Screening Patients with Type 2 Diabetes at High Risk of Obstructive Sleep Apnea: A Single Tertiary Center Experience

Abstract

Objective: Current guidelines suggest screening patients with type 2 diabetes (T2D) for obstructive sleep apnea (OSA). However, there is no consensus regarding the optimal method for OSA risk assessment. We aimed to identify those with diabetes who are at high risk for OSA and investigate the concordance among questionnaires utilized in assessing high OSA risk. Method: STOP, STOP-BANG, and Berlin questionnaires for the assessment of the risk of OSA and the Epworth Sleepiness Scale (ESS) for an investigation of daytime sleepiness were utilized. Results: We included 108 patients, with a median HbA1c of 7.5%, a BMI of 30.7 kg/m², and waist and neck circumferences measuring 104.3 cm and 38.9 cm, respectively. On ESS, 10.2% of patients had excessive daytime sleepiness. According to Berlin (38.9%), the number of patients at high risk of OSA was found to be lower than that of in STOP (53.7%) and STOP-BANG (68.5%) questionnaires. For patients with a BMI<30 kg/m², insufficient consistency was observed between Berlin with STOP and STOP-BANG (p<0.05), whereas there was a concordance between STOP and STOP-BANG (p=0.453). In those with BMI>30 kg/m², while Berlin and STOP were consistent (p=0.824), no concordance was detected between Berlin and STOP-BANG, as well as between STOP and STOP-BANG (p<0.05). The insulin therapy was the associated factor with a high OSA risk in multivariate logistic regression analysis (p=0.041). Conclusion: The questionnaires used to predict the risk of OSA in T2D exhibit insufficient compatibility. Insulin therapy contributes to the increased risk of OSA in individuals diagnosed with T2D.

Keywords

• Berlin Questionnaire
• Epworth Sleepiness Scale
• STOP-BANG
• Obesity
• Type 2 diabetes

Ethical Statement

The study was approved by Gazi University Ethical Board (decision number: 481, date: 05 June 2023).

Obstrüktif Uyku Apne Sendromu İçin Yüksek Riskli Olan Tip 2 Diyabet Hastalarının Belirlenmesi

Abstract

Amaç: Mevcut kılavuzlar, tip 2 diyabet (T2D) hastalarının obstrüktif uyku apnesi (OSA) açısından taranmasını önermektedir. Ancak, OSA risk değerlendirmesi için en uygun yöntem konusunda bir fikir birliği yoktur. Diyabeti olan ve OSA riski yüksek olan kişileri belirlemeyi ve yüksek OSA riski değerlendirmesinde kullanılan anketler arasındaki uyumu araştırmayı amaçladık. Yöntem: OSA riski değerlendirmesi için STOP, STOP-BANG ve Berlin anketleri ve gündüz uykululuğunu araştırmak için Epworth Uykululuk Ölçeği (ESS) kullanıldı. Sonuçlar: Çalışmaya dahil edilen 108 hastanın ortanca HbA1c değeri %7.5, vücut kitle indeksi (VKİ) değeri 30.7 kg/m² ve bel ve boyun çevreleri sırasıyla 104.3 cm ve 38.9 cm olarak bulundu. ESS’ye göre hastaların %10.2’sinde aşırı gündüz uykululuğu vardı. Berlin anketine göre (%38.9), yüksek OSA riski taşıyan hasta sayısı, STOP (%53.7) ve STOP-BANG (%68.5) anketlerine göre daha düşük bulundu. VKİ<30 kg/m² olan hastalarda, Berlin ile STOP ve STOP-BANG arasında yetersiz tutarlılık gözlenirken (p<0.05), STOP ile STOP-BANG arasında yeterli uyum vardı (p=0.453). VKİ>30 kg/m² olan hastalarda ise Berlin ile STOP arasında tutarlılık gözlenirken (p=0.824), Berlin ile STOP-BANG ve STOP ile STOP-BANG arasında uyum tespit edilmedi (p<0.05). Çok değişkenli lojistik regresyon analizinde, insülin tedavisinin yüksek OSA riski ile ilişkili faktör olduğu bulundu (p=0.041). Sonuç: T2D'de OSA riskini tahmin etmek için kullanılan anketler yetersiz uyum sergilemektedir. İnsülin tedavisi, T2D tanısı alan bireylerde artmış OSA riski ile ilişkilidir.

Keywords

• Berlin anketi
• Epworth uykululuk ölçeği
• STOP-BANG
• Obezite
• Tip 2 diyabet

References

1. 1. Heinzer R, Vat S, Marques-Vidal P, Marti-Soler H, Andries D, Tobback N, et al. Prevalence of sleep-disordered breathing in the general population: the HypnoLaus study. The Lancet Respiratory Medicine. 2015;3(4):310-8.
2. 2. Reutrakul S, Mokhlesi B. Obstructive Sleep Apnea and Diabetes: A State of the Art Review. Chest. 2017;152(5):1070-86. doi: 10.1016/j.chest.2017.05.009.
3. 3. Peppard PE, Young T, Barnet JH, Palta M, Hagen EW, Hla KM. Increased prevalence of sleep-disordered breathing in adults. Am J Epidemiol. 2013;177(9):1006-14.
4. 4. Li M, Li X, Lu Y. Obstructive Sleep Apnea Syndrome and Metabolic Diseases. Endocrinology. 2018;159(7):2670-5. doi: 10.1210/en.2018-00248.
5. 5. Sun H, Saeedi P, Karuranga S, Pinkepank M, Ogurtsova K, Duncan BB, et al. IDF Diabetes Atlas: Global, regional and country-level diabetes prevalence estimates for 2021 and projections for 2045. Diabetes research and clinical practice. 2022;183:109119.
6. 6. Zhang SX, Khalyfa A, Wang Y, Carreras A, Hakim F, Neel BA, et al. Sleep fragmentation promotes NADPH oxidase 2-mediated adipose tissue inflammation leading to insulin resistance in mice. International journal of obesity. 2014;38(4):619-24.
7. 7. Xu J, Long Y-S, Gozal D, Epstein PN. β-cell death and proliferation after intermittent hypoxia: Role of oxidative stress. Free Radical Biology and Medicine. 2009;46(6):783-90.
8. 8. Muraki I, Wada H, Tanigawa T. Sleep apnea and type 2 diabetes. J Diabetes Investig. 2018;9(5):991-7. doi: 10.1111/ jdi.12823.

9. 9. 5. Facilitating Positive Health Behaviors and Well-being to Improve Health Outcomes: Standards of Care in Diabetes—2024. Diabetes Care. 2024;47(Supplement_1):S77-S110.
10. 10. Ogilvie RP, Patel SR. The Epidemiology of Sleep and Diabetes. Curr Diab Rep. 2018;18(10):82. doi: 10.1007/s11892-018- 1055-8.
11. 11. 4. Comprehensive Medical Evaluation and Assessment of Comorbidities: Standards of Care in Diabetes-2024. Diabetes Care. 2024;47(Suppl 1):S52-s76. doi: 10.2337/dc24-S004.
12. 12. Lee JJ, Sundar KM. Evaluation and Management of Adults with Obstructive Sleep Apnea Syndrome. Lung. 2021;199(2):87- 101. doi: 10.1007/s00408-021-00426-w.
13. 13. 2. Diagnosis and Classification of Diabetes: Standards of Care in Diabetes-2024. Diabetes Care. 2024;47(Suppl 1):S20-s42. doi: 10.2337/dc24-S002.
14. 14. Sönmez A, Özdoğan Ö, Arici M, Salman S, DERİCİ Ü, DEĞER SM, et al. Consensus Statement of Endocrinology, Cardiology, and Nephrology (ENCARNE) Experts on Prevention, Diagnosis, and Management of Cardiovascular and Renal Complications of Diabetes. Turkish Journal of Endocrinology & Metabolism. 2021;25(4).
15. 15. Faselis C, Katsimardou A, Imprialos K, Deligkaris P, Kallistratos M, Dimitriadis K. Microvascular Complications of Type 2 Diabetes Mellitus. Curr Vasc Pharmacol. 2020;18(2):117-24. doi: 10.2174/1570161117666190502103733.
16. 16. Viigimaa M, Sachinidis A, Toumpourleka M, Koutsampasopoulos K, Alliksoo S, Titma T. Macrovascular Complications of Type 2 Diabetes Mellitus. Curr Vasc Pharmacol. 2020;18(2):110-6. doi: 10.2174/1570161117666190405165151.
17. 17. Bayram F, Bayraktaroğlu T, Sargin M, Şahin İ, Güldiken S, Dalbeler A, et al. A Cross-Sectional Study of the Prevalence of Cardiovascular Disease in Adults with Type 2 Diabetes in Turkiye: The CAPTURE Study. Turkish Journal of Endocrinology and Metabolism. 2022;26(1).
18. 18. Acar HV, Kaya A, Yücel F, Erdem M, Günal SE, Özgen F, et al. Validation of the STOP-Bang questionnaire: An obstructive sleep apnoea screening tool in Turkish population. Turkish Journal of Anaesthesiology & Reanimation. 2013;41(4):115.
19. 19. Yüceege M, Fırat H, Sever Ö, Demir A, Ardıç S. The effect of adding gender item to Berlin Questionnaire in determining obstructive sleep apnea in sleep clinics. Annals of thoracic medicine. 2015;10(1):25-8.
20. 20. Chung F, Yegneswaran B, Liao P, Chung SA, Vairavanathan S, Islam S, et al. STOP questionnaire: a tool to screen patients for obstructive sleep apnea. Anesthesiology. 2008;108(5):812-21. doi: 10.1097/ALN.0b013e31816d83e4.
21. 21. Chung F, Abdullah HR, Liao P. STOP-Bang Questionnaire: A Practical Approach to Screen for Obstructive Sleep Apnea. Chest. 2016;149(3):631-8. doi: 10.1378/chest.15-0903.
22. 22. Netzer NC, Stoohs RA, Netzer CM, Clark K, Strohl KP. Using the Berlin Questionnaire to identify patients at risk for the sleep apnea syndrome. Annals of internal medicine. 1999;131(7):485-91.
23. 23. Izci B, Ardic S, Firat H, Sahin A, Altinors M, Karacan I. Reliability and validity studies of the Turkish version of the Epworth Sleepiness Scale. Sleep and Breathing. 2008;12:161-8.
24. 24. Johns MW. A new method for measuring daytime sleepiness: the Epworth sleepiness scale. sleep. 1991;14(6):540-5.
25. 25. Chiu H-Y, Chen P-Y, Chuang L-P, Chen N-H, Tu Y-K, Hsieh Y-J, et al. Diagnostic accuracy of the Berlin questionnaire, STOP-BANG, STOP, and Epworth sleepiness scale in detecting obstructive sleep apnea: a bivariate meta-analysis. Sleep medicine reviews. 2017;36:57-70.
26. 26. Jinmei L, Rong H, Xu Z, Yi X, Jiong Z. STOP-Bang questionnaire is superior to Epworth sleepiness scales, Berlin questionnaire, and STOP questionnaire in screening obstructive sleep apnea hypopnea syndrome patients. Chinese medical journal. 2014;127(17):3065-70.
27. 27. Suliman LA, Shalabi NM, Elmorsy AS, Moawed MK. Value of STOP-BANG and Berlin questionnaires in the diagnosis and severity prediction of obstructive sleep apnea hypopnea syndrome. Egyptian Journal of Bronchology. 2017;11:367-71.
28. 28. Westlake K, Plihalova A, Pretl M, Lattova Z, Polak J. Screening for obstructive sleep apnea syndrome in patients with type 2 diabetes mellitus: a prospective study on sensitivity of Berlin and STOP-Bang questionnaires. Sleep Med. 2016;26:71-6. doi: 10.1016/j.sleep.2016.07.009.
29. 29. Westlake K, Polak J. Screening for obstructive sleep apnea in type 2 diabetes patients–questionnaires are not good enough. Frontiers in endocrinology. 2016;7:124.
30. 30. Wondie A, Taderegew MM, Girma B, Getawey A, Tsega D, Terefe TF, et al. Obstructive sleep apnea risk and its associated factors among type 2 diabetes mellitus patients at wolkite university specialized hospital, Wolkite, Southern Ethiopia, 2021. A comparative cross-sectional study. Diabetol Metab Syndr. 2022;14(1):157. doi: 10.1186/s13098-022-00931-9.
31. 31. Sokwalla SMR, Joshi MD, Amayo EO, Acharya K, Mecha JO, Mutai KK. Quality of sleep and risk for obstructive sleep apnoea in ambulant individuals with type 2 diabetes mellitus at a tertiary referral hospital in Kenya: a cross-sectional, comparative study. BMC endocrine disorders. 2017;17:1-8.
32. 32. Shnaimer JA, Dahlan HM, Hanbashi FM, Bahammam AS, Gosadi IM. Assessment of the risk of obstructive sleep apnoea among patients with type 2 diabetes and its associated factors using the STOP-BANG questionnaire: A cross-sectional study. J Taibah Univ Med Sci. 2022;17(4):606-13. doi: 10.1016/j. jtumed.2021.11.013.
33. 33. Butt AM, Syed U, Arshad A. Predictive Value of Clinical and Questionnaire Based Screening Tools of Obstructive Sleep Apnea in Patients With Type 2 Diabetes Mellitus. Cureus. 2021;13(9):e18009. doi: 10.7759/cureus.18009.
34. 34. Saad AM, Hiyasat D, Jaddou H, Obeidat N. The prevalence of high risk obstructive sleep apnoea among patients with type 2 diabetes in Jordan. Diabetes Research and Clinical Practice. 2019;152:16-22.
35. 35. Algeffari M, Alkhamis A, Almesned A, Alghammas N, Albulayhi S, AlGoblan A. Obstructive sleep apnea among people with type 2 diabetes in Saudi Arabia: a cross-sectional study. Majmaah Journal of Health Sciences. 2020;6(2):32-.
36. 36. Javaheri S, Barbe F, Campos-Rodriguez F, Dempsey JA, Khayat R, Javaheri S, et al. Sleep apnea: types, mechanisms, and clinical cardiovascular consequences. Journal of the American College of Cardiology. 2017;69(7):841-58.
37. 37. Paschou SA, Bletsa E, Saltiki K, Kazakou P, Kantreva K, Katsaounou P, et al. Sleep Apnea and Cardiovascular Risk in Patients with Prediabetes and Type 2 Diabetes. Nutrients. 2022;14(23). doi: 10.3390/nu14234989.
38. 38. Huang T, Lin BM, Stampfer MJ, Tworoger SS, Hu FB, Redline S. A Population-Based Study of the Bidirectional Association Between Obstructive Sleep Apnea and Type 2 Diabetes in Three Prospective U.S. Cohorts. Diabetes Care. 2018;41(10):2111-9. doi: 10.2337/dc18-0675.