Shaygannejad1

1- Neurosciences Research Center, Alzahra Research Institute, Isfahan University of Medical

Sciences, Isfahan, Iran

2- Student Research Committee, school of medicine, Isfahan University of Medical Sciences,

Isfahan, Iran.

shaygannejad@med.mui.ac.ir

Address for Correspondence: Vahid Shaygannejad MD, Department of Neurology, school of

medicine, Isfahan University of Medical Sciences, Isfahan, Iran.

ABSTRACT

Background:

Neuromyelitis optica spectrum disorder (NMOSD) and multiple sclerosis (MS) are associated

with reduced Health Related Quality of Life (HRQOL). To the best of our knowledge, change of
HRQOL in patients with NMOSD has not been yet measure in Iran. The objective of this study

was to assess HRQOL in NMOSD and MS patients and identify related factors

Methods:

A cross sectional study of 41 patients with NMOSD and 136 age and sex-match MS patients was

performed. A series of questionnaires including Persian validated questionnaires on HRQOL

(SF-36), fatigue (MFIS), depression (BDI-II), anxiety (HAM-A) and sleep quality (PSQI) were

record. All demographic variables, socioeconomic status and clinical data were also obtained.

Student`s T test and Mann–Whitney U test used to compare variables between groups and

multivariate regression analysis applied to assay predictor factors.

Results:

The mean scores of mental (MCS) and physical (PCS) components of QOL were statistically

lower in patients with NMOSD compare with MS patients (β=-4.49, P=0.004; β=-3.52,

P=0.015). Multivariate analysis indicated fatigue, depression and anxiety were independent,

significant predictor of MCS (β=-0.229, P=0.002; β=-0.229, P=0.002; β=-0.258, P=0.020

respectively). However, PCS was significantly predicted by fatigue (β=-0.258 P<0.001), solely.

Conclusion:

These findings indicate NMOSD patients have lower HRQOL in compare to patients with MS.

Also, screening and treatment of fatigue as the most important predictor for HRQOL is

necessary.

Keywords: Quality of life; Fatigue; Anxiety; Depression; Neuromyelitis optica spectrum

disorder; Multiple sclerosis
INTRODUCTION

Neuromyelitis Optica spectrum disorder (NMOSD) is an inflammatory disorder of the central

nervous system (CNS), predominantly disturbing the optic nerve and the spinal cord (1). The

disease usually follows a relapsing course with frequent attacks leading to severe disability, and

is highly associated with morbidity and mortality (1, 2). Multiple Sclerosis (MS) is an

autoimmune disease of CNS characterized by demyelinative inflammatory lesions (3, 4).

Relapsing-remitting MS is the least aggressive form of the disease seen in 85% of cases and is

characterized by relapses followed by recovery periods (3, 4).

Rehabilitation is a crucial part of care in these patients due to both physical and cognitive

disabilities associated with their disease (5, 6). Evaluation of Health Related Quality of Life

(HRQOL) is required to assess the rehabilitation needs and plan for applicable strategies (7).

Several studies have reported decreased HRQOL among MS patients (8-11). Different factors

are associated with decreased HRQOL in these patients, including depression, fatigue, disability,

anxiety, pain, cognitive disturbance, and others (8, 9, 12). Unlike frequent surveys on MS cases,

very limited number of researchers have evaluated the quality of life and associated factors

among NMOSD subjects (13, 14). According to these studies, anxiety, pain, disability, fatigue,

depression, and cognitive function affect QOL among NMOSD patients (13, 15-17).

On the other hand, QOL and some related factors (such as anxiety, depression, cognitive

function, …) are highly affected by cultural, ethnic, and religious issues while the current data

and care strategies are mostly developed based on reports from developed countries in Europe

and America (18). Thus, no research is conducted before to evaluate these features in Iran and

surrounding countries in the Middle East. To fill these gaps, we aimed to assess and compare
HRQOL and related factors in MS and NMOSD cases in Iran, in order to find out fluctuations in

patients’ physiological, psychological, and social function.

1. METHODS

This is a cross-sectional study which was conducted during 2017 in MS clinic of Kashani

hospital, affiliated to Isfahan University of Medical Sciences, Isfahan, Iran. The inclusion criteria

were defined as diagnosis of NMOSD based on the international consensus diagnostic criteria in

2015 (19) for the NMOSD group and diagnosis of MS based on the latest revision of McDonald

criteria (20) for the MS group. Also, subjects were required to have at least 18 years of age.

Patients who had any other neurological diseases and those who were taking antidepressants or

other medications affecting the mood (such as mood stabilizers and antipsychotics) in the last 6

months prior to the study were excluded. The study was approved by the regional bioethics

committee of Isfahan University of Medical Sciences. Written informed consents took from all

subjects before enrollment.

To calculate sample size, we used the equation for comparison of two means. Assumptions in

two groups (scores from 36-Item short health survey) were pre-specified on the basis of

previously published data (14). We hypothesized that an equivalent result will be detected in

groups. The sample size was calculated as at least 43 patients in each group.

After inclusion, all the patients were interviewed to collect data regarding demographic features

(age, gender, job status, and educational status), history of smoking, current medications (disease

modifying agents as well as any other medication), comorbid diseases, disease duration, and

expanded disability status scale (EDSS). Patients were asked then to fill the validated Farsi

version of the following questionnaires: Hamilton anxiety rating scale (HAM-A) (21), Pittsburgh
sleep quality index (PSQI) (22), Modified fatigue impact scale (MFIS) (23), Beck depression

inventory (BDI-II) (24), and 36-Item short health survey (SF-36) (25). Results from MFIS are

reported in three dimensions of physical, cognitive, and psychosocial, as well as the total score.

BDI-II scores are reported in two dimensions of somatic and cognitive, as well as the total score.

The Health Status Questionnaire (SF-36) is a one of the most widely-used generic health status

measures. It is a brief (36-item) scale established by Stewart, Hayes and Ware (1988) from items

comprised in the Medical Outcomes Study. The SF-36 has 8 multi-item domains including

Physical functioning, social function, role limitations related to physical problems, role

limitations related to emotional problems, mental health, vitality, bodily pain, and general health

perceptions. Each domain can be scored separately with scores ranging from 0 (worst health

state) to 100 (best health state). Two scales (Physical and Mental) have also been derived using

factor analytic methods. SF-36 results are presented in two categories of physical component

summary (PCS) and mental component summary (MCS). We should note that the primary

outcome of the study was assumed as the SF-36 scores.

Descriptive data was presented as mean (standard deviation [SD]) or frequency (%) for interval

and categorical variables, respectively. Moreover, comparisons of these scores between study

groups were done once with separation of gender to eliminate the possible confounding role of

gender on the results. The scores from each questionnaire were compared between two study

groups using independent sample t-test and Mann-Whitney U test, where applicable.

Multivariate generalized linear model (GLM) was used to define whether disease type had an

independent effect on baseline PCS and MCS, after adjusting for sociodemographic variables

(age, sex and education). Statistical analysis was performed using IBM SPSS (ver. 23, NY,

USA) and a P-value less than 0.05 was considered as significant.

 2. RESULTS

A total of 41 NMOSD patients and 136 MS cases enrolled in the study. No difference was found

between two groups regarding age and gender. No statistically significant difference was found

regarding the clinical and demographic characteristics of patients between two groups (P-

value>0.05), except for the frequency of comorbidities which was found to be greater in

NMOSD group (39% compared to 20.1% in MS group; P-value=0.014). MRI findings indicated

cervical segment spinal cord lesions in 82.3% of NMOSD patients. Brain MRI was normal in

73.8% of NMOSD patients and deep white matter of hemispheres and brainstem abnormality

was detected in 10.2% of patients. These findings are presented in details in Table 1.

Table1. demographic and clinical characteristics of study subjects

MS NMOSD

Mean (SD) or % Mean (SD) or %

Age 34.26 (9.02) 37.48 (9.50)

Female% 80.1% 73.2%

Married 63.2% 73.8%

Sociodemographic variables

Education%,

High school or less 56.6% 61.0%

> High school 43.4% 39.0%

Full- or part-time 23% 28.6%

employment

Positive History of 15.8% 14.3%

Smoking
 Disease duration, years 9.6 (4.2) 8.4 (3.8)

EDSS 2.86 (1.49) 2.72 (1.64)

Median time to second 1.8 1.6

attack, years

Positive NMO-Ab - 21.2%

Most common
Disease variables

symptoms%,

Optic neuritis 30.1% 59.4%

transverse myelitis - 35.8%

paresthesia 36.4% -

Beta interferon 63.4% -

Rituximab 5.18% 76.32%

Medication Natalizumab 16.29% -

Azathioprine 2.13% 18.60%

Sedative or epileptic drugs 17.2% 17.1%

Comparison of scores from HAM-A, PSQI, MFIS, and BDI-II, and SF-36 are presented in Table

2. We observed decreased BDI-II scores in both dimensions of somatic and cognitive among

NMOSD cases compared to MS patients (P-value<0.05). Additionally, NMOSD cases had lower

scores of MFIS in cognitive dimension compared to MS (P-value<0.05).

Table 2. Comparison of anxiety, depression, sleep quality, fatigue between study groups

Questionnaire NMOSD MS P-value

Mean (SD) Mean (SD)

Hamilton anxiety rating scale (HAM-A) 9.95 (8.03) 10.95 (7.74) 0.483

Pittsburgh sleep quality index (PSQI) 6.33 (2.77) 6.69 (3.09) 0.511

Modified fatigue Physical 13.36 (10) 16.16 (9.77) 0.120

impact scale Cognitive 8.31 (7.28) 12.52 (10.69) 0.006

(MFIS) Psychosocial 2.63 (2.85) 3.13 (2.61) 0.295

Total 25.05 (17.51) 31.37 (20.18) 0.084

Beck depression Somatic 17.51 (11.62) 24.51 (7.28) 0.001

inventory (BDI-II) Cognitive 10.13 (7.59) 13.51 (5.11) 0.011

Total 28.37 (18.47) 38.14 (11.67) 0.004

36-Item short Physical Component 41.19 (8.22) 42.96 (8.95) 0.284

health survey (SF- Summary

36) Mental Component 42.22 (11.68) 43.12 (10.94) 0.673

Summary

NMOSD: Neuromyelitis optica spectrum disorder; MS: Multiple sclerosis; SD: Standard

deviation

To evaluate the possible role of gender, we compared all the mentioned scores between two

study groups separated by gender (Table 3). We found that male NMOSD patients have lower

MFIS in cognitive category compared to male MS cases (P-value<0.05). Also, male NMOSD

cases had lower somatic, cognitive, and total BDI-II scores compared to male MS subjects (P-

values<0.05). Similarly, we found lower scores of MFIS cognitive category among female
NMOSD cases compared to female MS patients (P-value<0.05). Moreover, female NMOSD

cases showed lower somatic and total BDI-II scores compared to the other group (P-

values<0.05). No statistically significant difference was seen regarding other scores including

PSQI, HAM-A between groups (P-values>0.05). These findings show that sleep quality and

anxiety are not affected by gender.

Table 3. Comparison of fatigue and depression scores between study groups separated by gender

Questionnaire Gender NMOSD MS P-value

Mean (SD) Mean (SD)

Modified Cognitive Female 7.21 (6.49) 10.78 (10.05) 0.027

fatigue impact Male 17.18 (11.37) 18.89 (7.23) 0.031

scale (MFIS)

Beck Somatic Female 16.52 (11.44) 23.74 (7.03) 003

depression Male 20.40 (12.28) 27.71 (7.57) 0.042

inventory Cognitive Female 10.31 (7.44) 13 (4.79) 0.073

(BDI-II) Male 9.64 (8.31) 15.44 (5.88) 0.020

Total Female 27.43 (18.20) 36.92 (11.25) 0.013

Male 31 (19.95) 43.04 (12.30) 0.039

NMOSD: Neuromyelitis optica spectrum disorder; MS: Multiple sclerosis; SD: Standard

deviation

We also compared the scores between genders in each study group. We found that male MS

cases had higher scores regarding PSQI, cognitive and total MFIS, and BDI-II, and lower MCS
scores compared to female MS subjects (P-values<0.05). These findings are presented in Table

4.

Table 4. Comparison of sleep quality, fatigue, depression, and quality of life between male and

female patients with relapsing-remitting multiple sclerosis

Questionnaire MS (Mean (SD)) P-value

Female Male

(n=109) (n=27)

Pittsburgh sleep quality index (PSQI) 8.47 (3.24) 6.29 (2.92) 0.002

Modified fatigue impact scale Cognitive 10.78 (10.05) 19.27 (10.61) <0.001

(MFIS) Total 28.53 (20.17) 42.19 (16.51) 0.002

Beck depression inventory (BDI- Somatic 23.74 (7.03) 27.71 (7.57) 0.016

II) Cognitive 13 (4.79) 15.44 (5.88) 0.027

Total 36.92 (11.25) 43.04 (12.30) 0.021

36-Item short health survey (SF- Mental 45.21 (10.62) 35.60 (8.67) <0.001

36) Component

Summary

MS: Multiple sclerosis; SD: Standard deviation

Multivariate GLM was performed to analyze whether PCS and MCS scores varied between MS

and NMOSD groups, after adjusting for sociodemographic variables. Patients with NMOSD had

significantly lower MCS and PCS scores compared to MS subjects (Table 5). In an additive

multivariate analysis of variance with the MCS as dependent variable in NMOSD patients,

17.9%, 8.1% and 4.8% of the generalized variance in HRQOL (effect size) was accounted by

fatigue (β=-0.229, P=0.002), depression (β=-0.229, P=0.002) and anxiety β=-0.258, P=0.020),
respectively. On other hand, fatigue was predictor of PCS in NMOSD patients with the effect

size of 20.6% (β=-0.258 P<0.001).

Table 5. comparison of quality of life between NMOSD and MS subjects

Questionnaire NMOSD (Mean MS (Mean Standardized P-value

Coefficient β
(SD)) (SD))

PCS 39.54 43.07 -3.52 0.015

MCS 39.70 44.19 -4.49 0.004

3. DISCUSSION

As previously discussed, evaluating health-related quality of life in patients suffering from

chronic disabling disorders is of great importance to make treatment and rehabilitation decisions

(26, 27). In the current study, we evaluated anxiety, depression, sleep quality, fatigue, and

quality of life among NMOSD and MS cases and compared the scores between them. To the best

of our knowledge, this is the first comparative study to investigate QOL and the most important

related factors between these two diseases, as well as the first study on QOL and related factors

of these patients in Iran and the surrounding countries in the Middle East. Our results

demonstrated that NMOSD patients had considerably worse HRQOL compared to MS subjects.

Also, we found that fatigue was the most important variable to predict variance of physical and

mental components of HRQOL. In agreement with our results, Chanson et al surveyed HRQOL

in NMO patients using Multiple Sclerosis Quality of Life (MSQOL-54) questionnaire and found

impaired HRQOL among these cases (22).

Based on our findings, fatigue, depression and anxiety were predictive factors for mental

component of HRQOL, while PCS was predicted by fatigue, solely. In contrast with our

findings, Shi et al reported that anxiety was the best predictor for PCS and MCS in such patients

(17). This difference can be explained by hospitalization of patients in Shi et al study which may

have had a confounding influence on QOL and related factors, such as anxiety.

In our study, Fatigue scores were similar in both study groups, although NMOSD patients

reported lower levels of fatigue in cognitive dimension compared to MS cases. Chanson et al

found moderately higher levels of fatigue in psychosocial dimension in MS group, while no

difference was reported regarding other dimensions (14). Recent studies have shown that fatigue

have significant correlation with QOL in both NMOSD (13) and MS patients (12, 28, 29). We

found fatigue have an important role in prediction of both physical and mental components of

SF-36 in participants. Numerous studies investigated causes of fatigue in MS (30-32).

Nevertheless, the pathophysiology of NMOSD-induced fatigue is not clear and limited

investigations are performed to clarify it. Considering the important role of fatigue in predicting

QOL in NMOSD patients, early screening and diagnosis is necessary for sufficient and on-time

rehabilitation.

MS cases showed worse levels of depression in both somatic and cognitive category compared to

NMOSD patients. In contrast, Chanson et al found no difference regarding depression between

NMOSD and MS groups (14). Depression is suggested to be strongly correlated with QOL in

NMOSD (13). Same with previous findings, we observed that depression is a significant

predictive factor of MCS. Also, previous studies have shown that depression is the main

determinant of HRQOL in MS (9, 29), while we found depression as a significant predictive

factor of MCS only.

Separating the study groups by gender resulted in the same findings regarding differences

between anxiety, depression, sleep quality, fatigue, and quality of life among NMOSD and MS

subjects. This suggests that the gender was not a confounding factor in our study. On the other

hand, we found more severe depression among male NMOSD cases, compared to female

patients. Moreover, male MS cases reported worse status regarding sleep quality, fatigue in

cognitive and total dimensions, depression, and mental component of HRQOL compared to

female MS subjects. Likewise, lower levels of HRQOL, particularly in the mental dimension,

among men with MS was reported in two studies before (33, 34). They attributed the observed

difference to stronger adaptive mechanisms among female cases as well as the more destructive

effect of physical disability on men due to cultural beliefs (33, 34), which is generalizable to the

Iranian community.

We found no difference regarding anxiety levels between patients with NMOSD and MS. Shi et

al presented anxiety as a strong correlated factor with health-related QOL (HRQOL) in NMOSD

cases (13). Our results indicated that anxiety is a predictor factor of mental component of

HRQOL.

Lack of control group was the main limitation of our study, however, we mostly concentrated on

comparing QOL and related factors between NMOSD and MS. Also, are study is limited by the

cross-sectional design, lack of number of hospitalization and relapse type and different number

of cases in two study groups.

In conclusion, our results indicated that NMOSD patients had worse QOL in comparison to

patients with MS. This fact emerges the importance of active screening among NMOSD patients

for fatigue, depression, and other related impaired abilities, in order to better implementation of

rehabilitation strategies. Moreover, these findings give a clearer insight into how these disorders,
especially NMOSD, affect patient’s health-related quality of life. In addition, the results of this

study may provide information for the health care system and government in Iran and other

countries to help make better health and welfare service policies for patients with NMOSD and

ensure that such policies meet patients’ real needs.

Acknowledgements

Isfahan University of Medical Sciences has financially supported the present paper. We thank

our patients for their collaboration. Also the authors would like to thank the efforts of the staff at

the MS clinic in Kashani hospital. The neurosciences research center, Alzahra hospital, Isfahan,

Iran has supported this study financially and so we acknowledge this gesture.

Conflict of interest

The neurosciences research center, Alzahra hospital, Isfahan, Iran has supported this study
financially and so we acknowledge this gesture and none of the authors have any conflict of
interest to disclose.

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Highlights

“Patients with NMOSD had worse quality of life in comparison with MS patients.”
“In order to better implementation of rehabilitation strategies NMOSD patients could be
screened for fatigue, depression, and other related impaired abilities,”
“Fatigue is the most important variable to predict quality of life in NMOSD patients.”
“Health care policy makers in Iran and other countries should make better health and welfare
service policies for patients with NMOSD”