Güzide ATALIK, Yusuf Kemal KEMALOĞLU, Metin YILMAZ, Hakan GÖLAÇ

Reflux, dysphonia, and dysphagia symptoms in patients with diabetes and their association with diabetic complications

Background/aim: Diabetes mellitus (DM) could influence various organs, especially the eyes, kidneys, nerves, heart, and blood vessels, and finally results in many irreversible disease-related complications. In this paper, the association between reflux, swallowing, and voice symptoms in patients with DM and the possible effect of diabetic complications on these symptoms were investigated. Materials and methods: A total of 179 patients with diabetes were included to the study. Three self-reported questionnaires; Reflux Symptom Index (RSI), Eating Assessment Tool-10 (EAT-10), and Voice Handicap Index-10 (VHI-10) were administrated to the patients and, their association with DM-related neuropathy and nephropathy were examined. Results: The scores of each questionnaire were significantly correlated with each other (p < 0.001). There was not any statistically significant association between the score of T-RSI and the diabetic complications (p = 0.077), while a statistically significant association was found between the T-EAT-10 score and neuropathy (p < 0.001). Neither neuropathy nor nephropathy alone had an association with the T-VHI-10 score. However, the presence of nephropathy and neuropathy together was found to be associated with the T-VHI-10 score (p = 0.027). Conclusion: It is possible to conclude that gastrointestinal symptoms such as reflux, dysphonia, and dysphagia are associated with each other and they may possibly be related to the microvascular complications of DM. The clinicians should be aware of the possible reflux, voice, and swallowing complaints and also inquire about the presence of neuropathy and nephropathy in the diabetic population.

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1. Saeedi P, Petersohn I, Salpea P, Malanda B, Karuranga S et al. Global and regional diabetes prevalence estimates for 2019 and projections for 2030 and 2045: Results from the International Diabetes Federation Diabetes Atlas. Diabetes Research and Clinical Practice 2019; 157: 107843. doi: 10.1016/j. diabres.2019.107843
2. Huang ES, Laiteerapong N, Liu JY, John PM, Moffet HH et al. Rates of complications and mortality in older patients with diabetes mellitus: the diabetes and aging study. JAMA Internal Medicine 2014; 174(2): 251-258. doi: 10.1001/ jamainternmed.2013.12956
3. Zheng Y, Ley SH, Hu FB. Global aetiology and epidemiology of type 2 diabetes mellitus and its complications. Nature Reviews Endocrinology 2018; 14(2): 88. doi: 10.1038/nrendo.2017.151
4. Papatheodorou K, Banach M, Bekiari E, Rizzo M, Edmonds M. Complications of diabetes 2017. Journal of Diabetes Research 2018; 3086167. doi: 10.1155/2018/3086167
5. Bytzer P, Talley NJ, Hammer J, Young LJ, Jones MP et al. GI symptoms in diabetes mellitus are associated with both poor glycemic control and diabetic complications. The American Journal of Gastroenterology 2002; 97(3): 604-611. doi: 10.1111/j.1572-0241.2002.05537.x
6. Asgharnezhad M, Joukar F, Fathalipour M, Khosousi M, Hassanipour S et al. Gastrointestinal symptoms in patients with diabetes mellitus and non-diabetic: A cross-sectional study in north of Iran. Diabetes & Metabolic Syndrome 2019; 13(3): 2236-2240. doi: 10.1016/j.dsx.2019.05.028
7. Bytzer P, Talley NJ, Leemon M, Young LJ, Jones MP et al. Prevalence of gastrointestinal symptoms associated with diabetes mellitus: a population-based survey of 15 000 adults. Archives of Internal Medicine 2001; 161(16): 1989-1996. doi: 10.1001/archinte.161.16.1989
8. Ko GT, Chan WB, Chan JC, Tsang LW, Cockram CS. Gastrointestinal symptoms in Chinese patients with type 2 diabetes mellitus. Diabetic Medicine 1999; 16(8): 670-674. doi: 10.1046/j.1464-5491.1999.00135.x
9. Kase H, Hattori Y, Sato N, Banba N, Kasai K. Symptoms of gastroesophageal reflux in diabetes patients. Diabetes Research and Clinical Practice 2008; 79(2): e6-e7. doi: 10.1016/j. diabres.2007.08.019
10. Lluch I, Ascaso JF, Mora F, Minguez M, Peña A et al. Gastroesophageal reflux in diabetes mellitus. The American Journal of Gastroenterology 1999; 94(4): 919-924. doi: 10.1111/j.1572-0241.1999.987_j.x
11. Hamdan AL, Sharara AI, Younes A, Fuleihan N. Effect of aggressive therapy on laryngeal symptoms and voice characteristics in patients with gastroesophageal reflux. Acta Oto-laryngologica 2001; 121(7): 868-872. doi: 10.1080/00016480152602357
12. Tauber S, Gross M, Issing WJ. Association of laryngopharyngeal symptoms with gastroesophageal reflux disease. The Laryngoscope 2002; 112(5): 879-886. doi: 10.1097/00005537- 200205000-00019
13. Hamdan AL, Jabbour J, Barazi R, Korban Z, Azar ST. Prevalence of laryngopharyngeal reflux disease in patients with diabetes mellitus. Journal of Voice 2013; 27(4): 495-499. doi: 10.1016/j. jvoice.2012.07.010
14. Hamdan AL, Kurban Z, Azar ST. Prevalence of phonatory symptoms in patients with type 2 diabetes mellitus. Acta Diabetologica 2013; 50(5): 731-736. doi: 10.1007/s00592-012- 0392-3
15. Prince SA, Adamo KB, Hamel ME, Hardt J, Connor Gorber S et al. A comparison of direct versus self-report measures for assessing physical activity in adults: a systematic review. International Journal of Behavioral Nutrition and Physical Activity 2008; 5(1): 56. doi: 10.1186/1479-5868-5-56
16. Belafsky PC, Postma GN, Koufman JA. Validity and reliability of the reflux symptom index (RSI). Journal of Voice 2002; 16(2): 274-277. doi: 10.1016/s0892-1997(02)00097-8
17. Belafsky PC, Mouadeb DA, Rees CJ, Pryor JC, Postma GN et al. Validity and reliability of the Eating Assessment Tool (EAT-10). Annals of Otology, Rhinology & Laryngology 2008; 117(12): 919-924. doi: 10.1177/000348940811701210
18. Rosen CA, Lee AS, Osborne J, Zullo T, Murry T. Development and validation of the voice handicap index‐10. The Laryngoscope 2004; 114(9): 1549-1556. doi: 10.1097/00005537-200409000- 00009
19. Akbulut S, Aydinli FE, Kuşçu O, Özcebe E, Yilmaz T et al. Reliability and validity of the Turkish reflux symptom index. Journal of Voice 2020; 34(6): 965.e23-965.e28. doi: 10.1016/j. jvoice.2019.05.015
20. Demir N, Serel Arslan S, İnal Ö, Karaduman AA. Reliability and validity of the Turkish eating assessment tool (T-EAT-10). Dysphagia 2016; 31(5): 644-649. doi: 10.1007/s00455-016- 9723-9
21. Kiliç M, Okur E, Yildirim I, Oğüt F, Denizoğlu I et al. Reliability and validity of the Turkish version of the Voice Handicap Index. Journal of Ear, Nose, and Throat 2008; 18(3): 139-147.
22. Arffa RE, Krishna P, Gartner-Schmidt J, Rosen CA. Normative values for the voice handicap index-10. Journal of Voice 2012; 26(4): 462-465. doi: 10.1016/j.jvoice.2011.04.006
23. Mellitus D. Diagnosis and classification of diabetes mellitus. Diabetes Care 2005; 28(S37): S5-S10. doi: 10.2337/diacare.28. suppl_1.s37
24. Haffner SM, D’Agostino R, Mykkänen L, Tracy R, Howard B et al. Insulin sensitivity in subjects with type 2 diabetes. Relationship to cardiovascular risk factors: the Insulin Resistance Atherosclerosis Study. Diabetes Care 1999; 22(4): 562-568. doi: 10.2337/diacare.22.4.562
25. Abbott CA, Malik RA, van Ross ER, Kulkarni J, Boulton AJ. Prevalence and characteristics of painful diabetic neuropathy in a large community-based diabetic population in the UK. Diabetes Care 2011; 34(10): 2220-2224. doi: 10.2337/dc11- 1108
26. Daousi C, MacFarlane I, Woodward A, Nurmikko TJ, Bundred PE et al. Chronic painful peripheral neuropathy in an urban community: a controlled comparison of people with and without diabetes. Diabetic Medicine 2004; 21(9) :976-982. doi: 10.1111/j.1464-5491.2004.01271.x
27. Davies M, Brophy S, Williams R, Taylor A. The prevalence, severity, and impact of painful diabetic peripheral neuropathy in type 2 diabetes. Diabetes Care 2006; 29(7): 1518-1522. doi: 10.2337/dc05-2228
28. Alrawahi AH, Rizvi SGA, Al-Riyami D, Al-Anqoodi Z. Prevalence and risk factors of diabetic nephropathy in omani type 2 diabetics in Al-dakhiliyah region. Oman Medical Journal 2012; 27(3): 212. doi: 10.5001/omj.2012.48
29. Pedro RA, Ramon SA, Marc BB, Juan FB, Isabel MM. Prevalence and relationship between diabetic retinopathy and nephropathy, and its risk factors in the North-East of Spain, a population-based study. Ophthalmic Epidemiology 2010; 17(4): 251-265. doi: 10.3109/09286586.2010.498661
30. Gölaç H, Atalık G, Türkcan AK, Yapar D, Sel AT et al. Fiberoptic Endoscopic Evaluation of Swallowing in Patients with Type 2 Diabetes Who Have Self-Reported Swallowing Difficulties. Folia Phoniatrica et Logopaedica 2021; 73(4): 289-297. doi: 10.1159/000507623
31. Hamdan AL, Jabbour J, Nassar J, Dahouk I, Azar ST. Vocal characteristics in patients with type 2 diabetes mellitus. European Archives of Oto-Rhino-Laryngology 2012; 269(5): 1489-1495. doi: 10.1007/s00405-012-1933-7
32. Sayaca C. Swallowing dıfficulty and swallowing anxiety in patients with type-II diabetes mellitus. European Archives of Oto-Rhino-Laryngology 2020; 277(7): 2005-2010. doi: 10.1007/s00405-020-05902-2
33. Zakaria DA, Bekhet MM, Khodeir MS, Bassiouny SS, Saleh MM et al. Oropharyngeal Dysphagia and Diabetes Mellitus: Screening of 200 Type 1 and Type 2 Patients in Cairo, Egypt. Folia Phoniatrica et Logopaedica 2018; 70(3-4): 134-137. doi: 10.1159/000491079
34. Nishida T, Tsuji S, Tsujii M, Arimitsu S, Sato T et al. Gastroesophageal reflux disease related to diabetes: analysis of 241 cases with type 2 diabetes mellitus. Journal of Gastroenterology and Hepatology 2004; 19(3): 258-265. doi: 10.1111/j.1440-1746.2003.03288.x
35. Wang X, Pitchumoni C, Chandrarana K, Shah N. Increased prevalence of symptoms of gastroesophageal reflux diseases in type 2 diabetics with neuropathy. World Journal of Gastroenterology 2008; 14(5): 709. doi: 10.3748/wjg.14.709
36. Koufman JA. Low-acid diet for recalcitrant laryngopharyngeal reflux: therapeutic benefits and their implications. Annals of Otology, Rhinology & Laryngology 2011; 120(5): 281-287. doi: 10.1177/000348941112000501
37. Lechien JR, Huet K, Khalife M, De Marrez LG, Finck C et al. Alkaline, protein, low-fat and low-acid diet in laryngopharyngeal reflux disease: our experience on 65 patients. Clinical Otolaryngology 2019; 44(3): 379-384. doi: 10.1111/coa.13269
38. Yang J, Dehom S, Sanders S, Murry T, Krishna P et al. Treating laryngopharyngeal reflux: Evaluation of an anti-reflux program with comparison to medications. American Journal of Otolaryngology 2018; 39(1): 50-55. doi: 10.1016/j. amjoto.2017.10.014
39. Zalvan CH, Hu S, Greenberg B, Geliebter JA. A comparison of alkaline water and Mediterranean diet vs proton pump inhibition for treatment of laryngopharyngeal reflux. JAMA Otolaryngology–Head & Neck Surgery 2017; 143(10): 1023- 1029. doi: 10.1001/jamaoto.2017.1454
40. Hoy M, Domer A, Plowman EK, Loch R, Belafsky P. Causes of dysphagia in a tertiary-care swallowing center. Annals of Otology, Rhinology & Laryngology 2013; 122(5): 335-338. doi: 10.1177/000348941312200508
41. Koufman JA, Amin MR, Panetti M. Prevalence of reflux in 113 consecutive patients with laryngeal and voice disorders. Otolaryngology—Head and Neck Surgery 2000; 123(4): 385- 388. doi: 10.1067/mhn.2000.109935
42. Koufman JA, Aviv JE, Casiano RR, Shaw GY. Laryngopharyngeal reflux: position statement of the committee on speech, voice, and swallowing disorders of the American Academy of Otolaryngology-Head and Neck Surgery. Otolaryngology— Head and Neck Surgery 2002; 127(1): 32-35. doi: 10.1067/ mhn.2002.125760