Evaluation of anti-COVID-19 measures taken by the parents of children with celiac disease: a cross-sectional study

ABSTRACT BACKGROUND: Coronavirus disease 2019 (COVID-19) causes negative life changes brought about through lockdowns, in addition to severe complications and death. Among these changes, asplenism or hyposplenism has been reported in patients with celiac disease. It has been reported that the risk of pneumococcal sepsis is higher in celiac patients with hyposplenism. Moreover, celiac patients present high risk of admission to hospital due to influenza. OBJECTIVE: To determine the degree of awareness of COVID-19 among parents of children with celiac disease and examine the measures that they take. DESIGN AND SETTING: Cross-sectional study at a university hospital in the Middle Anatolian region of Turkey. METHODS: The diagnosis of celiac disease was confirmed through a survey conducted online among 73 parents between May and July 2020. RESULTS: The mean age was 37.57 ± 6.56 years for the mothers, 41.15 ± 5.56 years for the fathers and 11.36 ± 4.36 years for the children. 90.4% of the parents reported that COVID-19 was transmitted through “speaking, coughing, sneezing and infection of the face after contact with virus-infected surfaces”. Moreover, 78.1% indicated that they did not have any difficulty in finding gluten-free foods. CONCLUSION: These parents of children with celiac disease believed that their children’s risk of developing COVID-19 did not differ from that of healthy children. It was also observed that appetite and states of nervousness were higher among these children with celiac disease during lockdowns and that their sleep patterns were affected.

The Celiac Disease Foundation has proposed that, in the present pandemic situation, individuals with celiac disease should maintain stocks of gluten-free foods and should make gluten-free meal plans and train themselves to use new gluten-free recipes. Moreover, this foundation has underlined the need for celiac patients to stay away from crowds and to stay at home, in order to minimize their exposure to the virus. 11 Defective spleen function is frequently seen in autoimmune gastrointestinal diseases such as celiac disease. As it is well known that celiac patients are at high risk of developing sepsis with encapsulated bacteria, pneumococcal vaccination is recommended. 9,12 Asplenism or hyposplenism has been also reported in celiac patients, along with gastrointestinal symptoms. It has also been reported that the risk of pneumococcal sepsis is higher in celiac patients with hyposplenism. 13 Mårild et al. reported that celiac patients were at higher risk of hospital admissions due to influenza. Celiac patients experience anxiety and depression due to the increased risk of infection. 14 Moreover, lockdown conditions and limitations during the pandemic, along with fear of the difficulties that may be experienced in trying to find gluten-free foods, increase anxiety.
Celiac disease is a chronic disease that has leads to the risk of sepsis and hospitalizations due to influenza, and the risk of pneumococcal sepsis due to hyposplenism that patients may experience.
For this reason, patients with celiac disease need to be more careful in terms of the precautions to be taken in preventing COVID- 19, which is known to cause severe complications. Since the daily life requirements of children with celiac disease will be controlled by their parents, the measures taken by parents for their children were evaluated in this study.

OBJECTIVE
This study was carried out to determine the degree of awareness of COVID-19 among the parents of children with celiac disease and the measures that they take.

METHODS
This was a cross-sectional study that was conducted among the parents of patients aged 4-18 years who had been diagnosed with celiac disease in the pediatric gastroenterology outpatient clinic of a health sciences university in Afyonkarahisar, Turkey. The diagnosis of celiac disease was made based on serological tests to detect immunoglobulin A (IgA)-tissue transglutaminase IgA (tTGA) and/or immunoglobulin G (IgG)-tissue transglutaminase IgG (tTGG); and on and histological examination of small-intestine mucosal biopsies. Data for this study were collected by means of a questionnaire, which was generated online and could be completed within 10 minutes, between May 2020 and July 2020.
We arbitrarily decided to include the parents of patients with celiac disease who were undergoing regular follow-up at the study hospital. We included the mothers or fathers of children in the 0-18 age group with celiac disease. We collected data using a semi-structured questionnaire (this questionnaire is presented in the Appendix). The questionnaire was created based on up-to-date information from the literature. The parents who agreed to participate in the study were asked to fill out a demographic information form consisting of 17 questions and an information form relating to COVID-19 infection that included 34 questions. Although our aim was to reach a total of 150 parents, only 73 parents who agreed to participate and who were contacted through the internet were included in the study.
The data obtained were assessed by means of descriptive statistics (arithmetic mean, median, standard deviation and percentage distribution). Means were compared between groups and the compliance of the data with normal distribution was analyzed using the Shapiro-Wilk test. An independent-sample t test was used for parametric data and the Mann-Whitney U test was used for nonparametric data. The chi-square test was used to compare percentage distributions of categorical variables between groups.
The analyses on the data were conducted using the IBM SPSS Statistics™ software, version 20.0 (IBM Corporation, Armonk, NY).
The results were analyzed within a 95% confidence interval and P < 0.05 was considered to be statistically significant.
Approval for this study was obtained from the clinical research ethics committee of the local medical school (5.5.20/ 2011-KAEK-2/2020/186). All the participants in this study gave written consent for their inclusion.
Within the last month, 15 patients (20.5%) had had a weight gain of less than one kilogram, 17 patients (23.3%) had not had any weight change, 39 patients (53.4%) had had a weight gain of more than one kilogram and two patients (2.7%) had had a weight loss of more than one kilogram.
Among the families, 24 (32.9%) were living in a village, 14 (19.2%) were living in a town and 35 (47.9%) were living in a city center. Sixty-seven families (91.8%) were nuclear families and 6 (8.2%) were extended families. Among all the families participating in this study, four (5.5%) had one child, 28 (38.4%) had two children, 30 (41.1%) had three children and 11 (15.1%) had four or more children. Fifty-two families (71.2%) had health insurance and 21 (28.8%) did not. Thirty-four families (46.6%) indicated that they had experienced a loss of income during this pandemic period. The parents' education levels and employment statuses are shown in Table 1.
In response to the question "Do you think that your child has a greater risk of developing coronavirus disease (COVID-19) compared with other children?", 53.4% of the parents answered "yes" and 46.6% answered "no". No statistically significant difference was found between the mothers and fathers (P = 0.46).
"How should your child behave while coughing or sneezing?" was answered as "use the area inside the elbow while sneezing" by 75.3%, "use a napkin or handkerchief if available" by 23.3% and "use the back of the hand" by 1.4% of the parents.
19.2% of the individuals participating in the survey were found to have pets in their homes. They answered the question "Is coronavirus disease (COVID-19) transmitted from pets?" as "yes" by 37% and "no" by 63%.
The question "Which of the following precautions is effective in preventing transmission of coronavirus disease (COVID-19)?" was responded as "washing hands frequently with soap and water" by 17.8%, "staying away from people showing flu-like symptoms" by 1.4% and "washing hands frequently with soap and water, cleaning hands with alcohol-based disinfectants, avoiding face-to-face contact and staying away from people showing flulike symptoms" by 80.8%.
"Is the spread of coronavirus disease (COVID-19) affected by air temperature change?" was answered as "yes" by 93.4% and as "no" by 6.6% of the participants.
"What is the minimum alcohol content (%) that disinfectants need to have in order to kill the viral factor that causes coronavirus disease (COVID-19)?" was answered as "disinfectants containing at least 70% alcohol" by 72.6%.
"Is there a specific medication to treat coronavirus disease (COVID-19)?" was answered as "no" by 89% of the participants. The question "For at least how long should hands be washed in order to kill the viral factor that causes coronavirus disease (COVID-19)?" was answered as "20 seconds" by 94.5%.
"What do you use to clean common areas in your home (tables, stairs, door handles, light switches, counters, toilets, taps and sinks) in order to prevent transmission of coronavirus disease (COVID-19)?" was answered as "bleach" by 57.5%, "disinfectants containing 70% alcohol" by 19.2% and "vinegar" by 23.3%.
The question "What have you been using to clean places such as the toilet and bathroom in your home during the coronavirus disease (COVID-19) pandemic?" was answered as "1/100 diluted bleach" by 97.3% and "disinfectant containing 70% alcohol" by 2.7%.
The question "Have you been going out from your home for any reasons other than your urgent needs or for work during the coronavirus disease (COVID-19) pandemic?" was answered as "no" by 50.7% of the participants.
"Have you been allowing your child to go out from your home during the coronavirus disease (COVID-19) pandemic?" was answered as "no" by 78.1% of the parents included in the study.
"From where do you mostly get news about the coronavirus disease (COVID-19) pandemic?" was answered as "television" by 68.5, "internet" by 30.1% and "I do not follow the news" by 1.1%.
The question "Do you clean materials bought or brought from outside before using them, because of the coronavirus disease (COVID-19) pandemic?" was answered as "yes" by 95.9%.
"Have you been paying attention to social distancing rules during interactions with individuals outside your home during the coronavirus disease (COVID-19) pandemic?" was answered as "yes" by 98.6%.
"Have you been using a mask while going out during the coronavirus disease (COVID-19) pandemic?" was answered as "yes" by 98.6% of the parents. No relationship could be found between the education levels of the parents and their responses (P > 0.46).
"What should be the social distance in order to prevent transmission of coronavirus disease (COVID-19)?" was answered as "1-2 meters" by 97.3%.
"Have you been having any problems in finding foods for your child (gluten-free foods) during the coronavirus disease "Which of the following symptoms increased in your child with the closure of schools due to coronavirus disease (COVID-19)?" was answered as "no complaint" by 42 (57.5%), "state of nervousness" by 24.6%, "increase in appetite" by 13.6%, "lack of appetite" by 8.21%, "headache" by 6.84%, "stomach ache" by 4.1%, "increase in hair loss" by 2.73%, "allergic skin rash" by 2.73%, "having nightmares and scary dreams" by 1.36%, "nausea" by 1.36% and "constipation" by 1.36%. There were no mentions of abdominal distension, diarrhea or vomiting complaints in the answers.
"Has your child had any sickness requiring medication (like antibiotics), such as flu, cold or urinary tract infection, in the past month?" was answered as "no" by 94.5%.
"Has your child's sleep pattern and quality changed in the past month?" was answered as "increase in sleep duration" by 8.2% of the parents, "decrease in sleep duration" by 6.8%, "change in sleep pattern" by 43.8% and "no effect on sleep pattern" by 41.1%.
Among the answers given by the parents to the questions regarding COVID-19, a statistically significant difference was found only in relation to their preference for mask use, and this is shown in The details of the survey questionnaire and survey responses are shown in the Appendix. Fifty-nine parents (80.8%) indicated that "washing hands frequently with soap and water, cleaning the hands with alcohol-based disinfectants, avoiding face contact and staying away from people with flu-like symptoms" were important for prevention of transmission of COVID-19. Moreover, washing hands "for 20 seconds" was reported to be important by 94.5% of them. In the study by Pal et al., 53% of the participants stated that staying at home, ensuring that they paid attention to social distancing and doing regular hand washing were important for prevention of transmission of COVID-19. 17 72.6% of the parents in the present study stated that "disinfectants containing at least 70% alcohol" should be used in order to kill coronavirus, and 57.5% indicated that they cleaned common areas at home (tables, chairs, door handles, light switches, counters, toilets, taps and sinks) with bleach in order to In our study, we found that 78.1% of the parents of celiac patients did not experience any problems in finding gluten-free foods for their children during the lockdown, and they did not have any difficulties in complying with their children's gluten-free dietary needs. Since routine daily activities such as going to school were interrupted during the lockdown, the children became bored.

DISCUSSION
With boredom, they found solace through foods rich in fat, carbohydrates and proteins, which supplied them with large amounts of calories. Furthermore, hearing or reading news about the pandemic created distress and increased their likelihood of consuming certain foods. 19 Excessive intake of macronutrients during a lockdown situation causes lack of micronutrients and development of obesity.
We also found that 53.4% of the children with celiac disease had had a weight gain of more than one kilogram in the last month. The parents surveyed in the present study indicated that they preferred mainly garlic, kefir, oranges, kiwi fruit, spinach, fish, broccoli and pickles for strengthening their children's immune systems.
Taking immune-boosting foods and balanced planning of meals and portions have been also recommended for patients with celiac disease. Especially cellular immunity, phagocyte function, cytokine production, antibody response, antibody affinity and disturbance in complement system make patients with celiac disease more susceptible to viral infections. During a pandemic situation, consumption of foods containing high amounts of antioxidants, vitamins and minerals strengthens the immune system. 19 In this study, 58.9% of the parents surveyed here stated that their children's sleep patterns changed. It has been reported that social isolation during lockdowns causes sleep disorders through increasing anxiety and stress and that this also increases food intake. 19,22 In this study, we evaluated the parents' levels of knowledge about COVID-19 and the measures that they took in relation to their children. In addition, we evaluated these children's access to a gluten-free diet within their daily lives and their sleep and nutrition patterns during this period. The questions were multiple-choice and open-ended, so as not to affect the answers given by the parents.
The limitations of this study were the small sample size, the lack of a control group and the fact that it was conducted in a single center. We were aware that parents' feelings about their children's behaviors would possibly be heightened and that, therefore, their answers might be unintentionally biased. Therefore, we avoided asking directional questions.

CONCLUSION
This study is important with regard to determining the awareness of COVID-19 among parents who have children with celiac disease and examining the precautions that they take. The results from this study showed that these parents thought that their children with celiac disease did not present a risk of getting COVID-19 that differed from the risk among healthy children. This finding revealed that the parents of children with celiac disease should be informed more about the COVID-19 pandemic. It was seen that the children's state of nervousness and associated state of weight gain were found to be affected by the lockdown that was applied to prevent the spread of COVID-19. This lockdown situation had a negative effect on the conditions required to maintain a healthy lifestyle.