Расследование COVID-19-Induced У иранских пациентов с множественным склерозом в пандемическое время.

Introduction

As an infectious condition, the coronavirus disease 2019 (COVID‐19) can be the leading cause of many respiratory tract infections (RTIs) from a cold to chronic respiratory diseases (CRDs), such as the Middle East respiratory syndrome (MERS) and the severe acute respiratory syndrome (SARS) [ 1 , 2 ]. The first cases of coronavirus (CoV)‐induced infection were identified in the city of Wuhan, China, in December 2019 [ 3 , 4 ]. According to the statistics of the World Health Organization (WHO), until August 2023, 557 million people were infected with COVID‐19, of which 6.7 million people died [ 1 , 2 ]. In Iran, until August 2023, 38.7 million people were infected with this virus, which has placed Iran in 17th place in the world [ 3 , 4 ].

Given the unknown nature of this disease and the possibility of its deterioration, the pandemic resulted in numerous changes in the physical and mental health status in different people in society and vulnerable groups, especially patients with multiple sclerosis (MS) [ 5 , 6 , 7 , 8 ]. MS is an autoimmune, inflammatory, and chronic disease of the central nervous system that damages the myelin tissue of the brain and causes a wide range of neurological symptoms, such as muscle weakness, neurological and motor disorders, imbalance, visual disturbances, limb pain, and psychological disorders [ 9 , 10 ].

MS and mental health are intricately and deeply connected. The possibility that mental health problems usually precede the initiation of MS by extended periods of time may imply a key etiological role for mental health in the development and progression of the disease [ 11 ]. The results of the studies showed that mood or eating disorders, schizophrenia, bipolar disease, and anxiety are more prevalent during the 2–10 years preceding MS in subjects with MS than in the control group [ 11 , 12 ]. Patients with MS are affected by the psychological consequences of COVID‐19, such as stress, anxiety, depression, post‐traumatic stress disorder (PTSD), and especially adjustment disorder (AD) [ 11 , 13 ]. According to the diagnostic and statistical manual of mental disorders (DSM_V), AD is divided into six categories: depressed mood, anxiety, mixed form of depressed mood and anxiety, conduct disorder, mixed form of emotional disturbance, and unspecified conduct. This disorder occurs during stressful situations, such as during the COVID‐19 pandemic [ 14 , 15 , 16 , 17 ]. As evidenced in previous studies, the prevalence rate of AD in non‐pandemic times had been 5%–50% among normal individuals, which was likely to escalate during the COVID‐19 pandemic with reference to prior experiences [ 13 , 14 ].

According to the studies performed before the pandemic, the exacerbation of psychiatric disorders had led to an upward trend in suicidal thoughts, in a way that the rate of suicide attempts in MS patients was two times [ 13 , 14 , 15 ]. Moreover, AD could relapse and trigger off many problems if not treated properly or if the treatment was ineffective and neglected [ 11 ]. Also, according to the results of research, people with AD disease also suffer from anxiety disorders and depression [ 11 , 12 ].

Since concerns about contracting COVID‐19 could have adverse effects on the quality of life in patients with MS, and this worry can be associated with numerous psychological consequences such as depression, suicide, anxiety, and especially AD, it can harm the mental health and well‐being of patients with MS. Therefore, it is very important to examine the psychological status of these patients during the COVID‐19 pandemic. In view of this, the present study was to investigate the COVID‐19‐induced AD among Iranian patients with MS in 2020.

Materials and Methods

Study Design and Participations

This study is a cross‐sectional research design. this study was conducted on 247 members of MS patients as the statistical population in 31 provinces of Iran.

Inclusion and Exclusion Criteria

The inclusion criteria were Iranian citizenship and willingness to participate in the study, and the exclusion criterion was incomplete questionnaires.

Sampling Methods and Sample Size Determination

Sampling was further done online through Porsline, as a survey tool, and the link to the questionnaires was sent via instant messaging apps, such as WhatsApp, Telegram, and the like, used by these patients, within 4 months from September 5, 2020 to January 4, 2021. An electronic questionnaire was sent to all members of the research community. The sampling method of the present study was also census.

Instruments

As well, two research instruments were administered, viz., a sociodemographic‐medical information form, whose variables were developed by searching the relevant sources by the research team, and the 20‐item Adjustment Disorder New Module (ADNM).

Sociodemographic‐Medical Information Form

The sociodemographic information forms contained items: age, place of living, gender, educational attainment, marital status, occupation, having children, number of children, income adequacy, and life companions. Medical information contained items, history of physical illnesses other than current MS, duration of treatment, movement restrictions, medical appointments canceling due to COVID‐19, history of familial COVID‐19, worry about infection, discontinued treatment due to COVID‐19, receiving information, contracting other diseases, psychiatric disorders, taking psychiatric medications, a history of polymerase chain reaction (PCR) test for COVID‐19, fear of familial COVID‐19 infection, death of family members due to COVID‐19, death of friends or relatives caused by COVID‐19, and medication shortages amid COVID‐19.

Adjustment Disorder New Model‐20 (ADNM)

The New Model of Adjustment Disorder Scale was designed by Lorenz et al. in 2016 to measure AD [ 16 ]. This questionnaire consists of 20 questions, which include core symptoms (8 questions) and secondary symptoms (12 questions). The core symptoms assess two dimensions of preoccupation and maladjustment and four dimensions of avoidance, depressed mood, anxiety, and PTSD. The range of scores for this instrument is between 20 and 80. To calculate the total score, the scores of all questions are added together. A score of 47.5 was determined as the cutoff point for this instrument. Scores of 20–47 indicated low to moderate risk, and scores of 48–80 indicated high risk of AD [ 16 ]. The validity of this questionnaire had been reported as favorable (Cronbach's alpha coefficient = 0.90) in Iran by Sarafraz et al. (2018), using factor analysis [ 17 ].

Statistical Analysis

The data were then analyzed using the SPSS Statistics software (ver. 26). Descriptive analyses, mean ± standard deviation (SD), were applied to describe the quantitative variables. Moreover, frequency and percentage were also utilized to illustrate the qualitative ones. Other Statistical methods such as Mann–Whitney U test, independent‐samples t ‐test, Kruskal‐Wallis test, and analysis of variance (ANOVA) were used for statistical analysis. As well, p  < 0.05 was considered statistically significant.

Ethical Considerations

This is a cross‐sectional research design, which has been registered in Iran National Committee for Ethics in Biomedical Research (Code: IR.MAZUMS.REC.1399.347). This research project was approved by the Ethics Committee of Mazandaran University of Medical Sciences (code no. IR.MAZUMS.REC.1399.7574), Sari, Iran. All the workers agreed to participate in the study.

Results

The mean age of the participants was 36.10 ± 8.07 years, and 82.6% of them were women. Most of the participants lived in the city (94.3%) and were mostly married (70.9%). The sociodemographic‐medical characteristics of the study participants are given in Table  1 .

TABLE 1 Sociodemographic‐medical characteristics of MS patients in 2020. Variables Levels Frequency (percentage) Variables Levels Frequency (percentage)
Sociodemographic characteristics
Place of living City 233 (94.3) Gender Female 204 (82.6) Village 14 (5.7) Male 43 (17.4) Marital status Single 72 (29.1) Occupation Homemaker 127 (51.4) Married 175 (70.9) Employee 39 (15.8) Educational attainment Below high school diploma 13 (5.3) Self‐employed 28 (11.3) High school diploma 78 (31.6) Unemployed 13 (5.3) Associate's degree 22 (8.9) Retired 8 (3.2) Bachelor's degree 91 (36.8) University student 7 (2.8) Master's degree 32 (13) Worker 4 (1.6) Income adequacy Low 60 (24.3) Other 21 (8.5) Moderate 136 (55.1) Number of children 1 70 (28.3) Good 51 (20.6) 2 65 (26.3) Life companions Family members 227 (91.9) 3 and so 9 (3.6) Alone 17 (6.9) Having children Yes 144 (58.3) Other 3 (1.2) No 103 (41.7) Age Mean ± SD 36.10 ± 8.07
Medical characteristics
Duration of treatment Below 6 months 13 (5.3) Contracting other diseases Yes 64 (25.9) 6–12 months 16 (6.5) No 183 (74.1) 1–2 years 26 (10.5) Psychiatric disorders Yes 50 (20.2) 2–10 years 113 (45.7) No 197 (79.8) Over 10 years 79 (32) Taking psychiatric medications Yes 122 (49.4) Movement restrictions Yes 89 (36) No 125 (50.6) No 158 (64) A history of polymerase chain reaction (PCR) test for COVID‐19 Yes 50 (20.2) Medical appointments canceled due to COVID‐19 Yes 95 (38.5) No 187 (75.7) No 152 (61.5) No information 10 (4) A history of COVID‐19 infection Yes 65 (26.3) Fear of familial COVID‐19 infection Yes 205 (83) No 182 (73.8) No 42 (17) A history of familial COVID‐19 infection Yes 112 (45.3) Death of family members due to COVID‐19 Yes 22 (8.9) No 135 (54.7) No 225 (91.1) Worry about COVID‐19 infection Yes 133 (53.8) Death of friends or relatives caused by COVID‐19 Yes 139 (56.3) No 114 (46.2) No 108 (43.7) Discontinued treatment due to COVID‐19 Yes 25 (10.1) Medication shortages amid COVID‐19 Yes 52 (21.1) No 222 (89.9) No 195 (78.9) Receiving information Yes 215 (87) No 32 (13)

Sociodemographic‐medical characteristics of MS patients in 2020.

The AD mean score was also 44.09 ± 13.89, at the moderate level, which was significantly correlated with some variables (Tables  2 and 3 ). According to the AD score, 57.1% (141 patients) of patients with MS had a low risk of AD, and 42.9% (106 patients) had a high risk of AD. The mean total AD score was 44.09 ± 13.89.

TABLE 2 AD mean score of in patients with MS in 2020. Variable
Mean ± S . D
Confidence interval 95% AD 44/09 ± 13/89 42/35 ± 45/83

AD mean score of in patients with MS in 2020.

TABLE 3 Comparing AD mean scores in terms of sociodemographic‐medical variables in patients with MS in 2020. Variables Levels Parameters Significance level AD Independent‐samples t ‐test* or Mann–Whitney U test** Marital status Single 43.93 ± 13.68 0.906** Married 44.16 ± 14.02 Gender Female 45.46 ± 13.44 0.001** Male 37.58 ± 14.29 Number of children 1 45.30 ± 12.57 0.403** 2 or so 43.36 ± 14.81 Movement restrictions Yes 43.17 ± 15.30 0.460** No 44.60 ± 13.05 Psychiatric disorders Yes 50.50 ± 14.31 0.001** No 42.46 ± 13.33 Taking psychiatric medications Yes 47.83 ± 13.51 0.001** No 40.44 ± 13.32 Medication shortages amid COVID‐19 Yes 48.11 ± 15.01 0.018** No 43.02 ± 13.42 Medical appointments canceled due to COVID‐19 Yes 47.67 ± 13.34 0.001** No 41.85 ± 13.80 A history of COVID‐19 infection Yes 47.56 ± 13.49 0.018** No 42.85 ± 13.86 A history PCR test for COVID‐19 Yes 47.76 ± 13.85 0.042** No 43.19 ± 13.75 Worry about COVID‐19 infection Yes 49.61 ± 12.22 0.001** No 37.64 ± 12.95 A history of familial COVID‐19 infection Yes 45.65 ± 13.50 0.001** No 42.80 ± 14.12 Fear of familial COVID‐19 infection Yes 45.98 ± 13.48 0.001** No 34.85 ± 12.15 Death of friends and relatives caused by COVID‐19 Yes 45.84 ± 13.85 0.025** No 41.84 ± 13.67 Parameters Place of living Significance level City Village Other Kruskal‐Wallis test ANOVA AD 43.13 ± 14.13 45.71 ± 13.60 45.77 ± 13.42 — 0.359
Parameters

Income adequacy

Significance level
Low Moderate Good Kruskal‐Wallis test ANOVA AD 45.45 ± 15.72 44.40 ± 12.79 41.66 ± 14.39 — 0.335
Parameters

Occupation

Significance level
Employee or retired Homemaker Other Kruskal‐Wallis test ANOVA AD 38.76 ± 13.27 45.97 ± 13.80 44.24 ± 13.74 — 0.009
Parameters

Duration of treatment

Significance level
Below 2 years 2–10 years Over 10 years Kruskal‐Wallis test ANOVA AD 46.10 ± 14.38 44.61 ± 13.93 41.94 ± 13.37 0.203 —
Note: The asterisks indicate significance level was considered at p  < 0.05.

Comparing AD mean scores in terms of sociodemographic‐medical variables in patients with MS in 2020.

Note: The asterisks indicate significance level was considered at p  < 0.05.

The relationships between AD mean scores in terms of sociodemographic‐medical variables in patients with MS Using statistical tests independent‐samples t ‐test, Mann–Whitney U test, and ANOVA are shown in Tables  2 and 3 .

The mean AD score was also significantly higher in women than in men ( p  = 0.001). This score was significantly related to employment status ( p  = 0.009), psychiatric disorders ( p  = 0.001), taking psychiatric medications ( p  = 0.001), medical appointments canceled due to COVID‐19 ( p  = 0.001), history of COVID‐19 infection ( p  = 0.018), a history PCR test for COVID‐19 ( p  = 0.042), worry about COVID‐19 infection ( p  = 0.001), and death of friends and relatives caused by COVID‐19 ( p  = 0.025).

Discussion

This study was to investigate AD caused by COVID‐19 among patients living with MS in Iran in 2020. Accordingly, the study results demonstrated that the AD mean score in the participants was 44.09 ± 13.89, which was at the moderate level. The results of the present study were consistent with those of Dragan, Grajewski, and Shevlin (2020) [ 18 ]. Dragan, Grajewski, and Shevlin (2020) found that 75% of the participants in the general population in Poland had suffered from AD during the COVID‐19 pandemic [ 18 ]. The results of the present study were inconsistent with the study of Mahat‐Shamir et al. (2021) [ 19 ]. Mahat‐Shamir et al. (2021) further reported the level of AD higher than normal [ 19 ]. As well, Zarghami et al. (2022) revealed in a review study that mental health was moderate [ 20 ].

The results of the present study showed that the mean age of the participants was 36.10 ± 8.07 years, and 82.6% of them were women. Therefore, women were more likely to have AD than men ( p  = 0.001). In the present study, more women suffered from hospital‐associated AD than men. Besides, the AD mean score was significantly higher in homemakers than those with other occupations ( p  = 0.009), which could be the outcome of more access to gossips and bad news among patients and their free time. The results of the present study were consistent with Motolese et al. (2020) [ 21 ] and Dragan et al. (2020) [ 18 ]. Motolese et al. (2020) in their study on MS patients had correspondingly settled gender as a predisposing factor for psychiatric disorders [ 18 ]. In this regard, Dragan et al. (2020) had reported stay‐at‐home and unemployment as the effective factors in men [ 21 ].

As confirmed in the present study, AD was significantly higher in patients with psychiatric disorders ( p  = 0.001) and a history of taking psychiatric medications ( p  = 0.001) than those without these conditions. The results of this study were significant with Deng et al. [ 5 ] and Wu et al. [ 6 ]. This could be attributable to a history of illnesses and psychiatric disorders in the participants. Also, in our study, AD was significantly associated with a history of COVID‐19 infection ( p  = 0.018), a history of PCR testing for COVID‐19 ( p  = 0.042), worry about COVID‐19 infection ( p  = 0.001), and the death of friends and relatives caused by COVID‐19 ( p  = 0.025). Thus, the patients who had a history of COVID‐19 infection or such a condition in one of their family members, or those who had experienced the death of friends or relatives caused by this pandemic, also reported higher AD. In this regard, Nakhostin Ansari (2019) [ 22 ] and Hosseini Largani (2020) [ 23 ] had achieved results consistent with this present study and detected a history of COVID‐19 infection in the family and relatives as factors augmenting the incidence rates of AD, depression, and severe anxiety in the participants.

Other results of this present study were that AD was significantly higher in patients who had canceled their appointments ( p  = 0.001) and had difficulty obtaining medication. This inability could be due to mobility limitations, economic difficulties, or quarantine. The results of the present study were consistent with Stojanov et al. (2020) [ 7 ] and Alschuler et al. (2020) [ 8 ].

In Stojanov et al. (2020), the problems of medication shortages and hospital referrals had been considered to be the major causes of concerns among the patients [ 7 ]. Alschuler et al. (2020), examining a statistical population of MS patients, had also introduced age and disease severity as the most important factors associated with emotional distress in the participants [ 8 ], which somehow supported the findings in the present study in terms of duration of treatment, as a key factor related to the risk of patient survival. It was thus correlated with AD severity, but age was not so unlike that in Alschuler et al. (2020), which could be attributed to the discrepancy in the sample size and the participants' age dispersion [ 8 ].

Strengths and Limitations of the Study

One of the strengths of the present study is that it was conducted on a population at risk of patients with a homogeneous disease. Among the limitations of the present study, we can mention the type of study, which was cross‐sectional. Also, the sampling method of the present study was available. Another limitation of the present study is the type of instrument, which was self‐report.

Conclusion

The present study established that AD in the MS patients was at the moderate level, and it was even associated with some distinctive variables such as female gender, psychiatric disorders, taking psychiatric medication, medical appointments canceled due to COVID‐19, history of COVID‐19 infection, worry about COVID‐19 infection, and etc. So, data from multicenter studies are needed to achieve better recommendations regarding screening psychiatric disorders and supportive strategies in clinical practice.

Author Contributions

E.S. drafted the manuscript, contributed to the revision of the manuscript. F.E. the CL psychiatrist, conceptualized the work, performed the literature search, and contributed to the revision of the manuscript. M.M. contributed to the interpretation of the findings, re‐evaluated the data, and revised the manuscript. S.M.B. participated in the clinical management of the patient as a neurologist and participated in data gathering. Z.S. and S.Z.H.N. contributed to the revision of the manuscript. All authors approved the final manuscript.

Ethics Statement

Ethics committee affiliated with Mazandaran University of Medical Sciences approved this report (IR. MAZUMS.REC. 1399.347).

Consent

Written informed consent was obtained from the patients.

Conflicts of Interest

The authors declare no conflicts of interest.

Acknowledgments

The authors hereby acknowledge Mazandaran University of Medical Sciences, Sari, Iran, and all hospital staff that were involved in patients management (7789).

Funding: This work was by Mazandaran University of Medical Sciences (347).

Data Availability Statement

The data from this research have not been made publicly available because the disclosure of individual data was not specified in the study protocol, and consent for public data sharing was not obtained from the participants.

References

Associated Data

Data Availability Statement

The data from this research have not been made publicly available because the disclosure of individual data was not specified in the study protocol, and consent for public data sharing was not obtained from the participants.