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Sleep-related breathing disorders in facioscapulohumeral dystrophy

  • Neurology • Original Article
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Abstract

Purpose

Severe manifestations of facioscapulohumeral dystrophy (FSHD) may be associated with sleep-disordered breathing (SDB), including obstructive sleep apnea (OSA) and nocturnal hypoventilation (NH), but prevalence data are scarce. In patients with respiratory muscle weakness, detection of NH can be facilitated by transcutaneous capnometry, but respective data derived from FSHD patients have not yet been published.

Methods

We collected sleep studies and capnometry recordings from 31 adult patients with genetically confirmed FSHD who were admitted to our sleep laboratory for first-ever evaluation of sleep-related breathing. Indications for admission included non-restorative sleep, morning headache, or excessive daytime sleepiness. In addition, sleep studies were initiated if symptoms or signs of respiratory muscle weakness were present. Thirty-one subjects with insomnia served as controls for comparison of respiratory measures during sleep.

Results

In the FSHD group, 17/31 (55%) patients showed OSA and 8 (26%) had NH. NH would have been missed in 7/8 patients if only oximetry criteria of hypoventilation had been applied. Capnography results were correlated with disease severity as reflected by the Clinical Severity Score (CSS). Non-invasive ventilation (NIV) was started in 6 patients with NH and 3 individuals with OSA. Nocturnal continuous positive airway pressure was administered to 2 patients, and positional therapy was sufficient in 4 individuals. In patients initiated on NIV, nocturnal gas exchange already improved in the first night of treatment.

Conclusions

SDB is common in adult patients with FSHD complaining of sleep-related symptoms. It may comprise OSA, NH, and most often, the combination of both. Sleep-related hypercapnia is associated with disease severity. Transcutaneous capnometry is superior to pulse oximetry for detection of NH.

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Abbreviations

AHI:

Apnea-Hypopnea Index

BMI:

Body mass index

CO2 :

Carbon dioxide

CPAP:

Continuous positive airway pressure

CSS:

Clinical Severity Scale

EDS:

Excessive daytime sleepiness

ESS:

Epworth Sleepiness Scale

FSHD:

Facioscapulohumeral dystrophy

FSS:

Fatigue Severity Scale

NH:

Nocturnal hypoventilation

NIV:

Non-invasive ventilation

NS:

Not significant

ODI:

Oxygen desaturation index

OSA:

Obstructive sleep apnea

PAP:

Positive airway pressure

pCO2 :

Carbon dioxide pressure

PSG:

Polysomnography

PSQI:

Pittsburg Sleep Quality Index

ptcCO2 :

Transcutaneous carbon dioxide tension

REM:

Rapid eye movement

SD:

Standard deviation

SDB:

Sleep-disordered breathing

SpO2 :

Oxygen saturation

TC:

Transcutaneous capnometry

References

  1. Lemmers RJLF, Miller DG, van der Maarel SM. Facioscapulohumeral muscular dystrophy. 1999 Mar 8 [Updated 2014 Mar 20]. In: Adam MP, Ardinger HH, Pagon RA, et al., editors. GeneReviews® [Internet]. Seattle (WA): University of Washington, Seattle; 1993-2018. Available from: https://www.ncbi.nlm.nih.gov/books/NBK1443/

  2. Statland J, Tawil R (2014) Facioscapulohumeral muscular dystrophy. Neurol Clin 32:721–728. https://doi.org/10.1016/j.ncl.2014.04.003

    Article  PubMed  PubMed Central  Google Scholar 

  3. Jordan B, Eger K, Koesling S, Zierz S (2011) Camptocormia phenotype of FSHD: a clinical and MRI study on six patients. J Neurol 258:866–873. https://doi.org/10.1007/s00415-010-5858-z

    Article  PubMed  Google Scholar 

  4. Theadom A, Rodrigues M, Roxburgh R, Balalla S, Higgins C, Bhattacharjee R, Jones K, Krishnamurthi R, Feigin V (2014) Prevalence of muscular dystrophies: a systematic literature review. Neuroepidemiology 43:259–268. https://doi.org/10.1159/000369343

    Article  PubMed  Google Scholar 

  5. Fisher J, Upadhyaya M (1997) Molecular genetics of facioscapulohumeral muscular dystrophy (FSHD). Neuromuscul Disord 7:655–662. https://doi.org/10.1016/S0960-8966(96)00400-2

    Article  Google Scholar 

  6. Ricci E, Galluzzi G, Deidda G, Cacurri S, Colantoni L, Merico B, Piazzo N, Servidei S, Vigneti E, Pasceri V, Silvestri G, Mirabella M, Mangiola F, Tonali P, Felicetti L (1999) Progress in the molecular diagnosis of facioscapulohumeral muscular dystrophy and correlation between the number of KpnI repeats at the 4q35 locus and clinical phenotype. Ann Neurol 45:751–757. https://doi.org/10.1002/1531-8249(199906)45:6<751::AID-ANA9>3.0.CO;2-M

    Article  CAS  PubMed  Google Scholar 

  7. Larsen M, Rost S, El Hajj N, Ferbert A, Deschauer M, Walter MC et al (2015) Diagnostic approach for FSHD revisited: SMCHD1 mutations cause FSHD2 and act as modifiers of disease severity in FSHD1. Eur J Hum Genet 23:808–816. https://doi.org/10.1038/ejhg.2014.191

    Article  CAS  PubMed  Google Scholar 

  8. LoMauro A, D’Angelo MG, Aliverti A (2017) Sleep disordered breathing in Duchenne muscular dystrophy. Curr Neurol Neurosci Rep 17:44. https://doi.org/10.1007/s11910-017-0750-1

    Article  PubMed  Google Scholar 

  9. Smith PEM, Edwards RHT, Calverley PMA (1989) Ventilation and breathing pattern during sleep in Duchenne muscular dystrophy. Chest 96:1346–1351. https://doi.org/10.1378/chest.96.6.1346

    Article  CAS  PubMed  Google Scholar 

  10. Bianchi MLL, Losurdo A, Di Blasi C, Santoro M, Masciullo M, Conte G et al (2014) Prevalence and clinical correlates of sleep disordered breathing in myotonic dystrophy types 1 and 2. Sleep Breath 18:579–589. https://doi.org/10.1007/s11325-013-0921-5

    Article  PubMed  Google Scholar 

  11. Poppe M, Cree L, Bourke J, Eagle M, Anderson LVB, Birchall D, Brockington M, Buddles M, Busby M, Muntoni F, Wills A, Bushby K (2003) The phenotype of limb-girdle muscular dystrophy type 2I. Neurology 60:1246–1251. https://doi.org/10.1212/01.WNL.0000058902.88181.3D

    Article  CAS  PubMed  Google Scholar 

  12. Fayssoil A, Ogna A, Chaffaut C, Chevret S, Guimarães-Costa R, Leturcq F, Wahbi K, Prigent H, Lofaso F, Nardi O, Clair B, Behin A, Stojkovic T, Laforet P, Orlikowski D, Annane D (2016) Natural history of cardiac and respiratory involvement, prognosis and predictive factors for long-term survival in adult patients with limb girdle muscular dystrophies type 2C and 2D. PLoS One 11:e0153095. https://doi.org/10.1371/journal.pone.0153095

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Boentert M, Wenninger S, Sansone VAA (2017) Respiratory involvement in neuromuscular disorders. Curr Opin Neurol 30:529–537. https://doi.org/10.1097/WCO.0000000000000470

    Article  CAS  PubMed  Google Scholar 

  14. Wohlgemuth M, Van Der Kooi EL, Van Kesteren RG, Van Der Maarel SM, Padberg GW (2004) Ventilatory support in facioscapulohumeral muscular dystrophy. Neurology 63:176–178. https://doi.org/10.1212/01.WNL.0000133126.86377.E8

    Article  CAS  PubMed  Google Scholar 

  15. Moreira S, Wood L, Smith D, Marini-Bettolo C, Guglieri M, McMacken G, Bailey G, Mayhew A, Muni-Lofra R, Eglon G, Williams M, Straub V, Lochmüller H, Evangelista T (2017) Respiratory involvement in ambulant and non-ambulant patients with facioscapulohumeral muscular dystrophy. J Neurol 264:1271–1280. https://doi.org/10.1007/s00415-017-8525-9

    Article  PubMed  PubMed Central  Google Scholar 

  16. Della Marca G, Frusciante R, Dittoni S, Vollono C, Buccarella C, Iannaccone E, Rossi M, Scarano E, Pirronti T, Cianfoni A, Mazza S, Tonali PA, Ricci E (2009) Sleep disordered breathing in facioscapulohumeral muscular dystrophy. J Neurol Sci 285:54–58. https://doi.org/10.1016/j.jns.2009.05.014

    Article  PubMed  Google Scholar 

  17. Boentert M, Glatz C, Helmle C, Okegwo A, Young P (2018) Prevalence of sleep apnoea and capnographic detection of nocturnal hypoventilation in amyotrophic lateral sclerosis. J Neurol Neurosurg Psychiatry 89:418–424. https://doi.org/10.1136/jnnp-2017-316515

    Article  PubMed  Google Scholar 

  18. Georges M, Nguyen-Baranoff D, Griffon L, Foignot C, Bonniaud P, Camus P, Pepin JL, Rabec C (2016) Usefulness of transcutaneous PCO2 to assess nocturnal hypoventilation in restrictive lung disorders. Respirology 21:1300–1306. https://doi.org/10.1111/resp.12812

    Article  PubMed  Google Scholar 

  19. Ogna A, Quera Salva MA, Prigent H, Mroue G, Vaugier I, Annane D, Lofaso F, Orlikowski D (2016) Nocturnal hypoventilation in neuromuscular disease: prevalence according to different definitions issued from the literature. Sleep Breath 20:575–581. https://doi.org/10.1007/s11325-015-1247-2

    Article  PubMed  Google Scholar 

  20. The AASM Manual for the scoring of sleep and associated events n.d.

  21. Berry RB, Budhiraja R, Gottlieb DJ, Gozal D, Iber C, Kapur VK, Marcus CL, Mehra R, Parthasarathy S, Quan SF, Redline S, Strohl KP, Davidson Ward SL, Tangredi MM, American Academy of Sleep Medicine (2012) Rules for scoring respiratory events in sleep: update of the 2007 AASM manual for the scoring of sleep and associated events. J Clin Sleep Med 8:597–619. https://doi.org/10.5664/jcsm.2172

    Article  PubMed  PubMed Central  Google Scholar 

  22. Storre JH, Magnet FS, Dreher M, Windisch W (2011) Transcutaneous monitoring as a replacement for arterial PCO(2) monitoring during nocturnal non-invasive ventilation. Respir Med 105:143–150. https://doi.org/10.1016/j.rmed.2010.10.007

    Article  PubMed  Google Scholar 

  23. Windisch W, Dreher M, Geiseler J, Siemon K, Brambring J, Dellweg D, Grolle B, Hirschfeld S, Köhnlein T, Mellies U, Rosseau S, Schönhofer B, Schucher B, Schütz A, Sitter H, Stieglitz S, Storre J, Winterholler M, Young P, Walterspacher S, für die Leitliniengruppe “Nichtinvasive und invasive Beatmung als Therapie der chronischen respiratorischen Insuffizienz” (2017) Guidelines for non-invasive and invasive home mechanical ventilation for treatment of chronic respiratory failure - update 2017. Pneumologie 71:722–795. https://doi.org/10.1055/s-0043-118040

    Article  CAS  PubMed  Google Scholar 

  24. Clinical indications for noninvasive positive pressure ventilation in chronic respiratory failure due to restrictive lung disease, COPD, and nocturnal hypoventilation–a consensus conference report. Chest 1999;116:521–34. https://doi.org/10.1378/chest.116.2.521.

  25. Nardi J, Prigent H, Adala A, Bohic M, Lebargy F, Quera-Salva MA, Orlikowski D, Lofaso F (2012) Nocturnal oximetry and transcutaneous carbon dioxide in home-ventilated neuromuscular patients. Respir Care 57:1425–1430. https://doi.org/10.4187/respcare.01658

    Article  PubMed  Google Scholar 

  26. Janssens JP, Borel JC, Pepin JL, groupe Somno VNI (2014) Nocturnal monitoring of home non-invasive ventilation: contribution of simple tools such as pulse-oximetry, capnography, built-in ventilator software and autonomic markers of sleep fragmentation. Rev Mal Respir 31:107–118. https://doi.org/10.1016/j.rmr.2013.08.003

    Article  PubMed  Google Scholar 

  27. Johns MW (1991) A new method for measuring daytime sleepiness: the Epworth sleepiness scale. Sleep 14:540–545. https://doi.org/10.1093/sleep/14.6.540

    Article  CAS  PubMed  Google Scholar 

  28. Buysse DJ, Reynolds CF 3rd, Monk TH, Berman SR, Kupfer DJ (1989) The Pittsburgh Sleep Quality Index: a new instrument for psychiatric practice and research. Psychiatry Res 28:193–213. https://doi.org/10.1016/0165-1781(89)90047-4

    Article  CAS  PubMed  Google Scholar 

  29. Krupp LB, LaRocca NG, Muir-Nash J, Steinberg AD (1989) The fatigue severity scale: application to patients with multiple sclerosis and systemic lupus erythematosus. Arch Neurol 46:1121–1123. https://doi.org/10.1001/archneur.1989.00520460115022

    Article  CAS  PubMed  Google Scholar 

  30. Windisch W, Walterspacher S, Siemon K, Geiseler J, Sitter H (2010) Guidelines for non-invasive and invasive mechanical ventilation for treatment of chronic respiratory failure. Published by the German Society for Pneumology (DGP). Pneumologie 64:640–652. https://doi.org/10.1055/s-0030-1255558

    Article  CAS  PubMed  Google Scholar 

  31. Boentert M, Brenscheidt I, Glatz C, Young P (2015) Effects of non-invasive ventilation on objective sleep and nocturnal respiration in patients with amyotrophic lateral sclerosis. J Neurol 262:2073–2082. https://doi.org/10.1007/s00415-015-7822-4

    Article  CAS  PubMed  Google Scholar 

  32. Annane D, Orlikowski D, Chevret S (2014) Nocturnal mechanical ventilation for chronic hypoventilation in patients with neuromuscular and chest wall disorders. Cochrane Database Syst Rev 12:CD001941. https://doi.org/10.1002/14651858.CD001941.pub3

    Article  Google Scholar 

  33. Boentert M, Dräger B, Glatz C, Young P (2016) Sleep-disordered breathing and effects of noninvasive ventilation in patients with late-onset Pompe disease. J Clin Sleep Med 12:1623–1632. https://doi.org/10.5664/jcsm.6346

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

English language editing assistance was provided by Nicola Ryan, independent medical writer.

Author information

Author notes

  1. Maya Runte and Jens Spiesshoefer contributed equally to this work.

Authors and Affiliations

  1. Department of Neurology, University Hospital Muenster, Albert-Schweitzer-Campus 1, Building A1, 48149, Muenster, Germany

    Maya Runte, Jens Spiesshoefer, Anna Heidbreder & Matthias Boentert

  2. Department of Pneumology and Intensive Care Medicine, University Hospital RWTH Aachen, Aachen, Germany

    Michael Dreher

  3. Medical Park Klinik Reithofpark, Neurology, Bad Feilnbach, Germany

    Peter Young

  4. Institute of Medical Informatics, University of Muenster, Muenster, Germany

    Tobias Brix

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  1. Maya Runte
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Correspondence to Matthias Boentert.

Ethics declarations

This retrospective study was conducted in accordance with the regulations set by the local ethics committee (Ethikkommission der Ärztekammer Westfalen-Lippe und der Medizinischen Fakultät der Westfälischen Wilhelms-Universität Münster).

Conflict of interest

JS is supported by the Else-Kröner-Fresenius Stiftung (Grant A109) and by Kommission für Innovative Medizinische Forschung an der Medizinischen Fakultät Muenster (IMF Grant SP 11 18 15) outside this work. PY and MB have received speaker honoraria and financial research support from Löwenstein Mecdical GmbH (Bad Ems, Germany) or the Löwenstein Foundation (Bad Ems, Germany), respectively. MD received fees for speaking and advising from ResMed, Philips, and Linde. MD received unrestricted research grants from ResMed. All other authors declare that they have no conflicts of interest.

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Runte, M., Spiesshoefer, J., Heidbreder, A. et al. Sleep-related breathing disorders in facioscapulohumeral dystrophy. Sleep Breath 23, 899–906 (2019). https://doi.org/10.1007/s11325-019-01843-1

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