International Journal of Rheumatic Diseases 2014

ORIGINAL ARTICLE

Assessment of sleep problems in children with familial Mediterranean fever Balahan MAKAY,1 Serdar Kamer KILIC ß ASLAN,2 Ahmet ANIK,2 Elcßin BORA,3 1 € € Ozlem BOZKAYA,3 Tufan C ß ANKAYA3 and Erbil UNSAL 1 3

Division of Rheumatology, Department of Pediatrics, Faculty of Medicine, Dokuz Eyl€ ul University, Departments of 2Pediatrics, and Medical Genetics, Izmir, Turkey

Abstract Aims: This study aimed to investigate sleep patterns, sleep disturbances and possible factors that are associated with sleep disturbances among children with familial Mediterranean fever (FMF). Patients and methods: Fifty-one patients with FMF and 84 age- and sex-matched healthy controls were enrolled in the study. The patients who had an attack during the last 2 weeks were not included. Demographic data, FMF symptoms, disease duration, dose of colchicine, disease severity score, number of attacks in the last year, MEFV mutation and serum C-reactive protein (CRP) levels were recorded for each patient. A Children’s Sleep Habits Questionnaire was performed. Results: The total sleep scores of the patients with FMF were significantly higher than the control group. Total sleep durations were similar between FMF patients and controls. Children with FMF had significantly higher scores regarding sleep-onset delay, sleep anxiety, night wakings and sleep-disordered breathing when compared to healthy controls. There was a significant positive correlation between number of attacks in the last year and sleep onset delay, night wakings and sleep disordered-breathing. Disease severity score and CRP levels were not associated with any of the subscale scores. The patients with exertional leg pain had significantly higher total sleep scores than the ones without. Furthermore, patients with exertional leg pain had significantly higher subscale scores regarding sleep onset delay, parasomnias and sleep-disordered breathing. Conclusion: This study showed for the first time that children with FMF had more sleep disturbances than their healthy peers. Higher numbers of attacks and exertional leg pain were associated with poor sleep quality. In conclusion, this study underlines the need to assess and manage sleep problems in children with FMF. Key words: familial Mediterranean fever, sleep disturbances, sleep patterns.

INTRODUCTION Familial Mediterranean fever (FMF) is the most common inherited autoinflammatory disease around the world. It is characterized by recurrent episodes of fever and serositis, particularly peritonitis, pleuritis and arthritis.1 Autosomal recessively inherited mutations in the Correspondence: Dr Balahan Makay, MD, Associate Professor, Division of Rheumatology, Department of Pediatrics, Dokuz Eyl€ ul University Hospital, 35340 Balcßova, Izmir, Turkey. Email: [email protected]

MEFV (FMF) gene, which encode pyrin or marenostrin, are the genetic causes of this disease.2 Elevation of acute phase reactants during FMF attacks as well as attack-free periods are well documented in the literature.3,4 FMF is a lifelong disorder requiring continuous treatment with colchicine.5,6 Although current treatments have greatly improved the health status of patients with FMF, this condition is associated with significant morbidity in some cases, such as amyloid nephropathy.7,8 Sleep disturbances are much more prevalent among medically ill children and adolescents when compared

© 2014 Asia Pacific League of Associations for Rheumatology and Wiley Publishing Asia Pty Ltd

B. Makay et al.

with the general population and the presence of co-morbidity may adversely affect medical outcomes and quality of life (QoL) of these patients.9–15 Although the prevalence and impact of sleep problems have been described in several chronic rheumatological conditions such as rheumatoid arthritis,12,13 fibromyalgia,12,13 juvenile idiopathic arthritis,14 juvenile dermatomyositis14 and systemic lupus eryhthematosus,15 much less is known about FMF. Reports of sleep problems in children are particularly important because nocturnal sleep disturbances have been associated with daytime behavioral problems, inattention, poor school performance and reduced health-related QoL.16,17 Given the lack of data regarding the nature of sleep problems in FMF patients, the objective of this study was, with an objective and reliable tool, to investigate sleep patterns, sleep disturbances and possible factors that are associated with sleep disturbances among children with FMF.

PATIENTS AND METHODS Study population This study was conducted in Dokuz Eyl€ ul University Faculty of Medicine, Department of Pediatrics, Division of Rheumatology; Izmir Turkey, between October 2011 and November 2012. Participants included children and adolescents (6–17 years old). Fifty-one patients (28 females and 23 males) with FMF and 84 healthy controls (38 females and 46 males) were enrolled in the study. The healthy controls were selected from the children who visited the ‘well child outpatient clinic’ of the department. FMF patients fulfilled the Tel-Hashomer criteria.18 MEFV mutations were identified in all patients. Fifteen of 51 patients were homozygous for M694V mutation and 14 other genotypes were present in the remaining 38 patients. All of the patients were on colchicine treatment and were not receiving any other regular treatment. The patients were enrolled in the study during an attackfree period. So, the patients who had an attack during the last 2 weeks were not included. None of the patients had enlarged tonsils, adenoid problems or morbid obesity, which may cause obstructive apnea. The clinical characteristics of the patients are given in Table 1. Eighty-four healthy children who were matched for age, sex, economic status, parental education and family structure constituted the control group. Mean age of the patients was 11.7  3.5 years and controls were 11  3.1 years (P = 0.2). No significant difference considering age and gender was found between the patients and the controls.

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Table 1 Demographics of familial Mediterranean fever (FMF) patients Variable Disease duration (years) Range Mean  SD No. of attacks in the last year, mean  SD Dose of colchicine (mg), mean  SD Severity score (%) 1 2 3 FMF symptoms (%) Fever Peritonitis Pleuritis Arthritis (episodic) Rash Exertional leg pain Acute scrotum (males) Nephropathy/ amyloidosis MEFV mutation (%) M694V/M694V Other

0.5–16 5.9  4.1 2.1  1.8 (min. 0, max. 8) 1.1  0.3 (min. 0.5, max. 2)

23% 67% 10% 82% 78% 30% 23% 14% 52% 13% 0%

29 71

Method A parent-reported sleep inventory was applied to all participants. The Children’s Sleep Habits Questionnaire (CSHQ) was the instrument used.19 The validity and reliability of the Turkish version of the CSHQ had been previously shown.20 The study protocol was approved by the ethics committee of the Dokuz Eylul University, Faculty of Medicine. Parents and children were informed about the scale and the procedure. Demographic data, disease duration, FMF symptoms, number of attacks in the last year, dose of colchicine, disease severity score, MEFV mutation and serum C-reactive protein (CRP) levels were recorded for each patient. The disease severity score was calculated according to the scoring system suggested by Pras et al.21 The starting dose of colchicine was 0.5 mg/day for children ≤ 5 years of age and 1.0 mg/day for children > 6 years. Colchicine dose was increased in a stepwise fashion (0.25 or 0.5 mg/step) up to a maximum of 2.0 mg/day to control disease in patients who did not clinically respond to the starting dose. The response to colchicine was evaluated according to previously suggested princi€ ples by Ben-Chetrit and Ozdo gan depending on the

International Journal of Rheumatic Diseases 2014

Sleep problems ın familial Mediterranean fever

decreasing rate of annual FMF attacks.22 If colchicine reduced the attack rate by 50%, we designated it as ‘FMF-50’ response. Excepting two patients (4%), all the patients achieved FMF-50 response.

Childrens Sleep Habits Questionnaire Children’s Sleep Habits Questionnaire is a parentreported questionnaire assessing the typical sleep patterns of preschool and school-age children. It includes 33 items measuring sleep disturbances and three items collecting information about bedtime, wake-up time and sleep duration (nighttime sleep and daytime nap) over a ‘typical’ recent week. If the patients have an extraordinary event in the week prior to the questionnaire, such as examination, competition and so on, parents are asked to fill it according to the nearest typical week. Parents rate the frequency of each item on a three-point Likert scale: ‘usually’ (5–7 times per week), ‘sometimes’ (2–4 times per week) and ‘rarely’ (0–1 time per week). Higher scores indicate more frequent sleep disturbances. The CSHQ yields a total sleep disturbance score and eight subscale scores: bedtime resistance, sleep-onset delay, sleep duration, sleep anxiety, night wakings, parasomnias, sleep disorder breathing and daytime sleepiness. A total score of ≥ 41 defines ‘clinically significant sleep disturbance’. ALthough developers have not established norms for the scale, they determined that a total score of 41 points makes an effective cutoff for screening purposes as it correctly identified 80% of the clinical sample in their initial psychometric study.19

Statistical analysis Data was evaluated using the Statistical Package for Social Sciences (SPSS Inc., Chicago, IL, USA) 15.0 program for Windows and by analyzing descriptive statistics (means, standard deviation), comparing the means of quantitative data for dual groups by using the Student t-test and Mann–Whitney U-test when appropriate. Chi-square test was used to evaluate the differences in proportions. CSHQ total sleep score was compared by gender using one-way analysis of variance (ANOVA). Games–Howell corrections were applied to control for multiple comparisons. Intercorrelations between parameters were computed through the Pearson’s correlation analysis. Correlation coefficient indicated low correlation at 0.10–0.29, medium correlation at 0.30–0.49 and high correlation at ≥ 0.50. P-values ≤ 0.05 were considered as significant. Internal consistency of the scale was determined by calculating Cronbach’s coefficient alpha. Scales with reliabilities of 0.70 or greater are recommended for comparing groups.

RESULTS Comparisons of patients and controls The total sleep scores of the patients with FMF were significantly higher than the control group (51.7  11.3 vs. 46.4  6.6, P = 0.001) (Table 2). Total sleep durations were similar between FMF patients and controls (9  1.4 vs. 8.8  1, P = 0.42) (Table 2). Table 2 shows the comparison of subscale scores among patients and controls. Children with

Table 2 Sleep parameters of patients and controls FMF patients (n = 51) Average bedtime (PM) Average waketime (AM) Length of wakings (min) Total sleep duration (h) Total sleep score Subscales Bedtime resistance Sleep-onset delay Sleep duration Sleep anxiety Nightwakings Parasomnias Sleep-disordered breathing Day-time sleepiness

22 : 23 07 : 32 9.7 9 51.7

    

1 : 01 1 : 16 18.1 1.4 11.3

8.8 2.2 3.8 6.1 4.7 8.9 4.1 14.3

       

4 2.4 1.4 2.4 1.5 2.2 1.7 5.2

Healthy controls (n = 84)

P-value†

22 : 17 07 : 36 3.1 8.8 46.4

    

0 : 56 0 : 50 3.6 1 6.6

0.55 0.67 0.001 0.42 0.001

7.7 1.4 3.9 5.3 3.9 8.8 3.4 14.5

       

2.2 0.6 1.3 1.7 1 1.8 0.8 3.8

0.048 0.005 0.546 0.018 0.001 0.878 0.002 0.835

FMF, familial Mediterranean fever. P-values in bold are significant. †Student’s t-test.

International Journal of Rheumatic Diseases 2014

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FMF had significantly higher scores regarding sleeponset delay, sleep anxiety, night wakings and sleep-disordered breathing when compared to healthy controls (P = 0.005, P = 0.018, P = 0.001 and P = 0.002, respectively) (Table 2). Younger age was associated with longer duration of sleep (r = 0.560, P < 0.001), higher rates of bedtime resistance (r = 0.226, P = 0.008), sleep anxiety (r = 0.244, P = 0.004), night wakings (r = 0.234, P = 0.006) and sleep disordered-breathing (r = 0.178, P = 0.04) in the whole study population. However, there was not a significant correlation between total sleep score and age (r = 0.141, P = 0.102). The total sleep scores of the male FMF patients were significantly higher than the female FMF patients, healthy males and healthy females (P = 0.036, P = 0.013 and P = 0.004, respectively). However, total sleep scores of the healthy males were not significantly different from female patients with FMF and healthy females (P = 0.983 and P = 0.789, respectively).

Relationships between FMF disease characteristics and sleep behaviors There was not a significant correlation between the total sleep score and disease duration (r = 0.017, P = 0.908), dose of colchicine (r = 0.028, P = 0.946), duration of colchicine use (r = 0.026, P = 0.85), disease severity score (r = 0.226, P = 0.008), number of attacks in the last year (r = 0.009, P = 0.959) and serum CRP levels (r = 0.003, P = 0.981) in FMF patients. There was a significant positive correlation between numbers of attacks in the last year and sleep onset delay (r = 0.537, P < 0.001), night wakings (r = 0.437, P = 0.003) and sleep disordered-breathing (r = 0.306, P = 0.044). Disease severity scores and CRP

levels were not associated with any of the subscale scores (data not shown). Six patients (14%) had mild, 31 (72%) had moderate and six (14%) had severe disease according to the scoring system. There were no significant differences regarding total sleep scores between patients with mild and moderate disease (P = 0.28), mild and severe disease (P = 0.2) and moderate and severe disease (P = 0.77). There were 26 patients (52%) who reported exertional leg pain. The patients with and without exertional leg pain were not significantly different regarding age and gender (P = 0.74 and P = 0.2, respectively). The patients with exertional leg pain had significantly higher total sleep scores than the patients without (54.8  11.3 vs. 46.3  7.8, P = 0.008). Furthermore, patients with exertional leg pain had significantly higher subscale scores regarding sleep onset delay, parasomnias and sleep disordered-breathing (P = 0.01, P = 0.02 and P = 0.04, respectively) (Table 3). The most prevalent genotype of this study was M694V/M694V; patients having this mutation were compared to patients having other genotypes. The total sleep scores of the patients homozygous for M694V were not significantly different from the others (P = 0.87). Internal consistency reliability alpha coefficient for CSHQ in the patient group and control group were 0.83 and 0.71, respectively.

DISCUSSION The results of this study indicated that patients with FMF had more sleep problems than their healthy peers. The patients with FMF reported higher scores of sleep onset delay, sleep anxiety, night wakings and sleep

Table 3 Subscale comparisons between familial Mediterranean fever (FMF) patients with and without exertional leg pain (ELP) Patients with ELP (Group 1) (n = 26) Total sleep score Bedtime resistance Sleep-onset delay Sleep duration Sleep anxiety Nightwakings Parasomnias Sleep-disordered breathing Day-time sleepiness

56.7 9 2.5 3.9 6.2 4.7 9.3 4.5 15.1

        

12 4.2 2.4 1.8 2.6 1.2 2.6 1.8 5.7

Patients without ELP (Group 2) (n = 25) 46.5 8.5 1.8 3.7 6.1 4.7 8.4 3.7 13.5

        

8 3.7 2.4 1 2.3 1.9 1.6 1.6 4.5

Healthy controls (Group 3) (n = 84) 46.4 7.7 1.4 3.9 5.3 3.9 8.8 3.4 14.5

        

6.6 2.2 0.6 1.3 1.7 1 1.8 0.8 3.8

P-value group comparisons†

1–2 (0.00), 2–3 (0.99), 1–3 (0.00) 1–2 (0.35), 2–3 (0.78), 1–3 (0.02) 1–2 (0.01), 2–3 (0.67), 1–3 (0.00) 1–2 (0.70), 2–3 (0.89), 1–3 (0.79) 1–2 (0.78), 2–3 (0.22), 1–3 (0.1) 1–2 (0.35), 2–3 (0.08), 1–3 (0.00) 1–2 (0.02), 2–3 (0.48), 1–3 (0.04) 1–2 (0.04), 2–3 (0.38), 1–3 (0.00) 1–2 (0.15), 2–3 (0.25), 1–3 (0.19)

P < 0.05 is significant and is resented in bold. †Mann–Whitney U-test.

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Sleep problems ın familial Mediterranean fever

disordered-breathing when compared to healthy controls. To the best of our knowledge, this is the first study investigating sleep patterns, sleep disturbances and possible factors that are associated with sleep disturbances among children with FMF. Therefore, there is no other study available as such to be compared with our results. € ßakar et al.23 investigating In a previous study by Ozc the influence of subclinical inflammation on daily life of FMF patients, the authors asked questions about four items concerning weakness, lack of appetite, unwillingness to do daily activities, and sleep problems before and at least 6 months after colchicine therapy. They defined sleep problems as ‘a decrease in the duration and quality of sleep’. Although they did not use a validated tool to assess sleep habits, they reported a significant decrease in the rate of sleep problems after colchicine therapy. They did not find a significant difference between patients having mild and moderate disease regarding sleep problems. Similarly, total sleep scores were not affected by disease severity in our study. Familial Mediterranean fever is a disease that might rarely cause debilitating physical effects such as chronic arthritis and chronic renal insufficiency, which would definitely cause sleep disturbances.14,24 However, none of the patients in this study had chronic arthropathy or nephropathy. FMF is a disease of recurrent painful serositis, which particularly presents with abdominal and chest pain. Further, a lot of FMF patients experience exercise-induced muscle pain lasting for a few hours to the whole day, mainly affecting the legs following physical exertion or even prolonged standing.25 Fifty-two percent of patients in this study had exertional leg pain. Previous studies demonstrated the negative impact of recurrent and chronic pain on sleep quality in children and adolescents.26–28 Furthermore, the association between pain and sleep disturbance may be bi-directional: pain contributes to disrupted sleep and sleep disturbance can likewise enhance pain perception.29–31 The results of this study suggested that exertional leg pain, a common manifestation of FMF, could itself impair the sleep quality of FMF patients. The patients with exertional leg pain reported higher scores regarding sleep onset delay, parasomnias and sleep disordered-breathing than the patients without. Exertional leg pain, which occurs after mild exercise or physical activity in a young and normally fit patient, is a characteristic clinical manifestation of FMF, included among the minor criteria for its diagnosis.18 Growing pains and fibromyalgia syndrome (FMS) are two conditions that may interefere with and even sometimes cannot be differantieted from FMF

International Journal of Rheumatic Diseases 2014

exertional leg pain. Growing pains are common among children aged 2–12 years and are characterized by recurrent, self-limited, bilateral lower extremity pain, mostly in the afternoon and evening of a day with intensive physical activity, in an otherwise healthy child.32 FMS is characterized by chronic, widespread pain in the muscles and joints which is also accompanied by a variety of other common symptoms, including sleep disturbance, fatigue and mood disorders.33 The current criteria for diagnosis of FMS relies on the scoring of 11/18 positive tender points plus widespread pain lasting for more than 3 months.34 There are several studies reporting increased frequency of FMS in FMF patients.35,36 Previously, Buskila et al.37 showed that QoL of adult FMF patients was negatively correlated with diffuse widespraid pain associated with fibromyalgia. Similarly, in another study assessing QoL of children with FMF, we found that the patients with myalgia had significantly lower QoL scores than patients without.38 We believe that muscle pains may contribute to both impaired QoL and sleep disturbances in FMF patients. This study further demonstrated that sleep quality of pediatric FMF patients is negatively affected by the number of attacks. Higher numbers of FMF attacks were associated with difficulty in falling asleep, more night wakings and sleep disordered-breathing. Sleep disturbances in pediatric FMF patients may be associated with underlying disease-related mechanisms, such as inflammation. Previous studies showed that inflammatory mediators effect the regulation of sleep in the central nervous system.39–41 Interleukin-6 (IL-6), a proinflammatory cytokine, elevation was shown to affect the organism, with a focus on sleep-related symptoms and fatigue.42,43 It is demonstrated that IL-6 was increased either during or between attacks in FMF patients.3,44 Although we could not demonstrate the effect of acute phase response (CRP levels) on sleep scores in this study, we believe that the positive correlation between the number of FMF attacks and sleep disturbances may point out underlying inflammation. Evidence supports an increased prevalence of obstructive sleep apnea in some rheumatic diseases, particularly rheumatoid arthritis.45 Patients with obstructive sleep apnea have also been found to have elevations in circulating acute phase reactants and pro-inflammatory cytokines. We showed for the first time that FMF patients had higher rates of sleep-disordered breathing as well. However, further studies are required to elicit the exact mechanism of sleep-disordered breathing in patients with FMF.

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Although the exact mechanism of the action of vitamin B12 on sleep disorders is unknown, administration of vitamin B12 was reported to normalize human sleep– wake rhythm disorders.46,47 Previous studies showed that colchicine might induce reversible vitamin B12 malabsorption by altering the function of ileal mucosa.48 However, we did not measure vitamin B12 levels, which might be associated with sleep disturbances in our patients. The strength of this study includes the use of a pediatric sleep habit questionnaire with previously demonstrated reliability and validity in pediatric rheumatic diseases. The limitations of this study include the small sample size and the inclusion of children who were all attending the same rheumatology clinic, which may limit the geographic, racial and ethnic diversity of the sample. As a result, it is necessary to be cautious when generalizing the results of this study to all children with FMF. Also, it would be optimal to assess the changes in sleep scores before and after colchicine therapy; however, in the present study all of the patients were already on colchicine therapy. In conclusion, this study underlines the need to assess and manage sleep problems in children with FMF. Clinical assessment of the nature of patients’ sleep disruptions is critical for individualizing interventions in FMF patients.

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Assessment of sleep problems in children with familial Mediterranean fever.

This study aimed to investigate sleep patterns, sleep disturbances and possible factors that are associated with sleep disturbances among children wit...
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