Abstract
Introduction
While the COVID-19 pandemic disrupted everyday life for all individuals, its impact was especially pronounced in patients with chronic illnesses. Among them, individuals undergoing biological therapy experienced additional difficulties related to continuity of care and access to medical professionals.
Aim
We aimed to evaluate the health-related quality of life (HRQoL) in inflammatory bowel disease (IBD) patients, who were receiving biological therapy, before and during the COVID-19 pandemic.
Material and methods
To our knowledge, this is the first study in the Balkans to examine the HRQoL exclusively in IBD patients treated with intravenous biological therapy, in the context of the COVID-19 epidemic. The cross-sectional study was conducted in two acts; in 2019 and during the second wave of the COVID-19 pandemic in 2020. All examinees filled out the short quality of life questionnaire. Patients were assessed for clinical disease activity using clinical activity indices. Also, they completed a questionnaire for the presence of depression – the Patient Health Questionnaire.
Results
There were 90 patients in the group before the pandemic, and 94 IBD patients were examined during the pandemic. The proportion of patients with a poorer HRQoL increased during the pandemic (16.7% vs. 26.6%), but not statistically significantly (p = 0.103). The greatest impact on HRQoL in multivariate analysis both before and during the COVID-19 outbreak was shown by disease activity (p = 0.014; p = 0.023) and the presence of depressive symptoms (p = 0.001; p = 0.002). The percentage of employed IBD patients decreased significantly during the pandemic (from 64.4% before the pandemic to 47.9%; p = 0.024).
Conclusions
An active disease and the presence of depressive symptoms had the greatest impact on impairment of the HRQoL of IBD patients, regardless of the pandemic. Mental health should be given more comprehensive attention in these patients.
Keywords: health-related quality of life, COVID-19, inflammatory bowel diseases, biological therapy
Introduction
Inflammatory bowel diseases (IBD) are long-term conditions that affect the gastrointestinal system, including ulcerative colitis (UC) and Crohn’s disease (CD). These illnesses can have a relapsing-remitting course and significantly impact patients’ quality of life [1]. IBD is a serious public health concern worldwide, with over 6 million people affected globally [2]. Although more common in developed countries, the prevalence of IBD is increasing in developing countries due to changes in lifestyle. Unfortunately, there are no official data on the incidence of IBD in Montenegro for children or adults.
The impact of the COVID-19 pandemic on health-related quality of life in IBD patients
The healthcare system and patients worldwide were greatly affected by the COVID-19 pandemic, but those with chronic diseases such as IBD were hit even harder. Studies indicate that individuals with IBD experienced a decline in their health-related quality of life (HRQoL) during the pandemic compared to before [3, 4]. The outbreak also presented challenges for healthcare systems, making it more difficult for patients to receive care and further impacting their quality of life [4]. Given Montenegro’s high incidence of COVID-19 infections in the second half of 2020, there were concerns about the potential impact on the HRQoL of IBD patients.
Health-related quality of life in IBD patients
In recent years, the treatment of IBD has seen significant improvements due to the development of immunomodulatory (biological) therapy [4]. This therapy has proven highly effective in reducing hospitalizations, complications, and the need for surgical intervention [4]. Its primary objective is to regulate the disease activity, allowing patients to maintain a more normal daily routine and improve their health-related quality of life (HRQoL) [5, 6]. The World Health Organization places great importance on promoting the holistic well-being of all patients and views health as a state of complete physical, mental, and social well-being, not simply the absence of disease or infirmity [7]. While the measurement of a patient’s quality of life can be challenging, it remains an essential indicator of their overall well-being. The Selecting Therapeutic Targets in Inflammatory Bowel Disease (STRIDE-II) Initiative has identified clinical remission, restoration of QoL, and the absence of disability as the most important long-term treatment targets for IBD patients [8].
The concept of HRQoL is a multifaceted and all-encompassing one, covering a range of dimensions such as physical health, mental well-being, social life, personal beliefs, and relationships with the world outside [9]. Furthermore, HRQoL also takes into account an individual’s perception of their place in a value system, cultural context, goals, standards, and expectations [10]. To assess the HRQoL of patients with IBD, researchers have created and validated several questionnaires that address their physical, emotional, and social health, as well as their IBD symptoms [9].
IBD is a long-term affliction that results in alterations in bowel movements, weight loss, rectal bleeding, and the need for extensive therapy, frequent hospitalizations, or surgery. It can also lead to social, emotional, and financial difficulties, which can significantly impact the HRQoL of some IBD patients [11]. The COVID-19 pandemic has only exacerbated this existing problem.
It is crucial to monitor the HRQoL of patients with IBD who are receiving intravenous biological therapy such as anti-tumor-necrosis factor (anti-TNF) and anti-integrins. Both patients and physicians should monitor the disease’s impact to determine the effectiveness of therapy [9]. Numerous studies have shown that biological therapy can significantly improve HRQoL [5, 6].
Aim
To our knowledge, this is the first study in the Balkans to examine the HRQoL of IBD patients treated with intravenous biological therapy, including anti-TNF and anti-integrins, and to identify potential factors that could lead to lower HRQoL before and during the COVID-19 pandemic.
Material and methods
Patients
The present study represents the first attempt to examine the HRQoL of patients with IBD who are treated with intravenous biological therapy in Montenegro. The study included 90 patients with IBD receiving biological treatment. The first examination was conducted at the end of 2018, before the COVID-19 pandemic, and 94 IBD patients receiving biological treatment were examined during the pandemic. The study was carried out at the Clinical Center of Montenegro, which serves as the sole referral center for IBD treatment in the country. The second examination of patients was conducted at the moment when the highest incidence of newly diagnosed patients with SARS-CoV-2 infection was recorded in Montenegro during the second wave of the pandemic in 2020.
Inclusion criteria for the study were patients who were at least 18 years of age and had been diagnosed with either UC and CD confirmed by histopathological analysis. The patients were receiving an intravenous form of biological therapy (anti-TNF-α or anti-integrin) for at least 3 months at the time of the study. Patients who had been diagnosed with psychiatric disorders were excluded from the study.
Methods
During their visit to the Outpatient Clinic for IBD treatment, patients completed a questionnaire to assess their quality of life using a short version of the IBD questionnaire (SIBDQ). The SIBDQ consists of ten questions about how the patients have been feeling over the past 2 weeks. The total response score can range from 10 to 70, with a score below 50 indicating poor quality of life [12]. For each question, the patients could choose one of the answers offered, which were later classified into four domains: bowel and systematic symptoms, and social and emotional function.
To assess depressive symptoms in patients, the quick and easy Patient Health Questionnaire 9 (PHQ9) – a diagnostic tool used by medical professionals to screen for depressive symptoms – was used. The test consists of 9 questions, and scores range from 0 to 27, with a higher score indicating more severe symptoms of depression. A cut-off of ≥ 10 points was used to classify the severe form of depressive symptoms (moderate and severe), with a sensitivity and specificity of 88% according to the literature [13].
The study also collected data on patients’ demographic characteristics such as age, gender, smoking habits, marital and employment status, and socio-economic status. Additionally, the patients provided information about the type of biological therapy they were receiving, as well as the use of corticosteroid preparations (parenteral, oral, or topical) and thiopurines during the past year. Data on the duration of the disease (less than or more than 5 years), the need for surgical interventions, as well as the need for hospitalization related to the underlying disease were also collected.
The Harvey-Bradshaw Index (HBI) was used to assess disease activity in CD [14], while the Partial Mayo Index Score (PMIS) [15] was used in the first trial to assess disease activity in UC. The Simple Clinical Colitis Activity Index (SCCAI) was used during the COVID-19 pandemic to assess disease activity [16]. Patients with clinically active disease (moderate and severe) had values ≥ 8 on the HBI, PMIS ≥ 5, and SCCAI ≥ 5.
Statistical analysis
All statistical analyses were performed using the statistical program IBM SPSS Statistics for Windows, Version 26.0. The Wilcoxon test was used to evaluate the difference in HRQoL in IBD patients before and during the COVID-19 pandemic. To evaluate the difference in categorical variables, the χ2 test was used for dependent samples. The Shapiro-Wilk test was used to test the normality of the distribution. Univariate and multivariate logistic regression was used to identify variables associated with increased likelihood of poor quality of life during the COVID-19 period. The study was approved by the institutional ethics committee (03/01-21867/1).
Results
The study enrolled a group of 90 patients with IBD examined before the COVID-19 pandemic, including 42 (46.7%) with CD and 48 (53.3%) with UC, and 94 IBD patients examined during the pandemic, including 42 (44.7%) with CD and 52 (55.3%) with UC. Before and during the COVID-19 period, in almost half of the examinees (51.1%), their disease had persisted longer than 5 years at the time of participating in the study. All the patients were receiving intravenous biological therapy (58.9% anti-TNF and 41.1% anti-integrin) throughout the examined period. The use of corticosteroids and thiopurines among IBD patients was similar before and during the pandemic (23.3% vs. 24.5%; 25.6% vs. 22.3%, respectively). According to the clinical activity questionnaires, about a quarter of the respondents had an active form of their disease in the pre-COVID-19 period, while the remainder were in remission. During the pandemic, the number of patients with an active form of the disease decreased (25.6% vs. 16.0%), but this was not statistically significant (p = 0.108). The percentage of employed IBD patients dropped significantly during the pandemic compared to pre-COVID-19, from 64.4% to 47.9%; this difference was statistically significant (p = 0.024). The majority of respondents did not self-report depressive symptoms either before (80.0%) or during (86.2%) the COVID-19 pandemic. There was no statistically significant difference in overall HRQoL among the IBD patients, before and during the COVID-19 pandemic (p = 0.103). Characteristics such as gender, marital status, socio-economic status, smoking, type of IBD, and duration of illness (treatment) revealed no statistically significant differences between the examined patients before and during the pandemic (Table I).
Table I.
Sample characteristics before and during the COVID-19 pandemic
| Variables | Pre-COVID-19 | During COVID-19 | χ2 | P-value | |||
|---|---|---|---|---|---|---|---|
| Sex | |||||||
| Male | 39 | 43.3% | 40 | 42.6% | 0.011 | 0.915 | |
| Female | 51 | 56.7% | 54 | 57.4% | |||
| Marital status | |||||||
| Married | 57 | 63.3% | 65 | 69.1% | 0.696 | 0.404 | |
| Unmarried | 33 | 36.7% | 29 | 30.9% | |||
| Employment status | |||||||
| Employed | 58 | 64.4% | 45 | 47.9% | 5.124 | 0.024 | |
| Unemployed | 32 | 35.6% | 49 | 52.1% | |||
| Socio-economic status | |||||||
| Low | 19 | 21.1% | 9 | 9.6% | 4.891 | 0.087 | |
| Medium | 55 | 61.1% | 68 | 72.3% | |||
| High | 16 | 17.8% | 17 | 18.1% | |||
| Smoking | |||||||
| Yes | 20 | 22.2% | 13 | 13.8% | 2.200 | 0.138 | |
| No | 70 | 77.8% | 81 | 86.2% | |||
| IBD characteristics and course | |||||||
| Type of IBD | |||||||
| CD | 42 | 46.7% | 42 | 44.7% | 0.073 | 0.787 | |
| UC | 48 | 53.3% | 52 | 55.3% | |||
| Biological therapy | |||||||
| Anti-TNF | 53 | 58.9% | 59 | 62.8% | 0.290 | 0.590 | |
| Anti-integrins | 37 | 41.1% | 35 | 37.2% | |||
| Duration of illness | |||||||
| < 5 years | 46 | 51.1% | 48 | 51.1% | 0.000 | 0.995 | |
| > 5 years | 44 | 48.9% | 46 | 48.9% | |||
| Hospitalization | |||||||
| Yes | 31 | 34.4% | 19 | 20.2% | 4.706 | 0.030 | |
| No | 59 | 65.6% | 75 | 79.8% | |||
| Disease activity | |||||||
| Active disease | 23 | 25.6% | 15 | 16.0% | 2.585a | 0.108 | |
| Remission | 67 | 74.4% | 79 | 84.0% | |||
| Biological and conventional drugs | |||||||
| Corticosteroid use | |||||||
| Yes | 21 | 23.3% | 23 | 24.5% | 0.033 | 0.857 | |
| No | 69 | 76.7% | 71 | 75.5% | |||
| Thiopurine use | |||||||
| Yes | 23 | 25.6% | 21 | 22.3% | 0.261 | 0.609 | |
| No | 67 | 74.4% | 73 | 77.7% | |||
| PHQ9 score | |||||||
| Depression | 18 | 20.0% | 13 | 13.8% | 1.249 | 0.264 | |
| Without depression | 72 | 80.0% | 81 | 86.2% | |||
| Quality of life | |||||||
| Good | 75 | 83.3% | 69 | 73.4% | 2.664 | 0.103 | |
| Poor | 15 | 16.7% | 25 | 26.6% | |||
χ2 – chi-square test, CD – Crohn’s disease, UC – ulcerative colitis, anti-TNF – anti-tumor necrosis factor, PHQ9 – Patient Health Questionnaire 9.
The results showed that 26.6% of IBD patients during the COVID-19 pandemic had poor HRQoL, which is about 10% higher than it was before the pandemic, but this difference was not statistically significant (p = 0.103). Nevertheless, this increase was influenced by factors that were active during the COVID-19 pandemic (Table II).
Table II.
Evaluation of difference in quality of life of patients with IBD before and during the COVID-19 pandemic
| HRQoL | Pre-COVID-19 | During COVID-19 | P-value | ||||
|---|---|---|---|---|---|---|---|
| N | Median (IQR) | Mean ±SD | N | Median (IQR) | Mean ±SD | ||
| Bowel domains | 90 | 19 (16–20) | 17.7 ±3.2 | 94 | 19 (16–20) | 17.4 ±3.2 | 0.753 |
| Systematic domains | 90 | 11 (9–13) | 10.8 ±2.5 | 94 | 11 (9–13) | 10.6 ±2.7 | 0.522 |
| Emotional domains | 90 | 18 (15–20) | 16.9 ±3.4 | 94 | 18 (16–19.25) | 17.4 ±2.8 | 0.462 |
| Social domains | 90 | 13 (11–14) | 12.1 ±2.7 | 94 | 13 (11–14) | 11.9 ±2.4 | 0.604 |
There was no statistically significant difference in HRQoL in IBD patients before and during the COVID-19 pandemic, either for Bowel (p = 0.753), Systematic (p = 0.522), Emotional (p = 0.462), or Social (p = 0.604) categories.
The results of univariate logistic regression showed that several factors before the COVID-19 pandemic were statistically significant predictors of poor HRQoL, such as socio-economic status, disease activity, use of corticosteroids and thiopurines, and the presence of depressive symptoms. In the multivariate model, only disease activity and the presence of depressive symptoms were statistically significant predictors of poor HRQoL (Hosmer and Lemeshow = 0.525), with an explanation of the HRQoL in the interval of 34.8% (Cox & Snell R2) and 58.7% (Nagelkerke R2) (Table III).
Table III.
Evaluation of quality of life in IBD patients before the COVID-19 pandemic period
| Parameter | OR | 95% CI | Sig. | OR | 95% CI | Sig. | |||
|---|---|---|---|---|---|---|---|---|---|
| Lower | Upper | Lower | Upper | ||||||
| Demographic and IBD characteristics | |||||||||
| Age [years] | 0.981 | 0.942 | 1.022 | 0.356 | |||||
| Sex | 2.250 | 0.726 | 6.976 | 0.160 | |||||
| Marital status | 0.438 | 0.142 | 1.344 | 0.149 | |||||
| Employment status | 0.796 | 0.255 | 2.482 | 0.694 | |||||
| Socio-economic status | 2.666 | 1.019 | 6.977 | 0.046 | 4.017 | 0.918 | 17.566 | 0.065 | |
| Smoking | 0.853 | 0.215 | 3.376 | 0.821 | |||||
| Type of IBD | 0.514 | 0.160 | 1.646 | 0.262 | |||||
| Treatment and course of illness | |||||||||
| Biological therapy | 1.488 | 0.463 | 4.781 | 0.504 | |||||
| Duration of illness [years] | 1.541 | 0.499 | 4.759 | 0.453 | |||||
| Hospitalization | 0.942 | 0.291 | 3.049 | 0.921 | |||||
| Disease activity | 9.538 | 2.791 | 32.593 | 0.000 | 9.268 | 1.565 | 54.893 | 0.014 | |
| Corticosteroid use | 3.812 | 1.185 | 12.270 | 0.025 | 0.388 | 0.046 | 3.305 | 0.387 | |
| Thiopurine use | 4.571 | 1.431 | 14.604 | 0.010 | 2.780 | 0.485 | 15.946 | 0.251 | |
| PHQ9 score | 0.601 | 0.467 | 0.773 | 0.000 | 26.967 | 4.173 | 174.281 | 0.001 | |
PHQ9 – Patient Health Questionnaire 9, OR – odds ratio, CI – confidence interval.
In the univariate model, during the COVID-19 pandemic, factors including socio-economic status, disease activity, and the presence of depressive symptoms were statistically significantly associated with increased likelihood that the HRQoL in IBD patients would be poor. In the multivariate model, disease activity and depression, but not socioeconomic status, were statistically significant predictors of poor HRQoL (Hosmer and Lemeshow = 0.525), with an explanation of the HRQoL in the interval of 34.9% (Cox & Snell R2) and 58.8% (Nagelkerke R2) (Table IV).
Table IV.
Evaluation of quality of life in IBD patients during the COVID-19 pandemic
| Parameter | OR | 95% CI | Sig. | OR | 95% CI | Sig. | |||
|---|---|---|---|---|---|---|---|---|---|
| Demographic and IBD characteristics | |||||||||
| Age [years] | 0.989 | 0.959 | 1.019 | 0.458 | |||||
| Sex | 1.352 | 0.539 | 3.392 | 0.521 | |||||
| Marital status | 0.930 | 0.347 | 2.488 | 0.885 | |||||
| Employment status | 0.516 | 0.201 | 1.325 | 0.169 | |||||
| Socio-economic status | 9.333 | 1.447 | 60.213 | 0.019 | 4.063 | 0.450 | 36.648 | 0.212 | |
| Smoking | 0.805 | 0.202 | 3.198 | 0.757 | |||||
| Type of IBD | 1.864 | 0.739 | 4.697 | 0.187 | |||||
| Treatment and course of illness | |||||||||
| Biological therapy | 0.852 | 0.333 | 2.179 | 0.739 | |||||
| Duration of illness [years] | 0.544 | 0.215 | 1.379 | 0.199 | |||||
| Hospitalization | 2.481 | 0.860 | 7.155 | 0.093 | |||||
| Disease activity | 8.533 | 2.540 | 28.669 | 0.001 | 12.226 | 2.584 | 57.852 | 0.002 | |
| Corticosteroid use | 1.288 | 0.457 | 3.633 | 0.632 | |||||
| Thiopurine use | 0.828 | 0.268 | 2.559 | 0.743 | |||||
| PHQ9 score | 62.769 | 7.500 | 525.306 | 0.000 | 72.041 | 7.117 | 729.173 | 0.000 | |
PHQ9 – Patient Health Questionnaire 9, OR – odds ratio, CI – confidence interval.
Discussion
Our study showed that the HRQoL of IBD patients did not significantly change during the COVID-19 pandemic. The main predisposing factors for poor quality of life were, as before the pandemic, disease activity and severe depression. These findings did not support our hypothesis that HRQoL was significantly impaired during the COVDI-19 pandemic in these patients. IBD patients experience a significantly decreased HRQoL due to the relapsing-remitting course of the disease and the lack of a definitive cure [17]. The COVID-19 pandemic has further exacerbated this condition, imposing an additional burden on both patients and healthcare systems worldwide. This study aimed to investigate whether the COVID-19 pandemic has had a significant effect on the HRQoL of Montenegrin IBD patients. The results showed that there was no significant difference in HRQoL in IBD patients before and during the pandemic. This finding was in contrast to the results of other studies that suggested that the COVID-19 pandemic has negatively affected the mental health and lifestyle of IBD patients, sometimes even influencing the entire course of illness [18–20]. Although biological therapy generally improves an IBD patient’s HRQoL [5, 6], numerous studies still report numerous factors that may affect the HRQoL in these patients, regardless of the COVID-19 pandemic difficulties [21–24]. The study found that disease activity and the presence of depressive symptoms were the primary factors that influenced the HRQoL in IBD patients, regardless of the pandemic, which is concordant with results from many other studies [21–24]. Supporting our conclusion, Conti et al. (2021) reported that the quality of life of IBD patients seemed to be more influenced by psychological and somatic distressing symptoms than the pandemic-related living conditions [25].
Surprisingly, despite the pandemic difficulties, the majority of Montenegrin IBD patients self-reported good HRQoL in general, which could be attributed to regular biological therapy and the availability of adequate medical support.
The study further revealed that the number of unemployed adult IBD patients during the COVID-19 pandemic was higher compared to pre-pandemic data, consistent with other studies [26]. The pandemic has produced several psychosocial effects on this vulnerable cohort, such as employment and income stability [26]. Nevertheless, the pandemic did not seem to affect the overall quality of life in the Montenegrin IBD patient cohort.
Finally, the study showed that hospital admissions of Montenegrin IBD patients due to disease deterioration significantly decreased during the COVID-19 pandemic. This was due to the fact that most of the Clinical Center, the sole tertiary public healthcare center in the country, and the only one specialized in IBD treatment, was converted into a COVID-19 hospital. This reduced hospitalization rates of non-COVID patients in general. Similar data on lower hospital admission rates of IBD patients during the COVID-19 pandemic were reported by a nationwide observational study in England [27].
The limitation of this study is the small number of participants, which reflects the fact that Montenegro has a very small population (around 650,000 inhabitants). Additionally, some IBD patients who received biological therapy subcutaneously were not included in this study, because the administration of these medications was performed in Primary Health Centers. Nonetheless, the study included all IBD patients in Montenegro who had a severe course of the disease and hence were undergoing intravenous biological therapy. It is important to emphasize that the results presented in this paper came from one of the South Eastern European countries that are generally experiencing a lack of research in the field of IBD and gastroenterology in general, as a result of low socio-economic status, and that makes our study notable.
Conclusions
The HRQoL of IBD patients who received intravenous biological therapy in Montenegro is generally reported as favorable. It can be inferred that the HRQoL of IBD patients who received biological therapy during the COVID-19 outbreak did not significantly deteriorate compared to the pre-pandemic period. Active disease and depressive symptoms had the most significant impact on poor HRQoL, emphasizing the importance of inducing remission as a fundamental aspect of care to improve HRQoL in IBD patients. Besides the routine efforts to achieve remission, mental health should be given more comprehensive attention in these patients. Psychological counseling programs, in addition to medical interventions, appear to be necessary for improving the health of IBD patients.
Funding
No external funding.
Ethical approval
The study was approved by the institutional ethics committee (03/01-21867/1).
Conflict of interest
The authors declare no conflict of interest.
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