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The Role of Telehealth Services in Children with Cystic Fibrosis During Coronavirus Disease 2019 Outbreak

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Introduction

The coronavirus disease 2019 (COVID-19) pandemic caused by the novel coronavirus SARS-CoV-2 has resulted in an ongoing public health crisis.1 Many studies show that the clinical manifestations of COVID-19 are primarily related to the respiratory system.2–4 Cystic fibrosis (CF) is a multisystemic disease, and the primary causes of morbidity and mortality in CF patients are respiratory complications and CF-related chronic diseases.3 These problems can cause a range of psychological symptoms in pediatric CF patients and their caregivers.5–7 It is known that pediatric CF patients and their caregivers have higher depression and anxiety scores than the general population.8–10

Viral respiratory tract infections cause more severe illness in children with CF than in their healthy peers. The number of CF patients who have been diagnosed with COVID-19 currently remains low,11 making it difficult to make conclusions about the impact of COVID-19 infection on CF patients. In healthy individuals COVID-19 can be mild, but in individuals with significant respiratory problems, the risk of more severe illness increases.11 Respiratory infections can cause weight loss in CF patients and, therefore, tracking their nutritional status is of critical importance.12

The present study aimed to monitor the health status and nutritional status in pediatric CF patients during the COVID-19 pandemic, as measured via telehealth services. Additional aims were to determine the level of anxiety in the patients and their caregivers during the pandemic, and to determine the COVID-19 transmission status in the patients.

Materials and Methods

This prospective cross-sectional study included 144 pediatric CF patients, their caregivers, and 49 healthy age- and gender-matched controls, their caregivers. The study was performed at Istanbul University, Cerrahpaşa School of Medicine, Department of Pediatric Gastroenterology, Hepatology, and Nutrition, and Department of Pediatric Pulmonology, Istanbul, Turkey. Inclusion criteria for patients included follow-up for CF at our center for ≥1 year. Exclusion criteria for CF patients were total or partial gastrectomy, a history of solid organ transplantation, and requiring administration of intravenous antibiotics or oxygen supplementation. There were 176 eligible CF patients; however, the study included the 144 patients that were regularly contacted via telehealth services follow-up.

The hospital’s CF team supported the patients via remote contact, including dedicated telephone lines. Regular CF appointments were conducted via telehealth services during the COVID-19 pandemic, from March 11, 2020 to December 1, 2020. The inpatient team was on site, but only saw patients face-to-face when absolutely necessary. The telehealth services team consisted of two pediatric gastroenterologists, two pediatric pulmonology specialists, one CF dietitian, and one nurse who performed a mix of inpatient and outpatient work.

As a decrease in nutritional status in pediatric CF patients can cause a decrease in health status, the caregivers of patients were asked to measure their children’s weight, which was then compared to the z-scores last measured in hospital. Body mass index-for-age (BMI-FA) z-score were calculated using the WHO Anthro Program v.3.2.2 (January 2011) for children aged >5 years.

Via telehealth services a general questionnaire was administered to pediatric CF patients’ caregivers who collected data on daily life, clinical symptoms, and medical problems. This questionnaire included questions about disease exacerbations, access to medicines, patient and family history of contact with confirmed COVID-19 cases, compliance with prescribed diet, and compliance with the COVID-19 guidelines recommended by the Turkish Ministry of Health (see in Supplementary Data S1). The general questionnaire was administered by clinicians affiliated with the CF care team to identify problems experienced by the patients and their families, and to determine the health status of the patients during the pandemic. This questionnaire was not validated because we did not have resources on COVID-19 outbreak, but was used for an earlier study conducted at our hospital.13 We adapted this questionnaire for use with CF patients (see in Supplementary Data S2).

The Hospital Anxiety and Depression Scale (HAD) and general questionnaire were administered to the patients’ and controls’ caregivers via telehealth services. The State-Trait Anxiety Inventory (STAI) was administered to CF patients and controls aged >8 years via telehealth services. HAD and STAI were administered by a clinician during medical health care interviews conducted via video calls.

The control group included patients who presented to the Cerrahpaşa Pediatric Clinic for such acute reasons as upper respiratory tract infection or vaccination. Inclusion criteria for the controls were aged 8–18 years, no chronic or acute disease. The patient and control groups were administered the same questionnaires. The caregivers of the patients and controls provided written informed consent. The study protocol was approved by the Ethics Committee of Istanbul University Cerrahpaşa School of Medicine (approval no. 29430533-604).

Correlations between the anxiety status in the CF patients and the anxiety-depression status in their caregivers were statistically examined. The same correlations were also analyzed in the controls and their caregivers. In all, 49 pediatric CF patients had adequate intellectual ability and education to complete STAI. The control group included 49 children to match the 49 patients aged >8 years.

Statistical Analysis

Data were analyzed using IBM SPSS Statistics for Windows v.21.0 (IBM Corp., Armonk, NY). Associations between the study variables were measured via Pearson’s chi-square test, the Mann-Whitney U test, and Student’s t-test. The level of statistical significance was set at p < 0.05.

Results

Descriptive Findings

The study included 144 pediatric patients (74 males and 70 females) and their caregivers. Mean age of the patients was 8.9 years. The study also included 49 controls (29 females, 20 males) with a mean age of 9.2 ± 2.1 years (range: 8–12 years). There was a mean 4.33 individuals per patient household, with a mean age of 30.9 years. Among the patients, 15 had a decrease in appetite, of which 90% had exacerbations and 80% were hospitalized. In total, 50% of the patients (mean age: 8.81 years) had no change in appetite and 30.5% (mean age: 10.42 years) had an increase in appetite. There was not a significant difference between patient age groups based on Student’s t-test.

In all, 101 of the patients did not have any CF-related symptoms, whereas 43 did, including cough (n = 16), fever (n = 12), wheezing and shortness of breath (n = 8), nasal obstruction (n = 6), stomachache (n = 6), nausea (n = 6), diarrhea (n = 4), and constipation (n = 2). Moreover, 22 of the patients reported via telehealth services that they had greasy stool. Among the caregivers of the patients, 98.02% never considered stopping their children’s regular medication. Among the patients, 70 came to the hospital for face to face visits, during which time their height and weight were recorded. Descriptive characteristics of the patients are presented in Table 1.

Table 1. Descriptive Findings and Clinical Features in the Patient Group
  NUMBER, MEAN (%) P
Age 8.9  
Gender
 Male 74 (51.39)  
 Female 70 (48.61)  
CF medication   <0.001
Compliance
 Yes 128 (88.9)  
 No 16 (11.1)  
Hospitalized cases
 Yes 12 (8.3)  
 No 132 (91.7)  
Difficulty accessing medications   <0.001
 Yes 26 (18.1)  
 No 118 (81.9)  
Patients had appetite loss   <0.001
 Yes 23 (16.0)  
 No 121 (84.0)  
Symptoms   0.03
 Fever 12  
 Cough 16  
 Wheezing 8  
 Shortness of breath 8  
 Nasal obstruction 6  
 Diarrhea 4  
 Constipation 2  
 Greasy stool 22  
 Nausea 6  
 Stomachache 6  

COVID-19-Positive Cases

In total, 42 (29.2%) of the CF patients were tested for COVID-19 via polymerase chain reaction (PCR), of which 4 were positive. Among those 42 patients, 28 were tested due to COVID-19-positive cases in their family, of which only 3 were positive. In all, 14 of the CF patients were tested for COVID-19 due to the presence of COVID-19 symptoms; only 1 was positive, 3 quarantined at home because they did not have any COVID-19 symptoms, and 1 was treated in hospital due to clinical symptoms of COVID-19. The characteristics of the COVID-19-positive CF patients are shown in Table 2.

Table 2. Characteristics of Coronavirus Disease 2019-Positive Cystic Fibrosis Patients
  CASE 1 CASE 2 CASE 3 CASE 4
Age (years) 1.2 5.8 3 6
Gender (F/M) F F F M
Symptoms
 Fever No No Yes No
 Cough No No Yes No
 Nausea/vomiting No No Yes No
 Diarrhea No No No No
Pneumonia No No No No
HFA z-score 1.09 –1.01 –1.39 1.25
WFA z-score 0.37 –0.87 –2.26 2.00
WFH z-scorea   –0.59 –2.00  
Body mass index for age z-score –0.44 –0.41 –1.93 1.83
Hospitalization No No Yes No
Chronic colonization with Pseudomonas aeruginosa No No Yes No
Dornase alpha compliance Yes Yes Yes Yes
Vitamin A, D, E, and K use Yes Yes Yes Yes
Pancreatic insufficiency Yes Yes Yes Yes
CFRD No No No No

As we could not confirm the complaints of the patients via telehealth services, suspected patients were invited to the clinic for a COVID-19 test; the PCR test was used as a diagnostic test. Samples were collected from suspicious patients via the nasopharyngeal swab and oropharyngeal swab method. Although the test was negative, we did not have a patient diagnosed with computed tomography (CT) findings or any other methods.

STAI and HAD

STAI was administered to the 49 CF patients aged >8 years. The STAI-S score in all 49 patients was above the cutoff value (normal <45). The mean State-Trait Anxiety Inventory-State (STAI-S) score was significantly lower in the patient group than in the control group (p < 0.001). STAI-S scores were significantly higher in the male CF patients than in the controls and female CF patients. STAI-S scores showed that adolescent patients were more anxious than the younger CF patients and the controls (see in Table 3). In addition, adolescents with CF had a significantly higher STAI-S score than their healthy peers and CF patients aged 8–14 years. Similarly, State-Trait Anxiety Inventory-Trait (STAI-T) scores were higher in the control group than in the patient group. In contrast to STAI-S findings, STAI-T scores did not differ significantly according to age in the patient group. In addition, there was no significant difference in STAI-T scores between the patients and controls.

Table 3. The Mean State-Trait Anxiety Inventory Values in the Patient and Control Groups
SUBSCALES PATIENTS, N = 49 MEAN ± SD CONTROLS, N = 49 MEAN ± SD Pa
STAI-S 27.91 ± 6.78 41.73 ± 10.4 <0.001
Gender
 Male 67.32 ± 31.46 39.40 ± 2.16 0.52
 Female 29.04 ± 4.93 43.95 ± 10.45  
Age groups
 8–14 years 28.38 ± 8.57 43.09 ± 8.26 0.03
 14–18 years 58.6 ± 34.57 40.16 ± 11.81  
STAI-Trait 31.71 ± 3.37 44.68 ± 7.35 <0.001
Gender
 Male 31.71 ± 3.94 44.80 ± 5.39 0.12
 Female 31.96 ± 2.16 44.57 ± 8.96  
Age groups
 8–14 years 34.14 ± 4.45 44.14 ± 6.31 0.17
 14–18 years 31.8 ± 3.82 45.32 ± 8.52  

HAD was administered to the caregivers of 144 CF patients and the caregivers of 140 healthy controls. The mean HAD anxiety score in the patients’ caregivers was significantly higher than in the controls’ caregivers (p = 0.005). The mean HAD depression score was also significantly higher in the patients’ caregivers than in the controls’ caregivers (p < 0.001). Table 4 presents HAD scores difference between the caregiver’s group.

Table 4. Mean Hospital Anxiety and Depression Scale Scores in the Patient and Control Groups’ Caregivers
TESTS CAREGIVERS OF PATIENTS (N = 140) CAREGIVERS OF CONTROLS (N = 144) Pa
HAD anxiety 11.15 ± 4.46 7.76 ± 3.76 0.005
HAD depression 12.72 ± 4.62 6.45 ± 4.17 <0.001

Nutritional Status

The patients’ BMI-FA z-scores before and after the COVID-19 pandemic were compared. BMI for age z-scores in the CF patients improved significantly during the pandemic (p = 0.002). There was significant weight gain in the patients during the pandemic (p < 0.001), as 74.3% (n = 107) of the patients gained weight. Moreover, 11.8% of the patients maintained their current weight and 13.8% lost >3% of their weight; these patients reported having CF-related symptoms. Nutritional status was compared according to age groups and gender. In total, 82.8% of the females improved their z-scores while 7.1% of the them did not. Among the female patients, 10% lost >3% of their weight. Among the male patients, 66.2% improved their z-scores, while 16.2% did not change their weight during the outbreak. In all, 17.6% of the male patients lost >3% of their weight. There was no significant difference between the genders in the patient group.

Discussion

The burden of COVID-19 is increasing worldwide and is thought to be greater in individuals with chronic diseases. In addition, it is predicted that COVID-19 will be more aggressive in patients with CF, as the virus affects the respiratory tract and can cause more severe disease in those with a compromised immune system. The present study aimed to remotely monitor pediatric CF patients during the COVID-19 pandemic.

Patients in the present study were contacted by phone greater than or equal to two times during the study period by the telehealth services team. In general, we evaluate pediatric CF patients in our clinic every 3 months, depending on their health status; however, the present study period was 3 months and our patients were remotely followed-up greater than or equal to two times to monitor their nutritional status and health status during the COVID-19 pandemic.

The present findings show that there were no significant problems in the supply of CF drugs or their use during the pandemic (p < 0.001 and p = 0.001, respectively). The present findings also show that during the pandemic, there was not an increase in the frequency of CF symptoms or a decrease in appetite (p = 0.03 and p < 0.001, respectively). Based on these findings, we think that pediatric CF patients in Turkey are not affected by these problems due to well-organized treatment protocols, such as extending the health reports of those with chronic diseases, delivering medicines to those with chronic diseases, and regular patient contact.

According to the last spirometry measurements, performed just before the COVID-19 pandemic, the mean FEV1 value was 92.9%, which may be one of the reasons why our patients maintained their health status during the pandemic. Another reason could be the effectiveness of our telehealth services. The reason behind the comfortable recovery of our patients with COVID-19 positivity can be attributed to the good progress of their general clinics; however, as these patients were aged <7 years, we could not remotely measure their respiratory functions via spirometry, which is why these FEV1 findings are not provided. In addition, Dornase alpha is a known effective treatment for COVID-19.14 Dornase alpha was prescribed to 94.8% of the present study’s CF patients, which might account for the low incidence of COVID-19 positivity and rapid recovery of the patients with COVID-19 positivity.

Studies have shown that patients with chronic diseases are not infected with COVID-19 at a higher rate than the general population.15 In the present study, only 4 of 144 pediatric CF patients were COVID-19 positive. We think that the COVID-19 positivity rate was low because as the patients had a chronic disease, their caregivers were careful about keeping them isolated. The number of COVID-19-positive CF patients in the study was too small to make a comparison with those that were COVID-19 negative; however, it was noted that among the four COVID-19-positive cases, three were infected via familial contact and were asymptomatic. On the contrary, it was observed that the 1 symptomatic COVID-19 patient had a significantly low BMI for age z-score and Pseudomonas aeruginosa colonization.

It is clear that the COVID-19 pandemic psychologically affects individuals of all ages, which is probably related to fear and anxiety.16–18 Even though some studies have reported that patients with CF have higher levels of anxiety than healthy controls,19 CF patients are born with the disease, struggle with infections from the onset, routinely use masks, and must take medicines daily without interruption; therefore, the effects of the pandemic, such as masking and disinfecting hands, could be expected to have less of a negative effect on children with CF than their healthy peers. In the present study, STAI-S and STAI-T scores in the CF patient group were significantly lower than in the control group (p < 0.001 and p < 0.001, respectively), which is in accordance with earlier reports.20

Symptoms of anxiety are more common in adolescents and adults than in the general population.21 In the present study, anxiety scores were significantly higher in the 14- to 18-year-old CF patients than in the younger ones. Similarly, it was reported that adolescents with non-CF bronchiectasis had higher STAI-S scores than their healthy peers.22,23 Children with CF routinely experience exacerbation of lung symptoms, which can increase their anxiety level during the COVID-19 pandemic; however, high anxiety levels in healthy children may be due to the fact that they have not encountered any serious illness before the COVID-19 pandemic. STAI-T and STAI-S scores in the present study’s CF patients aged 8–14 years did not differ from those in their healthy peers, which might have been due to the fact that the patients were used to having lung problems.

In the present study, HAD anxiety and HAD depression scores in the caregivers of the CF patients were higher than in caregivers of the controls, as previously reported.24 As the presence of an accompanying chronic illness that primarily affects the immune and respiratory systems would likely increase the anxiety level to a greater degree in the caregivers of healthy children, this was an expected finding.25

Malnutrition was reported to be an independent factor that negatively affects survival.26 One of the aims of the present study was to determine the nutritional status of the CF patients via telehealth services and intervene as necessary. The findings show that the CF patients significantly improved their nutritional status during the COVID-19 pandemic (p = 0.002), which might have been due to two reasons. The first is that the patients attended school online due to the pandemic and spent more time at home than usual; consequently, their caregivers could more easily monitor their food intake. The other reason might be that the CF care team continued routine follow-up remotely, which reduced the patients’ and caregivers’ anxiety and increased their confidence in managing CF-related complications.

Conclusions

Telehealth is an innovative method for providing health care services while avoiding the risk of exposure to and spread of COVID-19. Telehealth services reduce CF patients’ and caregivers’ anxiety and increase their confidence in managing CF-related complications. The present findings show that children with CF are affected more than the healthy controls in terms of anxiety and highlight the fact that they require psychiatric evaluation and psychosocial support.

Authors’ Contributions

O.F.B. and E.P.U.K. were involved in the conception and design and data analysis of the study. E.H. and A.A.K.S. preformed the data analysis. A.D.T collected the data with support from T.D.D., H.Ç., and F.Ç.Ç helped supervise the article. All authors approved the final article as submitted and gave final approval of this version.

Disclosure Statement

No competing financial interests exist.

Funding Information

No funding was received for this article.

Supplementary Material

Supplementary Data S1

Supplementary Data S2

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