Introduction: Psychiatric disorders, especially anxiety, are considered extraintestinal manifestations of celiac disease (CD). Objective: This study aims to evaluate the level of anxiety in treated patients with CD in Iran. Methods: A total of 283 CD patients (190 female, 93 male) were enrolled in a study during 2016–2018 from 9 centers in Iran. The Zung Self-Rating Anxiety Scale questionnaire was completed. The anxiety index was calculated. Also, demographic data and the duration of treatment with a gluten-free diet (GFD) were recorded. Data were analyzed by SPSS version 20. Results: Anxiety symptoms were reported in 67.8% of patients. Female patients had a higher anxiety index than male patients. Duration of treatment with a GFD did not influence the anxiety index (17.3% were on a GFD for <1 year, 33.6% for 1–2 years, and 49.1% had GFD for >2 years; p = 0.86). Conclusions: These results suggest that anxiety symptoms are common among patients, especially females, with CD in Iran and GFD duration has no effect on their improvement.

Celiac disease (CD) is the most common gluten-related disease and the result of both environmental and genetic factors. This chronic disease is characterized by small intestine villous atrophy, due to the ingestion of gluten. CD is diagnosed by serological tests and intestinal biopsy [1]. The worldwide prevalence of CD is 1% in the general population and 0.3–2.9% in children, with marked geographical variation [2]. In Iran, the prevalence of CD is considered to be 1% in the general population [3, 4].

CD can develop at any age and present with a wide variety of gastrointestinal and non-gastrointestinal symptoms. Furthermore, some CD patients may be asymptomatic [5]. Common presentations of CD include chronic diarrhea, malabsorption, abdominal pain, weight loss, and steatorrhea. Extraintestinal symptoms include hair loss, mouth ulceration, and fatigue. Studies have suggested that CD is associated with psychiatric conditions, such as anxiety, depression, and mood disorders, and, in rare cases, suicide has been reported in patients with CD [6-10]. This chronic disorder affects not only health but also the patient’s overall well-being and quality of life. Depression and anxiety are the most common psychiatric conditions, diagnosed in adults and pediatric CD patients [11, 12]. The mechanisms underlying the development of mental health problems in patients with CD remain uncertain. Some studies have suggested mechanisms including a deficiency of amino acids such as tryptophan [13-15] and central serotonin hypofunction [16] as possible causes. Alternative etiological factors may include cerebral hypoperfusion, vitamin deficiency due to malabsorption, or hyper-homocysteinemia. Hyper-homocystinuria might compromise the blood-brain barrier [17-19]. Other studies have suggested that patient anxiety and depression could relate to the perception of the illness, treatment, and concerns regarding socializing with others and a feeling of loneliness and worry [20, 21].

The effect of gluten-free diet (GFD) on psychological symptoms such as anxiety remains uncertain, but some researchers have suggested that anxiety may improve after starting a GFD [22, 23]. Some researchers have claimed that celiac patients have a higher risk of anxiety than the general population. Butwicka et al. [24] suggested that pediatric patients with CD have a 1.4-fold higher risk of psychiatric disorders than healthy children. A study by Fera et al. [25] revealed that CD patients suffered from higher anxiety and depression rates than the controlled group. The aim of this study is to evaluate the level of anxiety among Iranian patients with CD and the effect of a GFD.

Participants

This was a nationwide study that recruited 283 asymptomatic CD patients, on a GFD, from seven cities across different parts of Iran (Tehran in the center, Sari and Gorgan in the north, Ilam in the west, Mashhad in the east, Gonabad in the northeast, and Tabriz in the northwest) and who had been admitted to outpatient clinics from October 2016 to February 2018. Patients were diagnosed by gastroenterologists according to positive serological tests (tTG-IgA) and histological data of small intestinal biopsy based on Marsh criteria [26].

Materials and Procedure

In our study, we used a questionnaire. The questionnaire contained two parts. The first part related to demographic information such as age, gender, education level, marital status, family history of CD, and duration of GFD, and the second part consisted of 20 anxiety assessment questions. The second part contained questions regarding anxiety symptoms and the Zung Self-Rating Anxiety Scale to assess the prevalence and quantify anxiety symptoms. Within the 20 anxiety assessment questions, five enquired about affective symptoms like anxiety, fear, panic, and mental disintegration. The other 15 enquired about somatic symptoms such as tremor, body pain, weakness, restlessness, palpitation, dizziness, faintness, dyspnea, nausea and vomiting, urinary frequency, sweating, face flushing, insomnia, and nightmare.

Patients scored each question from 1 to 4 (based on the following replies: a little part of the time, some part of the time, a good part of the time, most of the time). The total score ranged from 20 to 80. An anxiety index score was calculated for each patient. The anxiety index score was used to determine each patient’s anxiety level using the following values [27, 28]:

  • 20–44, normal range

  • 45–59, mild to moderate anxiety levels

  • 60–74, marked to severe anxiety levels

  • 75–80, extreme anxiety levels

The questionnaire was distributed in celiac clinics to patients, aged older than 15 years, who were attending for a routine checkup and were willing to participate in this study. The study was approved by the ethics committee of the Research Institute for Gastroenterology and Liver Disease, Shahid Beheshti University of Medical Science, Tehran, Iran and all participants signed the consent form.

Data Analyses

The statistical package for social sciences (SPSS version 20 for Windows) was used for the statistical analysis. The variables in this study included sex (male, female), age (>30, <30), marital status (married, single), history of CD (yes, no), duration of GFD (less than 1 year, between 1 and 2 years, more than 2 years), and educational achievement. The educational level includes illiterate, under diploma (categorized as the low educational group), diploma, and academic (categorized as high educational group). The variables’ values were given as the mean, standard deviation, minimum, and maximum. Independent samples t test was applied as a parametric test to compare two groups of continuous variables with normal distribution, and Leven’s test was used to compare two groups of variables without normal distribution. Numerical data were processed by ANOVA and nominal data utilizing t test, applying Yates correction when required. Also, Mann-Whitney nonparametric test was performed for ordinal variables. All data were presented as mean and with a 95% confidence interval of difference. A p value of <0.05 was considered to be significant in this study.

The study population included 283 patients, of whom 190 were women (67.1%). The participants were between 15 and 66 years of age, and the mean age of the study group was 32.5 ± 14.5 years. 44.2% (125) were less than 30 years of age. 55.1% of patients (156) were married and 16.6% (47) reported a family history of CD. 37.8% (176) of patients were in the low educated level group. In terms of the duration of the GFD, 17.3% (49) reported less than 1 year, 33.6% (95) between 1 and 2 years, and 49.1% (139) had been on the diet for more than 2 years. 83.4% of patients (236) were resident in an urban area. The demographics between males and females were not significantly different. However, the duration of the GFD was longer in females, compared to males (p = 0.02) (Table 1).

Table 1.

Distribution of demographic factors according to number (percent) among males and females

Distribution of demographic factors according to number (percent) among males and females
Distribution of demographic factors according to number (percent) among males and females

The anxiety index in our study population was high, with a mean percentage of 52.08% (mean score = 41.67, min. percent = 25 and max. percent = 92.5). According to the anxiety index, only 32.2% of patients had a normal level of anxiety, 41% had a mild to moderate level of anxiety, 19.4% had severe anxiety, and 7.4% had extreme anxiety levels.

Multivariate analysis revealed that anxiety rate was significantly higher for women than men. Other demographic factors indicated no significant association with anxiety index; specifically, there was no relationship between anxiety index and the GFD duration (p = 0.86). The results are presented in Table 2.

Table 2.

Comparison of anxiety percent in celiac disease patients by gender, marital status, family history of celiac disease, age, education level, and duration of gluten-free diet

Comparison of anxiety percent in celiac disease patients by gender, marital status, family history of celiac disease, age, education level, and duration of gluten-free diet
Comparison of anxiety percent in celiac disease patients by gender, marital status, family history of celiac disease, age, education level, and duration of gluten-free diet

The effect of gender on each anxiety scale question was studied using the Mann-Whitney test. Feeling upset or panicky was higher in women, compared to men (p = 0.007). Also, suffering with a feeling of physical shaking in arms and legs (p = 0.002), experiencing headaches, neck and back pain (p = 0.001), experiencing feelings of numbness and tingling in fingers and toes (p < 0.001) and dizzy spells (p = 0.02), and experiencing hot flushes in their face (p = 0.007) were higher in women (Table 3).

Table 3.

Mean scores of the Zung anxiety scale in celiac disease (CD) patients divided by gender

Mean scores of the Zung anxiety scale in celiac disease (CD) patients divided by gender
Mean scores of the Zung anxiety scale in celiac disease (CD) patients divided by gender

The results of this study showed that anxiety symptoms are frequent among Iranian CD patients and their frequency is higher among women than men. In particular, women reported physical signs of anxiety, such as tremors of arms and legs, headaches and back pain, numbness of extremities, dizzy spells, and a flushed face more frequently than men.

However, other variables under examination, such as the duration of treatment with a GFD, did not influence the presence of anxiety symptoms. To our knowledge, this is the first study on the topic in the Middle East.

Psychiatric symptoms such as anxiety and depression are potentially challenging extraintestinal symptoms that can occur before or after a diagnosis of CD [29]. The mechanisms of anxiety associated with CD are not fully understood. Tryptophan deficiency and central serotoninergic hypofunction are possible causes [10]. Addolorato et al. [11] have suggested that anxiety is probably due to being affected by a chronic disease, but the depressive symptoms may be a characteristic of CD [15]. Some researchers have suggested that CD patients, both adults and children, are more predisposed to anxiety than the general population [30]. In the first report, Hallert and Derefeldt [31] in 1982 showed evidence of a relationship between CD and psychiatric disorders. Butwicka et al. [24] showed that children with CD have a 1.4-fold higher risk of anxiety than healthy children and childhood CD is identified as a risk factor for anxiety disorders. Fera et al. [25] evaluated the level of anxiety by State-Trait Anxiety Inventory (STAI) questionnaires in CD patients. They reported higher levels of anxiety than healthy controls. In the study by Addolorato et al. [32], 75% of CD patients were positive for state anxiety, and 52.3% of CD patients were positive for trait anxiety, based on the STAI test. In our survey, anxiety was at 52.08% (mean score: 41.67), and this high anxiety level is in agreement with former studies.

Some investigations have shown no relationship between the anxiety complaints observed in CD patients and demographics such as gender, age, and educational level variables [33]. For example, Fera et al. [25] revealed that anxiety did not depend on demographic variables (age, gender, education, employment status). Some investigations described a higher level of anxiety in female CD patients compared to males. Our results showed that female CD patients feel more upset, panicky and have more somatic symptoms than male CD patients. Jansson-Knodell et al. [34] reported that the prevalence of intestinal and extraintestinal manifestations of CD is higher in women. Hallert et al. [35] believed that women express more concerns and worries about the impact of the disease on their social relations, and they have difficulty managing their disease. Our findings are consistent with the results of that study.

As the duration of a GFD for women was significantly longer than for men in our study, we hypothesize that this variable may affect the higher prevalence of anxiety in women. Addolorato et al. [29] and Ciacci et al. [15] claimed that anxiety levels decrease after starting a GFD, but depression symptoms remain. Campagna et al. [36], in their review, believed that a GFD is useful in the treatment of depression, anxiety, and neurological complications. The finding contrasts with studies that have reported no association between depression/anxiety and GFD compliance. Furthermore, studies have suggested that treatment with a GFD does not prevent the development of depression or anxiety [25, 37, 38]. In the study by Zingone et al. [39], a GFD did not induce any improvement in the STAI scores between untreated CD patients and CD patients on a GFD. Similar to the study by Zingone et al. [39], our results confirmed that the duration of a GFD had no noticeable effect on anxiety. This finding is in contrast with the study by Addolorato et al. [29], which found a significant improvement in anxiety after 1 year on a GFD. One possible explanation is that patients diagnosed with CD in Iran may struggle to fully comply with a GFD because “gluten-free products” may be inaccessible or very expensive. There may also be undefined contamination of gluten-free products. So subsequent studies could target the compliance of GFD and the accessibility to “gluten-free products” to clarify their potential impact on a patient’s anxiety.

In conclusion, we observed a high incidence of anxiety among the Iranian CD population, especially more frequently in women than men, with no association with age, marital status, family history, educational state, or duration of a GFD. In light of the present results, gastroenterologists and healthcare professionals should provide psychiatric support to CD patients. As anxiety in CD women on a GFD is higher than in men, screening for anxiety in CD women both at diagnosis and also on a GFD should be considered. Besides, since the prevalence of CD is high in Iran, CD screening among patients with anxiety would be recommended as an effective protocol for finding new cases of CD in Iran and psychiatrists could pay attention to this disorder as a cause of psychiatric symptoms.

We appreciate the Shahid Beheshti University of Medical Sciences, Tehran, Iran.

The study was approved by the ethics committee of the Research Institute for Gastroenterology and Liver Disease, Shahid Beheshti University of Medical Science, Tehran, Iran and all participants signed informed consent.

There is no conflict of interest.

This study was supported by National Institute for Medical Research Development (Grant No. 971025).

M. Rostami-Nejad and M.A. Pourhoseingholi provided the research topic and design the method. M. Rostami-Nejad, M.A. Pourhoseingholi, N. Taraghikhah, C. Ciacci, and F. Barzegar collected data and prepared the datasheet. M. Rezaei-Tavirani, D. Aldulaimi, and M. Reza Zali consulted the study. All authors contributed equally in manuscript writing and revising the final version.

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N. Taraghikhah is equal to the first author.

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