Open Access Peer-reviewed Research Article

Sleep as a mediator in the context of emotional problems in adolescents with IBD: A pilot study

Main Article Content

Ann-Kristin Manhart corresponding author
Angelika A. Schlarb

Abstract

Background: Sleep has an impact on daily life. Particularly among adolescents with IBD, adequate sleep seems to be important, as the disease itself and the associated symptoms can cause distress and impair daytime functioning. However, often parental and youth reports differ regarding perceived sleep problems of adolescents. Besides sleep problems, depression and anxiety are often prominent in young IBD patients. To date, the interplay between sleep, anxiety/depression symptoms and IBD is not fully understood. Therefore, the aim of this study was to (1) evaluate sleep problems in adolescents suffering from IBD, (2) compare adolescents’ sleep quality and impairments according to self- and parental reports, and (3) investigate the interaction between IBD symptomatology, emotional problems and sleep disturbances.
Methods: 29 adolescents (age 10 - 22; M = 14.44 , SD = 1.78 ) with IBD and their parents took part in the study. Adolescents and parents completed questionnaires concerning sleep, emotional problems, and IBD symptomatology.
Results: Especially overtiredness, insomnia symptoms, and nightmares play a prominent role regarding sleep problems in youths. Self-rated sleep problems and parental ratings were inconsistent, particularly for nightmares (Z = -2.12; p = 0.034). However, other ratings concerning emotional problems and sleep, especially anxiety and nightmares, were significantly related(r = 0.426, p = 0.034), even though we found no mediation effect for the association between IBD, nightmares and anxiety.
Discussion: The present study revealed the importance of sleep and emotional well-being for adolescents suffering from IBD. Moreover, it became clear that the role of anxiety in youths suffering from IBD and sleep problems is not sufficiently answered yet. Not only emotional behavior but also sleep should be addressed when diagnosing IBD or during treatment of IBD. In addition, these results show the need for further investigation regarding the differences between parental and self-reports concerning sleep problems in young IBD patients.

Keywords
inflammation, pain, insomnia, nightmares, anxiety, daytime consequences

Article Details

Supporting Agencies
We acknowledge support for the Article Processing Charge by the Deutsche Forschungsgemeinschaft and the Open Access Publication Fund of Bielefeld University.
How to Cite
Manhart, A.-K., & Schlarb, A. (2021). Sleep as a mediator in the context of emotional problems in adolescents with IBD: A pilot study. Theory and Clinical Practice in Pediatrics, 3(1), 71-82. https://doi.org/10.25082/TCPP.2021.01.004

References

  1. Roth-Isigkeit A, Thyen U, St¨oven H, et al. Pain among children and adolescents: Restrictions in daily living and triggering factors. Pediatrics, 2005, 115: 152-162. https://doi.org/10.1542/peds.2004-0682
  2. Julie B and Daphne KM. Sleep and culture in children with medical conditions. Journal of Pediatric Psychology, 2010, 35(9): 915-926. https://doi.org/10.1093/jpepsy/jsq016
  3. Palermo TM, Toliver-Sokol M, Fonareva I, et al. (2007). Objective and subjective assessment of sleep in adolescents with chronic pain compared to healthy adolescents. Clinical Journal of Pain, 2007, 23(9): 812-820. https://doi.org/10.1097/AJP.0b013e318156ca63
  4. Palermo TM, Wilson AC, Lewandowski AS, et al. Behavioral and psychosocial factors associated with insomnia in adolescents with chronic pain. Pain, 2011, 152: 89-94. https://doi.org/10.1016/j.pain.2010.09.035
  5. Valrie CR, Bromberg MH, Palermo T, et al. A Systematic Review of Sleep in Pediatric Pain Populations. Journal of Developmental and Behavioral Pediatrics, 2013, 34(2): 120-128. https://doi.org/10.1097/DBP.0b013e31827d5848
  6. Forrest CB, Forrest KD, Clegg JL, et al. Establishing the content validity of PROMIS Peditric pain interference, fatigue, sleep disturbance, and sleep-related impairment measures in children with chronic kidney disease and Crohn’s disease. Journal of Patient-Reported Outcomes, 2020, 4: 11. https://doi.org/10.1186/s41687-020-0178-2
  7. Jarasvaraparn C, Zlomke K, Vann NC, et al. The realtionship between sleep disturbance, and disease activity in pediatric patients with inflammatory bowel disease. Journal of Pediatric Gastroenterology and Nutrition, 2019, 68(2): 237-243. https://doi.org/10.1097/MPG.0000000000002156
  8. Pirinen T, Kolho K-L, Ashorn M, et al. Sleep and Emotional and Behavioral Symptoms in Adolescents with Inflammatory Bowel Disease. Sleep Disorders. 2014, 3: 379-450. https://doi.org/10.1155/2014/379450
  9. Ohayon MM, Priest RG, Zulley J, et al. The place of confusional arousals in sleep and mental disorders: findings in a general population sample of 13,057 subjects. Journal of Nervous & Mental Disease, 2000, 188(6): 340-348. https://doi.org/10.1097/00005053-200006000-00004
  10. Ohayon MM and Roberts RE. Comparability of sleep disorders diagnoses using DSM-IV and ICSD classifications for adolescents. Sleep, 2001, 24(8): 920-925. https://doi.org/10.1093/sleep/24.8.920
  11. Schlarb AA, Kulessa D and Gulewitsch MD. Sleep characteristics, sleep problems, and associations of self-efficacy among German university students. Nature and Science of Sleep, 2012, 4: 1-7. https://doi.org/10.2147/NSS.S27971
  12. Schlarb A, Bihlmaier I, Hautzinger M, et al. Nightmares and associations with sleep quality and self-efficacy among university students. Journal of Sleep Disorders and Management, 2015, 1(2): 1-5. https://doi.org/10.23937/2572-4053.1510006
  13. Johnson EO, Roth T, Schultz L, et al. Epidemiology of DSM-IV insomnia in adolescence: lifetime prevalence, chronicity, and an emergent gender difference. Pediatrics, 2006, 117(2): e247-e256. https://doi.org/10.1542/peds.2004-2629
  14. Kirmil-Gray K, Eagleston JR, Elizabeth G, et al. Sleep disturbance in adolescents: Sleep quality, sleep habits, beliefs about sleep, and daytime functioning. Journal of Youth and Adolescence, 1984, 13(5): 375-384. https://doi.org/10.1007/BF02088636
  15. Patten CA, Choi WS, Gillin JC, et al. Depressive symptoms and cigarette smoking predict development and persistence of sleep problems in US adolescents. Pediatrics, 2000, 106(2): e23-e23. https://doi.org/10.1542/peds.106.2.e23
  16. Ohayon MM and Roth T. Place of chronic insomnia in the course of depressive and anxiety disorders. Journal of Psychiatric Research, 2003, 37(1): 9-15. https://doi.org/10.1016/S0022-3956(02)00052-3
  17. Schlarb AA, Liddle CC and Hautzinger M. JuSt - a multimodal program for treatment of insomnia in adolescents: a pilot study. Nature & Science of Sleep, 2011, 3: 13-20. https://doi.org/10.2147/NSS.S14493
  18. Bihlmaier I and Schlarb AA. Sleep-efficacy and sleep problems. A pilot study comparing sleepdisordered and healthy school-age children. Somnologie, 2016, 20(4): 275-280. https://doi.org/10.1007/s11818-016-0085-1
  19. Roeser K, Eichholz R, Schwerdtle B, et al. Relationship of sleep quality and health-related quality of life in adolescents according to self- and proxy ratings: A questionnaire survey. Front Psychiatry, 2012, 3: 76. https://doi.org/10.3389/fpsyt.2012.00076
  20. Zschoche M and Schlarb AA. Is there an association between insomnia symptoms, aggressive behavior, and suicidality in adolescents? Adolescent Health, Medicine and Therapeutics, 2015, 6: 29-36. https://doi.org/10.2147/AHMT.S76511
  21. Van de Vjiver E, Van Gils A, Beckers L, et al. Fatigue in children and adolescents with inflammatory bowel disease. World Journal of Gastroenterology, 2019, 25(5): 632-643. https://doi.org/10.3748/wjg.v25.i5.632
  22. Liu X and Zhou H. Sleep duration, insomnia and behavioral problems among Chinese adolescents. Psychiatry Research, 2002, 111(1): 75-85. https://doi.org/10.1016/S0165-1781(02)00131-2
  23. Tynj¨al¨a J and Kannas L. Sleeping habit of Finnish schoolchildren by sociodemographic background. Health Promotion International, 1993, 8(4): 281-289. https://doi.org/10.1093/heapro/8.4.281
  24. Vignau J, Bailly D, Duhamel A, et al. Epidemiologic study of sleep quality and troubles in French secondary school adolescents. Journal of Adolescent Health, 1997, 21(5): 343-350. https://doi.org/10.1016/S1054-139X(97)00109-2
  25. Bloom BJ, Owens JA, McGuinn M, et al. Sleep and its relationship to pain, dysfunction, and disease activity in juvenile rheumatoid arthritis. The Journal of Rheumatology, 2002, 29(1): 169-173. https://doi.org/10.1300/J094v10n01_21
  26. Bruni O, Fabrizi P, Ottaviano S, et al. Prevalence of sleep disorders in childhood and adolescence with headache: a case-control study. Cephalalgia, 1997, 17(4): 492-498. https://doi.org/10.1046/j.1468-2982.1997.1704492.x
  27. Iovino P, Tremolaterra F, Boccia G, et al. Irritable bowel syndrome in childhood: visceral hypersensitivity and psychosocial aspects. Neurogastroenterology & Motility, 2010, 21(9): 940-974. https://doi.org/10.1111/j.1365-2982.2009.01303.x
  28. Qazi T and Farraye FA. Sleep and Inflammatory Bowel Disease: An Important Bi-Directional Relationship. Inflammatory Bowel Diseases, 2018, 25(5): 843-852. https://doi.org/10.1093/ibd/izy334
  29. Edwards RR, Almeida DM, Klick B, et al. Duration of sleep contributes to next-day pain report in the general population. Pain, 2008, 137: 202-207. https://doi.org/10.1016/j.pain.2008.01.025
  30. Lewin DS and Dahl RE. Importance of sleep in the management of pediatric pain. Journal of Developmental & Behavioral Pediatrics, 1999, 20(4): 244-252. https://doi.org/10.1097/00004703-199908000-00007
  31. O’Brien EM, Waxenberg LB, Atchison JW, et al. Intraindividual variability in daily sleep and painratings among chronic pain patients: bidirectional association and the role of negative mood. Clinical Journal of Pain, 2011, 27: 425-433. https://doi.org/10.1097/AJP.0b013e318208c8e4
  32. Zimmerman J. Extraintestinal symptoms in irritable bowel syndrome and inflammatory bowel diseases: nature, severity, and relationship to gastrointestinal symptoms. Digestive Diseases and Sciences, 2003, 48(4): 743-749. https://doi.org/10.1023/A:1022840910283
  33. Guan Q. A Comprehensive Review and Update on the Pathogenesis of Inflammatory Bowel Disease. Journal of Immunology Research, 2019: 7247238. https://doi.org/10.1155/2019/7247238
  34. Benchimol EI, Fortinsky KJ, Gozdyra P, et al. Epidemiology of pediatric inflammatory bowel disease: a systematic review of international trends. Inflammatory Bowel Diseases, 2011, 17(1): 423-439. https://doi.org/10.1002/ibd.21349
  35. Guilfoyle SM, Gray WN, Herzer-Maddux M, et al. Parenting stress predicts depressive symptoms in adolescents with inflammatory bowel disease. European Journal of Gastroenterology & Hepatology, 2014, 26(9): 964-971. https://doi.org/10.1097/MEG.0000000000000149
  36. Amre DK, Lu SE, Costea F, et al. Utility of serological markers in predicting the early occurrence of complications and surgery in pediatric Crohn’s disease patients. American Journal of Gastroenterology, 2006, 101: 645-652. https://doi.org/10.1111/j.1572-0241.2006.00468.x
  37. Bousvaros A, Sylvester F, Kugathasan S, et al. Challenges in pediatric inflammatory bowel disease. Inflammatory Bowel Diseases, 2006, 12: 885-913. https://doi.org/10.1097/01.mib.0000228358.25364.8b
  38. Dubinsky MC, Lin YC, Dutridge D, et al. Serum immune responses predict rapid disease progression among children with Crohn’s disease: immune responses predict disease progression. American Journal of Gastroenterology, 2006, 101: 360-367. https://doi.org/10.1111/j.1572-0241.2006.00456.x
  39. Selemon LD. A role for synaptic plasticity in the adolescent development of executive function. Translational Psychiatry, 2013, 3: e238-e238. https://doi.org/10.1038/tp.2013.7
  40. Engelmann G, Erhard D, Petersen M, et al. Health-related quality of life in adolescents with inflammatory bowel disease depends on disease activity and psychiatric comorbidity. Child Psychiatry & Human Development, 2015, 46(2): 300-307. https://doi.org/10.1007/s10578-014-0471-5
  41. Filipovic BR, Filipovic BF, Kerkez M, et al. Depression and anxiety levels in therapy-naive patients with inflammatory bowel disease and cancer of the colon. World Journal of Gastroenterology, 2007, 13(3): 438. https://doi.org/10.3748/wjg.v13.i3.438
  42. Gamwell KL, Baudino MN, Bakula DM, et al. Perceived Illness Stigma. Thwarted Belongingness, and Depressive Symptoms in Youth With Inflammatory Bowel Disease (IBD). Inflammatory Bowel Disease, 2018, 24(5): 960-965. https://doi.org/10.1093/ibd/izy011
  43. Stapersma L, van den Brink G, Szigethy EM, et al. Systematic review with meta-analysis: anxiety and depression in children and adolescents with inflammatory bowel disease. Alimentary Pharmacology and Therapeutics, 2018, 48(5): 496-506. https://doi.org/10.1111/apt.14865
  44. Acosta-Ram´ırez D, Pag´an-Ocasio V, Torres EA, et al. Profile of the inflammatory bowel disease patient with depressive disorders. Puerto Rico Health Sciences Journal, 2001, 20(3): 215-220.
  45. Kurina LM, Goldacre MJ, Yeates D, et al. Depression and anxiety in people with inflammatory bowel disease. Journal of Epidemiology and Community Health, 2001, 55(10): 716-720. https://doi.org/10.1136/jech.55.10.716
  46. Mackner LM and Crandall WV. Long-term psychosocial outcomes reported by children and adolescents with inflammatory bowel disease. American Journal of Gastroenterology, 2005, 100(6): 1386-1392. https://doi.org/10.1111/j.1572-0241.2005.41428.x
  47. De Vijver E, Van Gils A, Beckers L, et al. Fatigue in children and adolescents with inflammatory bowel disease. World Journal of Gastroenterology, 2019, 25(5): 632-643. https://doi.org/10.3748/wjg.v25.i5.632
  48. Micocka-Walus AA, Turnbull DA, Moulding NT, et al. Controversies surrounding the comorbidity of depression and anxiety in inflammatory bowel disease patients: A literature review. Inflammatory Bowel Diseases, 2007, 13(2): 225-234. https://doi.org/10.1002/ibd.20062
  49. Ananthakrishnan AN, Long MD, Martin CF, Sandler RS, et al. Sleep disturbance and risk of active disease in patients with Crohn’s disease and ulcerative colitis. Clinical Gastroenterology and Hepatology, 2013, 11: 965-971. https://doi.org/10.1016/j.cgh.2013.01.021
  50. Sobolewska-Wlodarczyk A, Wlodarczyk M, Banaski J, et al. Sleep disturbances and disease activity in adult patients with inflammatory bowel disease. Journal of Physiology and Pharmacology, 2018, 69(3): 423-428. https://doi.org/10.26402/jpp.2018.3.09
  51. Ranjbaran Z, Keefer L, Stepanski E, et al. The relevance of sleep abnormalities to chronic inflammatory conditions. Inflammation research, 2007, 56(2): 51-57. https://doi.org/10.1007/s00011-006-6067-1
  52. Manhart AK, Hellmann S, Hamelmann E, et al. The association of sleep with inflammatory bowel disease in children and adolescents. Somnologie, 2016, 20(3): 212-218. https://doi.org/10.1007/s11818-016-0067-3
  53. Mackner LM, Sisson DP and Crandall WV. Review: psychological issues in pediatric inflammatory bowel disease. Journal of Pediatrics Psychology, 2004, 29(4): 243-257. https://doi.org/10.1093/jpepsy/jsh027
  54. Starpersma L, van den Brink G, van der Ende J, et al. Illness Perception and Depression Are Associated with Health-Related Quality of Life in Youth with Inflammatory Bowel Disease. Inflammatory Bowel Disease, 2019, 26: 415-426.
  55. Pirinen T, Kolho KL, Simola P, et al. Parent and Self-Report of Sleep-Problems and Daytime Tiredness Among Adolescents With Inflammatory Bowel Disease and Their Population-Based Controls. Sleep, 2010, 33(11): 1487-1493. https://doi.org/10.1093/sleep/33.11.1487
  56. Szigethy E, McLafferty L and Goyal A. Inflammatory bowel disease. Child and Adolescent Psychiatric Clinics of North America, 2010, 19(2): 301-318. https://doi.org/10.1016/j.chc.2010.01.007
  57. M¨ahlmann L, Gerber M, Furlano RI, et al. Impaired objective and subjective sleep in children and adolescents with inflammatory bowel disease compared to healthy controls. Sleep Medicine, 2017, 39: 25-31. https://doi.org/10.1016/j.sleep.2017.08.015
  58. Loonen HJ, Grootenhuis MA, Last BF, et al. Measuring quality of life in children with inflammatory bowel disease: The Impact II (NL). Quality Life Research, 2002, 11: 47-56. https://doi.org/10.1023/A:1014455702807
  59. Achenbach TM. Manual for the Child Behavior Checklist/4-18 and 1991 profile. Burlington: Department of Psychiatry, University of Vermont, 1991a.
  60. Achenbach TM. Manual for the Youth-Self Report and 1991 Profile. University of Vermont, Department of Psychiatry; Burlington VT: 1991b.
  61. Alfano CA, Ginsburg GS and Kingery JN. Sleep-related problems among children and adolescents with anxiety disorders. Journal of the American Academy of Child and Adolescent Psychiatry, 2007, 46(2): 224-232. https://doi.org/10.1097/01.chi.0000242233.06011.8e
  62. Beck AT, Epstein N, Brown G, et al. An inventory for measuring clinical anxiety: psychometric properties. Journal of consulting and clinical psychology, 1988, 56(6): 893.
  63. Kovacs M. Rating scales to assess depression in school-aged children. Acta paedopsychiatrica, 1981, 46: 305-315. https://doi.org/10.1007/BF00583513
  64. Beck AT, Steer RA and Brown GK. BDI-II, Beck Depression Inventory: Manual (2nd ed.) Boston; Harcourt Brace, 1996.
  65. Field A. Discovering statistics using IBM SPSS statistics. 4th eds. London: Sage, 2013.
  66. Preacher KJ and Hayes AF. Asymptotic and resampling strategies for assessing and comparing indirect effects in multiple mediator models. Behavior Research Methods, 2008, 40(3): 879-891. https://doi.org/10.3758/BRM.40.3.879
  67. Hayes AF. Introduction to mediation, moderation, and conditional process analysis: A regressionbased approach. New York, NY: Guilford Press, 2013.
  68. Pirinen T, Kolho KL, Ashorn M, Aronen ET. Sleep and Emotional and Behavioral Symptoms in Adolescents with Inflammatory Bowel Disease. Sleep Disorders, 2014.
  69. Mindel JA and Barrett KM. Nightmares and anxiety in elementary-aged children: is there a relationship? Child Care Health & Development, 2002, 28(4): 317-322. https://doi.org/10.1046/j.1365-2214.2002.00274.x
  70. Carskadon MA, Harvey K, Duke P, et al. Pubertal changes in daytime sleepiness. Sleep, 1980, 2: 453-460. https://doi.org/10.1093/sleep/2.4.453
  71. Carskadon MA, Viera C and Acebo C. Association between Puberty and Delayed Phase Preference. Sleep, 1993, 16(3): 258-262. https://doi.org/10.1007/BF02257418
  72. Dahl RE and Carskadon MA. Sleep and its disorders in adolescence. In: Ferber R, Kryger M (eds). Principles and Practice of Sleep Medicine in the Child. Philadelphia: WB Saunders & Co., 1995: 19-27.
  73. Blagrove M, Farmer L and Williams E. The relationship of nightmare frequency and nightmare distress to well-being. Journal of Sleep Research, 2004, 13(2): 129-136. https://doi.org/10.1111/j.1365-2869.2004.00394.x
  74. Schredl M, Fricke-Oerkermann L, Mitschke A, et al. Longitudinal study of nightmares in children: stability and effect of emotional symptoms. Child Psychiatry and Human Development, 2009, 40(3): 439-449. https://doi.org/10.1007/s10578-009-0136-y
  75. Velten-Schurian K, Hautzinger M, Poets CF, et al. Association between sleep patterns and daytime functioning in children with insomnia: The contribution of parent reported frequency of night waking and wake time after sleep onset. Sleep Medicine, 2010, 11(3): 281-88. https://doi.org/10.1016/j.sleep.2009.03.012
  76. Hysing M, Sivertsen B, Stormark KM, et al. Sleep in children with chronic illness and the relation to emotional and behavioral problems-a population-based study. Journal of Pediatric Psychology, 2009, 34(6): 665-670. https://doi.org/10.1093/jpepsy/jsn095
  77. Belicki K. Nightmare frequency versus nightmare distress: relations to psychopathology and cognitive style. Journal of Abnormal Psychology, 1992, 101(3): 592. https://doi.org/10.1037/0021-843X.101.3.592
  78. Wiechers S, Schlarb AA, Urschitz MS, et al. Sleep problems and poor academic performance in primary school children. Somnologie, 2011, 15(4): 243-248. https://doi.org/10.1007/s11818-011-0535-8
  79. Engstr¨om I. Mental health and psychological functioning in children and adolescents with inflammatory bowel disease: a comparison with children having other chronic illnesses and with healthy children. Journal of Child Psychology and Psychiatry, 1992, 33(3): 563-582. https://doi.org/10.1111/j.1469-7610.1992.tb00891.x
  80. Gray WN, Denson LA, Baldassano RN, et al. Treatment adherence in adolescents with inflammatory bowel disease: the collective impact of barriers to adherence and anxiety/depressive symptoms. Journal of Pediatrics Psychology, 2012, 37(3): 282-291. https://doi.org/10.1093/jpepsy/jsr092
  81. Reigada LC, Bruzzese JM, Benkov KJ, et al. Illness-specific anxiety: Implications for functioning and utilization of medical services in adolescents with inflammatory bowel disease. Journal for Specialists in Pediatric Nursing, 2011, 16(3): 207-215. https://doi.org/10.1111/j.1744-6155.2011.00292.x
  82. Barkin RM. Acute infectious diarrhea in children. Postgraduate Medicine, 2009, 65(2): 173-179. https://doi.org/10.1080/00325481.1979.11715060
  83. Benhayon D, Youk A, McCarthy FN, et al. Characterization of relations among sleep, inflammation, and psychiatric dysfunction in depressed youth with Crohn’s disease. Journal of Pediatric Gastroenterology & Nutrition, 2013, 57(3): 335-342. https://doi.org/10.1097/MPG.0b013e31829641df
  84. Thompson RD, Craig AE, Mrakotsky C, et al. Using the Children’s Depression Inventory in youth with inflammatory bowel disease. Comprehensive Psychiatry, 2012, 53: 1194-1199. https://doi.org/10.1016/j.comppsych.2012.04.006