Skip to main content

Advertisement

SpringerLink
Log in

Relationship between nocturnal enuresis and sleep in children and adolescents

  • Systematic Review/Meta-analysis
  • Published:
Pediatric Nephrology Aims and scope Submit manuscript

Abstract

Background

Nocturnal enuresis (NE) is a multifactorial and complex condition. One less understood factor in its pathophysiology is the enuretic inability to wake up when the bladder is full (impaired arousal).

Objective

We aimed to investigate the relationship between sleep and NE in children and adolescents.

Methods

A systematic review was performed following the PRISMA guidelines, and the electronic databases MEDLINE (via PubMed) and SCOPUS were searched until March 2022. Eligibility criteria were studies that recruited patients aged five–17 years with a diagnosis of NE according to the International Child Continence Society (ICCS), Diagnostic and Statistical Manual of Mental Disorders—Fifth Edition (DSM-5), or International Classification Criteria of Sleep Disorders—Third edition (ICSD-3) who had their sleep assessed using validated questionnaires and/or polysomnography. The tool used to analyze the risk of bias in the included studies was the risk of bias in non-randomized studies of exposure.

Results

Of 1582 citations screened, nine were included, giving 1685 participants, 581 with NE. All studies were observational and half had a low risk of bias. Four studies evaluated sleep by questionnaires only; two used questionnaires and polysomnography; two used only polysomnography, and one used sleep logs and actigraphy. Sleep questionnaires showed that children with enuresis had more sleep problems than controls, especially parasomnias, breathing disorders, and daytime sleepiness. Among the polysomnography parameters, the sleep stage architecture and periodic limb movements during sleep had conflicting data between the two studies.

Limitations

The studies evaluated sleep through heterogeneous tools. They used different questionnaires; even those considered by polysomnography did not record the same channels.

Conclusion

It seems that enuretic children and adolescents sleep differently from those who are non-enuretic. More studies are needed to clarify the best way to assess sleep and better understand this relationship. The review protocol was registered with PROSPERO, CRD42021266338. There was no funding.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

Data availability

Data from this study are available from the corresponding author.

Abbreviations

AASM:

American Academy of Sleep Medicine

AHI:

Apnea-Hypopnea Index

CAP:

Cyclic alternating pattern

CCTQ:

Children’s Chronotype Questionnaire

CSHQ:

Children’s Sleep Habits Questionnaire

DSM-5:

Manual of Mental Disorders, fifth edition

ECG:

Electrocardiography

EEG:

Electroencephalography

EMG:

Electromyography

EOG:

Electrooculography

ICCS:

International Children’s Continence Society

ICSD3:

International Classification of Sleep Disorders, third edition

NE:

Nocturnal enuresis

NREM:

Non-rapid eye movement

OSA:

Obstructive sleep apnea

OSA-18:

OSA quality of life survey

PICO:

Problem or Population, Interventions, Comparison and Outcome

PLMS:

Periodic limb movements during sleep

PRISMA:

Preferred Reporting Items for Systematic Reviews and Meta-Analyses

PROSPERO:

International Prospective Register of Systematic Reviews

PSQ:

Pediatric Sleep Questionnaire

ROBINS-E:

Risk of bias in non-randomized studies of exposures

ROBVIS:

Risk-of-bias visualization

SaO2:

Arterial oxygen saturation

SDSC:

Sleep Disturbances Scale for Children

SCR:

Sleep Clinical Records

References

  1. Austin PF, Bauer SB, Bower W, Chase J, Franco I, Hoebeke P, Rittig S, Walle JV, von Gontard A, Wright A, Yang SS, Nevéus T (2016) The standardization of terminology of lower urinary tract function in children and adolescents: update report from the standardization committee of the International Children’s Continence Society. Neurourol Urodyn 35:471–481. https://doi.org/10.1002/nau.22751

    Article  PubMed  Google Scholar 

  2. Nevéus T, Fonseca E, Franco I, Kawauchi A, Kovacevic L, Nieuwhof-Leppink A, Raes A, Tekgül S, Yang SS, Rittig S (2020) Management and treatment of nocturnal enuresis-an updated standardization document from the International Children’s Continence Society. J Pediatr Urol 16:10–19. https://doi.org/10.1016/j.jpurol.2019.12.020

    Article  PubMed  Google Scholar 

  3. Mota DM, Barros AJ, Matijasevich A, Santos IS (2015) Prevalence of enuresis and urinary symptoms at age 7 years in the 2004 birth cohort from Pelotas, Brazil. J Pediatr (Rio J) 9:52–58. https://doi.org/10.1016/j.jped.2014.04.011

    Article  Google Scholar 

  4. Yeung CK, Sreedhar B, Sihoe JD, Sit FK, Lau J (2006) Differences in characteristics of nocturnal enuresis between children and adolescents: a critical appraisal from a large epidemiological study. BJU Int 97:1069–1073. https://doi.org/10.1111/j.1464-410X.2006.06074.x

    Article  PubMed  Google Scholar 

  5. Iscan B, Ozkayın N (2020) Evaluation of health-related quality of life and affecting factors in child with enuresis. J Pediatr Urol 16:95.e1-195.e7. https://doi.org/10.1016/j.jpurol.2019.12.018

    Article  Google Scholar 

  6. American Psychiatric Association (2013) Diagnostic and Statistical Manual of Mental Disorders (DSM-5), 5th edn. American Psychiatric Association, Washington DC

    Book  Google Scholar 

  7. American Academy of Sleep Medicine (2014) International Classification of Sleep Disorders, 3rd edn. American Academy of Sleep Medicine, Darien, IL

    Google Scholar 

  8. von Gontard A, Schaumburg H, Hollmann E, Eiberg H, Rittig S (2001) The genetics of enuresis: a review. J Urol 166:2438–2443. https://doi.org/10.1097/00005392-200112000-00117

    Article  Google Scholar 

  9. Nevéus T (2017) Pathogenesis of enuresis: towards a new understanding. Int J Urol 24:174–182. https://doi.org/10.1111/iju.13310

    Article  PubMed  Google Scholar 

  10. Carskadon MA, Dement WC (2011) Monitoring and staging human sleep. In Kryger MT, Roth T, Dement WC (eds) Principles and practice of sleep medicine, 5th edition, St. Louis, Elsevier Saunders, pp16–26

  11. Mindell JA, Owens JA (2015) A clinical guide to pediatric sleep, diagnosis, and management of sleep problems. Wolters Kluwer, Philadelphia

    Google Scholar 

  12. Pedersen MJ, Rittig S, Jennum PJ, Kamperis K (2020) The role of sleep in the pathophysiology of nocturnal enuresis. Sleep Med Rev 49:101228. https://doi.org/10.1016/j.smrv.2019.101228

    Article  PubMed  Google Scholar 

  13. Bader G, Nevéus T, Kruse S, Sillén U (2002) Sleep of primary enuretic children and controls. Sleep 25:579–583

    Article  PubMed  Google Scholar 

  14. Nevéus T, Stenberg A, Läckgren G, Tuvemo T, Hetta J (1999) Sleep of children with enuresis: a polysomnographic study. Pediatrics 103:1193–1197. https://doi.org/10.1542/peds.103.6.1193

    Article  PubMed  Google Scholar 

  15. Esposito M, Gallai B, Parisi L, Roccella M, Marotta R, Lavano SM, Mazzotta G, Carotenuto M (2013) Primary nocturnal enuresis as a risk factor for sleep disorders: an observational questionnaire-based multicenter study. Neuropsychiatr Dis Treat 9:437–443. https://doi.org/10.2147/NDT.S43673

    Article  PubMed  PubMed Central  Google Scholar 

  16. Martenstyn JA, Machaalani R, Caldwell P, Waters KA (2021) Relationship between sleep respiration, architecture, and childhood enuresis: correlates between polysomnography and questionnaire. J Paediatr Child Health 57:1923–1928. https://doi.org/10.1111/jpc.15613

    Article  PubMed  Google Scholar 

  17. Jönson Ring I, Markström A, Bazargani F, Nevéus T (2017) Sleep disordered breathing in enuretic children and controls. J Pediatr Urol 13:620.e1-620.e6. https://doi.org/10.1016/j.jpurol.2017.05.012

    Article  PubMed  Google Scholar 

  18. Ma J, Li S, Jiang F, Jin X, Zhang Y, Yan C, Tian Y, Shen X, Li F (2018) Relationship between sleep patterns, sleep problems, and childhood enuresis. Sleep Med 50:14–20. https://doi.org/10.1016/j.sleep.2018.05.022

    Article  PubMed  Google Scholar 

  19. Su MS, Li AM, So HK, Au CT, Ho C, Wing YK (2011) Nocturnal enuresis in children: prevalence, correlates, and relationship with obstructive sleep apnea. J Pediatr 159:238-242.e1. https://doi.org/10.1016/j.jpeds.2011.01.036

    Article  PubMed  Google Scholar 

  20. Wada H, Kimura M, Tajima T, Shirahama R, Suzuki Y, Suzuki Y, Hayashi T, Maruyama K, Endo M, Sakamoto N, Ikeda A, Gozal D, Tanigawa T (2018) Nocturnal enuresis and sleep disordered breathing in primary school children: potential implications. Pediatr Pulmonol 53:1541–1548. https://doi.org/10.1002/ppul.24156

    Article  PubMed  Google Scholar 

  21. Cohen-Zrubavel V, Kushnir B, Kushnir J, Sadeh A (2011) Sleep and sleepiness in children with nocturnal enuresis. Sleep 34:191–194. https://doi.org/10.1093/sleep/34.2.191

    Article  PubMed  PubMed Central  Google Scholar 

  22. Dhondt K, Van Herzeele C, Roels SP, Raes A, Groen LA, Hoebeke P, Walle JV (2015) Sleep fragmentation and periodic limb movements in children with monosymptomatic nocturnal enuresis and polyuria. Pediatr Nephrol 30:1157–1162. https://doi.org/10.1007/s00467-015-3044-3

    Article  PubMed  Google Scholar 

  23. Soster LA, Alves RC, Fagundes SN, Lebl A, Garzon E, Koch VH, Ferri R, Bruni O (2017) Non-REM sleep instability in children with primary monosymptomatic sleep enuresis. J Clin Sleep Med 13:1163–1170. https://doi.org/10.5664/jcsm.6762

    Article  PubMed  PubMed Central  Google Scholar 

  24. Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD, Shamseer L, Tetzlaff JM, Akl EA, Brennan SE, Chou R, Glanville J, Grimshaw JM, Hróbjartsson A, Lalu MM, Li T, Loder EW, Mayo-Wilson E, McDonald S, McGuinness LA, Stewart LA, Thomas J, Tricco AC, Welch VA, Whiting P, Moher D (2021) The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ 29(372):n71. https://doi.org/10.1136/bmj.n71

    Article  Google Scholar 

  25. Prospero University of York (2015) Centre for Reviews and Dissemination. International Prospective Register of Systematic Reviews (PROSPERO). Available from: http://www.crd.york.ac.uk/PROSPERO. Accessed 01 June 2021

  26. Erdoğan F, Kadak MT, Selvi Y, Kartal V, Şenkal E, Ateş BÖ, Akgül HM (2016) The influence of the sleep-wake cycle on primary monosymptomatic nocturnal enuresis: A non-randomized comparative study. Biol Rhythm Res 47:437–445. https://doi.org/10.1080/09291016.2015.1130944

    Article  Google Scholar 

  27. Bascom A, Penney T, Metcalfe M, Knox A, Witmans M, Uweira T, Metcalfe PD (2011) High risk of sleep disordered breathing in the enuresis population. J Urol 186:1710–1713. https://doi.org/10.1016/j.juro.2011.04.017

    Article  PubMed  Google Scholar 

  28. Stone J, Malone PS, Atwill D, McGrigor V, Hill CM (2008) Symptoms of sleep-disordered breathing in children with nocturnal enuresis. J Pediatr Urol 4:197–202. https://doi.org/10.1016/j.jpurol.2007.11.011

    Article  PubMed  Google Scholar 

  29. Shafiek H, Evangelisti M, Abd-Elwahab NH, Barreto M, Villa MP, Mahmoud MI (2020) Obstructive sleep apnea in school-aged children presented with nocturnal enuresis. Lung 198:187–194. https://doi.org/10.1007/s00408-019-00304-6

    Article  CAS  PubMed  Google Scholar 

  30. ROBINS-E Development Group (Higgins J, Morgan R, Rooney A, Taylor K, Thayer K, Silva R, Lemeris C, Akl A, Arroyave W, Bateson T, Berkman N, Demers P, Forastiere F, Glenn B, Hróbjartsson A, Kirrane E, LaKind J, Luben T, Lunn R, McAleenan A, McGuinness L, Meerpohl J, Mehta S, Nachman R, Obbagy J, O’Connor A, Radke E, Savović J, Schubauer-Berigan M, Schwingl P, Schunemann H, Shea B, Steenland K, Stewart T, Straif K, Tilling K, Verbeek V, Vermeulen R, Viswanathan M, Zahm S, Sterne J) (2022) Risk of bias in non-randomized studies - of exposure (ROBINS-E). Available from: https://www.riskofbias.info/welcome/robins-e-tool. Accessed 10 August 2022

  31. McGuinness LA, Higgins JPT (2021) Risk-of-bias VISualization (robvis): an R package and Shiny web app for visualizing risk-of-bias assessments. Res Synth Methods 12:55–61. https://doi.org/10.1002/jrsm.1411

    Article  PubMed  Google Scholar 

  32. Negoro H, Kanematsu A, Yoshimura K, Ogawa O (2013) Chronobiology of micturition: putative role of the circadian clock. J Urol 190:843–849. https://doi.org/10.1016/j.juro.2013.02.024

    Article  PubMed  Google Scholar 

  33. Ancoli-Israel S, Cole R, Alessi C, Chambers M, Moorcroft W, Pollak CP (2003) The role of actigraphy in the study of sleep and circadian rhythms. Sleep 26:342–392. https://doi.org/10.1093/sleep/26.3.342

    Article  PubMed  Google Scholar 

  34. Ishman SL, Yang CJ, Cohen AP, Benke JR, Meinzen-Derr JK, Anderson RM, Madden ME, Tabangin ME (2015) Is the OSA-18 predictive of obstructive sleep apnea: comparison to polysomnography. Laryngoscope 125:1491–1495. https://doi.org/10.1002/lary.25098

    Article  PubMed  Google Scholar 

  35. Villa MP, Paolino MC, Castaldo R, Vanacore N, Rizzoli A, Miano S, Del Pozzo M, Montesano M (2013) Sleep clinical record: an aid to rapid and accurate diagnosis of paediatric sleep disordered breathing. Eur Respir J 41:1355–1361. https://doi.org/10.1183/09031936.00215411

    Article  PubMed  Google Scholar 

  36. Wolfish NM, Pivik RT, Busby KA (1997) Elevated sleep arousal thresholds in enuretic boys: clinical implications. Acta Paediatr 86:381–384. https://doi.org/10.1111/j.1651-2227

    Article  CAS  PubMed  Google Scholar 

  37. Manconi M, Ferri R, Zucconi M, Bassetti CL, Fulda S, Aricò D, Ferini-Strambi L (2012) Dissociation of periodic leg movements from arousals in restless legs syndrome. Ann Neurol 71:834–844. https://doi.org/10.1002/ana.23565

    Article  PubMed  Google Scholar 

  38. Franco I (2016) Overactive bladder in children. Nat Rev Urol 13:520–532. https://doi.org/10.1038/nrurol.2016.152

    Article  CAS  PubMed  Google Scholar 

  39. Picchietti MA, Picchietti DL, England SJ, Walters AS, Couvadelli BV, Lewin DS, Hening W (2009) Children show individual night-to-night variability of periodic limb movements in sleep. Sleep 32:530–535. https://doi.org/10.1093/sleep/32.4.530

    Article  PubMed  PubMed Central  Google Scholar 

  40. Witthaus MW, Nipa F, Yang JH, Li Y, Lerner LB, Azadzoi KM (2015) Bladder oxidative stress in sleep apnea contributes to detrusor instability and nocturia. J Urol 193:1692–1699. https://doi.org/10.1016/j.juro.2014.11.055

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Pediatric Nephrology Unit, Faculty of Medicine - Pediatrics Department, Universidade Federal de Minas Gerais, Avenida Alfredo Balena 190. Sala 267, Santa Efigênia, Belo Horizonte, Minas Gerais, 30130-100, Brazil

    Ana Elisa Ribeiro Fernandes, José Reinaldo Corrêa Roveda, Carolina Rodrigues Fernandes, Diego Ferreira Silva, Isabela Cristina de Oliveira Guimarães, Eleonora Moreira Lima, Flávia Cristina de Carvalho Mrad & Mônica Maria de Almeida Vasconcelos

Authors
  1. Ana Elisa Ribeiro Fernandes
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. José Reinaldo Corrêa Roveda
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Carolina Rodrigues Fernandes
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Diego Ferreira Silva
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Isabela Cristina de Oliveira Guimarães
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Eleonora Moreira Lima
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Flávia Cristina de Carvalho Mrad
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Mônica Maria de Almeida Vasconcelos
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

The search in the database was carried out independently by MMAV and FCCM. After removing the duplicates, the remaining titles/abstracts were independently selected by two authors (MMAV and AERF). The full text of the studies using predefined eligibility criteria was examined by three independent reviewers (MMAV, AERF, and FCCM), and eligibility and discrepancies were resolved through discussion. JRR, CRF, and DFS were responsible for extracting data from articles selected for inclusion. All authors reviewed and agreed on the final version.

Ethics declarations

Ethical approval

Not applicable.

Conflict of interest

The authors declare no competing interests.

Institution where the research was carried out

Universidade Federal de Minas Gerais.

Additional information

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Fernandes, A.E.R., Roveda, J.R.C., Fernandes, C.R. et al. Relationship between nocturnal enuresis and sleep in children and adolescents. Pediatr Nephrol 38, 1427–1438 (2023). https://doi.org/10.1007/s00467-022-05818-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00467-022-05818-5

Keywords

Search

Navigation