A total of 522 patients with IBD were included in the study after providing written informed consent. Of these, 16 patients did not use biological treatments or did not complete the questionnaires, and were therefore excluded. All the remaining 506 questionnaires could be evaluated (response rate: 97%). Of the 506 analyzed patients, 217 (42.9%) were women, with a mean age of 40.8 years (SD 14.7); 199 (39. 3%) had UC, and 307 (60.7%) had CD. Detailed characteristics of the study sample are presented in Table 1.
Table 2 describes the IBD patients’ experience of restrictions due to the pandemic. Eighty patients (15.8%) thought they had an increased risk of being infected with COVID-19 because of IBD, and one-third voluntarily self-isolated. Thirty-eight patients (7.6%) were afraid of going to the hospital and 20 patients (4.0%) cancelled their appointment. The hospital re-scheduled from physical appointment to a telephone follow-up for 75 patients (15%). Bivariate analyses revealed that a significantly higher proportion of women compared to men reported symptoms of COVID-19, 48 (22.2%) vs. 39 (13.5%), respectively. In addition, a significanlty higher proportion of patients < 50 years reported symptoms of COVID-19, compared to those > = 50 years, n = 73 (19.6%) vs. n = 14 (10.7%), respectivily. Furthermore, a significantly higher proportion of women (38.5%) compared to men (27.7%) reported voluntarily self-isolation. There were no statistically significant differences between patients with ulcerative colitis and Crohn’s disease.
PHQ-9 and GAD-7 scores
Of the IBD patients, 90 patients (18.1%) met the criteria for major depression (PHQ-9 score ≥ 10), and 62 patients (12.5%) met the criteria for anxiety (GAD-7 score ≥ 8). Of those with a score ≥ 10 on PHQ-9, 51.1% were women; and of those with a score ≥ 8 on GAD-7, 61.3% were women. The mean PHQ-9 score was 5.52, 95% CI [5.07, 5.96]. Women had a significantly higher PHQ-9 scores compared to men (6.19, 95% CI [5.51, 6.88] vs. 5.05, 95% CI [4.42, 5.59], respectively). The mean GAD-7 score was 3.30, 95% CI [2.94, 3.65] for all 506 patients (Table 2). Women had a significantly higher GAD-7 score compared to men (4.13, 95% CI [3.53, 4.72] vs. 2.67, 95% CI [2.25, 3.08], respectively). Forty eight patients met the criterion for both anxiety and depression based on the cut-off scores.
Factors associated with depression
Logistic regression analyses were used to assess the strength of associations between major depression and sociodemographic and disease-related factors, questions regarding COVID-19 restrictions, and healthcare needs (Table 3). When adjusted for possible predictive factors, general condition, self-isolation, employment status, being afraid to go to the hospital, and whether the hospital made changes to patients’ appointments were all independently and significantly associated with higher depression levels. Compared to patients with unaffected general condition, patients with reduced condition were over five times more likely to be depressed (OR = 5.24, 95% CI [3.00, 9.19]). Those who chose to self-isolate were 2.7 times more likely to be depressed compared to those who did not (OR = 2.70, 95% CI [1.56, 4.70]).
Patients on sick leave or temporarily laid off were almost four times more likely to be depressed compared to patients who were employed or students (OR = 3.80, 95% CI [1.69, 8.51]). However, there were no differences in the odds of developing clinical depression between employed patients and those with disability benefits or pensioners.
Being afraid of going to the hospital had a significant impact on patients’ odds of clinical depression. Those who were afraid of going to the hospital were 2.6 times more likely to be depressed compared to those who were not afraid (OR = 2.62, 95% CI [1.08, 6.38]).
Changing the type of consultation from physical consultation to phone consultation greatly diminished patients’ odds of being depressed. The patients who had their consultation changed to phone consultation had about 70% reduced odds of depression compared to those who did not experience such changes (OR = 0.29, 95% CI [0.12, 0.72]).
Factors associated with anxiety
Logistic regression analyses were used to assess the association between anxiety and sociodemographic and disease-related factors, questions regarding COVID-19 restrictions, and healthcare needs (Table 4). The multiple logistic regression model revealed that female gender, having symptoms of COVID-19, self-isolation, perceived themselves as being more likely to get infected with COVID-19 because of IBD, as well as being afraid to go to the hospital because of COVID-19 restrictions, and having their appointment cancelled due to fear of getting infected were all independently and significantly associated with higher levels of anxiety.
Women were twice as likely to reach high levels of anxiety compared to men (OR = 2.01, 95% CI [1.08, 3.74]). Patients who experienced COVID-19 symptoms were almost three times more likely to be anxious compared to those who did not experience it (OR = 2.79, 95% CI [1.41, 5.53]).
Patients who perceived themselves as being more likely to get infected with COVID-19 had more than two times higher odds of being anxious (OR = 2.33[1.0, 5.44] and OR = 2.78[1.33, 5.81], for those who perceived themselves at higher risk and those who did not know if they were at such a risk, respectively. Being afraid of going to the hospital increased the odds of being anxious by more than threefold compared to patients who were not afraid (OR = 3.29, 95% CI [1.38, 7.82]).
Patients who cancelled their IBD consultation due to fear of becoming infected were more than twice as likely to be anxious compared to patients without such concern (OR = 2.89, 95% CI [0.86, 9.69]; however, the odds did not reach the level of statistical significance (p = 0.085).
Our results showed that, overall, a low proportion of IBD patients were worried about their treatment and follow-up at the hospital, and a high proportion felt safe at the hospital. However, we found several COVID-19-related factors independently associated with anxiety and depression.
One-fifth of patients reported major symptoms of depression. Our finding is in accordance with a rate of 22.5% in a newly published study that assessed depression with PHQ-9 in a hospital-based sample of IBD patients in the United Kingdom during the pandemic . In studies assessing depression with PHQ-9 in IBD populations before the pandemic, a prevalence between 25% and 34% was found [23, 24]. Only 12.5% reported anxiety in our study, which is somewhat lower than findings in a hospital-based cohort in the United Kingdom that found a prevalence of 18% . A study assessing anxiety with GAD-7 in an IBD population in 2018 found a prevalence of 21% . The mean levels of depression and anxiety in our study were however lower than the estimates from a study conducted among the general Norwegian population simultaneously during the pandemic .
Systematic reviews and meta-analyses have shown that anxiety and depression are prevalent among patients with IBD in the pre-pandemic samples [11, 12]. Comorbid anxiety and depression may affect the IBD patients’ health-related quality of life and their ability to manage living with IBD. A systematic literature review revealed that a systematic approach to screening for anxiety and depression is not common in IBD quality of care, leaving the patients non-medical needs untreated . To facilitate healthcare services for patients with IBD during the pandemic, knowledge of how restrictions may impact psychological health is needed to meet the patients’ non—medical needs and to include mental health professionals when needed.
An impaired general condition was the strongest predictor of depression. Patients in our study who had reported a decreased general condition were over five times more likely to be depressed than patients with unaffected general condition. General conditions and experiencing COVID-19 symptoms were the only disease-related factors associated with adverse psychological health outcomes. Both the general condition and symptoms of COVID-19 were self-assessed by the patients, and thus their subjective assessments of feeling sick. We assume that both physical and psychological factors are considered when assessing one’s level of activity, energy level, and overall well-being. These factors are also considered symptoms of depression, which may help explain the strong statistical association between these variables and the outcome.
Self-isolation, fear of visiting the hospital, and fear of contracting COVID-19 were all factors strongly associated with anxiety and depression. The same factors were found in a Portuguese study that used an online survey to assess the effects of the pandemic on disease and psychological outcomes among patients with IBD . Systematic reviews have revealed that anxiety and depression rates in patients with IBD were associated with impaired health-related quality of life and higher healthcare use [3, 26]. This may indicate that IBD patients have unmet needs related to support for psychological issues during follow-up from healthcare providers. We found that changing from a physical hospital appointment to telephone consultation was a predictive factor for depression in our patients with IBD. The patients who had their consultation changed to telephone consultation had about 70% reduced odds of depression compared to those who did not experience such changes. To feel safe for patients, it is important to provide sufficient information regarding treatment and follow-up during the pandemic. Structural elements, such as access to mail and telephone support, IBD-nurse consultation, and information and disease advice from IBD specialists regarding IBD and COVID-19 are recommended to provide the most effective model of care [6, 27].
We found that the IBD treatment adherence was 98% in our study. All patients in our study received biological treatment, and many patients received infusion therapy. Despite increased concerns among IBD patients during the pandemic, other recent studies also found a similarly high treatment adherence [25, 28].
Female patients with IBD were more likely to have higher levels of anxiety than male patients. One reason for this may be the higher proportion of women on sick leave or temporarily laid off than men. The distribution of employment status and depression was similar between the genders. However, patients on sick leave or temporarily laid off were almost four times more likely to be depressed than those who were employed or were students. This may be explained by the fact that being out of work contributes to uncertainty in general and is a highly stressful situation for some.
All patients with IBD included in this study received biological treatment as monotherapy or in combination with immunosuppressants. This patient subgroup is the most vulnerable with respect to COVID-19, and changes in follow-up might create higher levels of both disease-related and general life stress. The patients receiving biological treatment comprised nearly half of the outpatients visiting our IBD unit at the hospital. Improved access to healthcare professionals with IBD specialist expertise and better facilitation of healthcare services may reduce depression and anxiety in this cohort of patients with IBD.
Strengths and limitations
This study was conducted early during the pandemic and included a well-defined and complete cohort of outpatients with IBD on biologics from a large university hospital. The proportion of non-responders was negligible, thus ensuring the very high generalizability of our results. However, this study was conducted early in the pandemic in a single center at an University Hospital in Norway. Therefore, the results may not be generalized to a general IBD population, and the patient experiences of the pandemic situation and the identified association to anxiety and depression may be affected by this. When a tailored information from the Norwegian authorities and the health care providers is available, the patients’ experiences may be different. Therefore, a follow-up study would be recommended. At the time of the study, no validated questionnaire regarding COVID-19 restrictions had been developed, and some of our questions may have been ambiguous.
COVID-19 restrictions was associated with anxiety and depression in patients with IBD undergoing biological treatment. Structural elements such as easy access to mail and telephone support, high-quality information, and disease advice from physicians regarding IBD are factors associated with lower levels of anxiety and depression. These results will help us to facilitate future healthcare services for patients with IBD and develop updated and evidence-based guidelines for routine follow-up in outpatient clinics.