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Hearing Loss and Rheumatic Disease

Audiologic, Cognitive Manifestations in Inflammatory Rheumatic Disease

Dillmuth-Miller, Susan AuD; Batson-Magnuson, LuAnn PhD, CCC-SLP

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doi: 10.1097/01.HJ.0000654920.33807.df
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Inflammatory rheumatic diseases (IRDs) are characterized by inflammation in the joints, muscles,1 and, for some, organs of the body, including the brain.2 Many are considered immune-mitigated diseases.3,4 Audiological manifestations have been found in patients with IRDs, although they vary considerably.5–8 Because the middle ear is composed of muscles, joints, and cartilage, IRDs have the potential to affect middle and inner ear functions due to inflammation, reduced vascularity, and ototoxic medications used to treat the condition itself.9 These variations in results can be explained not only by methodological differences but also a lack of consistency in hearing evaluation protocols.7,8,10,11 Cognitive-linguistic effects are also prevalent in this population. For the past two years, our clinic has been conducting a study examining the audiologic and cognitive effects of IRD.12 Notably, we have found that many of the published studies do not involve hearing and speech-language professionals.

Shutterstock, rheumatic disease, hearing loss, cognition.
Table 1
Table 1:
Cognitive and Audiologic Symptoms Across IRDs. Rheumatic disease, hearing loss, cognition.
Figure 1.
Figure 1.:
Hearing loss among women with IRD. Rheumatic disease, hearing loss, cognition.

INFLAMMATORY RHEUMATIC DISEASES

Inflammation in IRD impacts the joints, tendons, ligaments, bones, and muscles of the body, as well as the organs, depending on the specific diagnosis.1 Helmick, Felson, and Lawrence2 reported that over seven million individuals in the United States are living with IRD. More than 30 specific diseases fall under the umbrella of IRD,4,13 and 8.4 percent of women14 and five percent of men15 will be diagnosed with IRD during their lifetime. In addition to the primary symptoms of each of these diseases, individuals with IRD are at increased risk of cardiovascular and cerebrovascular diseases.16 Recent research provides evidence that the inflammatory process associated with IRD affects the brain for the most prevalent diseases, including systemic lupus erythematosus (SLE), rheumatoid arthritis (RA), fibromyalgia (FM), and Lyme disease.

The presence of inflammatory markers and proteins associated with an inflammatory process has been identified in the blood serum of patients with IRD. Serum evidence supports the presence of high levels of antiphospholipid antibodies in SLE.17 When persistently high, antiphospholipids impact vascular function, resulting in decreased blood flow and cognitive decline.16 Higher concentrations of secreted pro-inflammatory proteins have been found in individuals with RA, SLE, and Lyme disease,18–20 and individuals with RA, SLE, and FM have been found to have high levels of cytokines, chemokines, and prostaglandins,21–25 which are secreted as part of the immune response and associated with systemic inflammation. Elevated levels of cytokines are associated with decreased blood flow and reduced cognitive abilities,26 while elevated levels of chemokines are seen in patients with Alzheimer's disease.27 High levels of prostaglandins have been associated with deficits in memory.22

Imaging has provided additional evidence of brain changes resulting from chronic inflammation. EEGs of patients with SLE showed the presence of prolonged P300 latencies and reductions in P300 amplitudes, which are neuro-physiological analogues for cognitive dysfunction and indicate possible demyelination.18 MRI studies include evidence of the activation of glial cells,22 white matter lesions,28 cortical atrophy,28 ventricular dilation,28 hypoperfusion of lobes of the brain,29,30 and decreased gray matter volume,31 while a review of SPECT and PET scan evidence supports the presence of hypometabolism and decreased perfusion.28,30 These inflammatory brain changes are associated with cognitive dysfunction.

COGNITIVE CORRELATES

Research into the cognitive correlates of rheumatic disease has focused mostly on RA, SLE, FM, and more recently, Lyme disease. The prevalence of negative cognitive effects in IRDs varies greatly, with 30 to 70 percent of RA patients exhibiting cognitive deficits.32–34 In studies on patients with SLE, 50 to 80 percent of patients reported or displayed cognitive deficits, while 81 to 87 percent of patients with neuropsychiatric lupus exhibited cognitive deficits.35 Approximately 50 to 90 percent of individuals with FM36 and 48 percent of individuals with Lyme disease report having cognitive deficiencies.37 Individuals with IRDs may experience deficits in short-term, working, and episodic memory,17,23,31,38–42 verbal comprehension,15 attention,17,31,37,39,40,42–44 verbal fluency,14 cognitive response times,29,45 and executive functioning.46,47 These cognitive deficits often result in a reduced quality of life48 and early retirement.49

Preliminary findings from our study looked at word-finding and memory performance for subjects with RA, SLE, and Lyme disease.12 Out of 32 subjects, 33 to 53 percent had below-average word-finding abilities, and 25 to 50 percent of subjects fell below average for memory based on standardized assessments. No correlation was found between pain, sleepiness, emotional state or disease activity, and cognitive performance.

AUDIOLOGICAL CORRELATES

Studies examining IRDs and audiological manifestations are few and show varied results. The incidence of hearing loss in those with RA and SLE ranges between 24 and 89 percent.5–8,50–52 Mostly bilateral high-frequency sensorineural hearing loss is reported, which seems to develop within the first five years of diagnosis.5,8,10,52–54 Using age-matched controls, decreased thresholds were found in younger patients with SLE, and older patients had decreased thresholds in both the lower and higher frequencies.52 Although RA has the potential to affect joints and muscles, conductive hearing loss in this population is a lot less common.5,8,53,55 During flare-ups, bilateral and fluctuating sensorineural hearing loss has been observed in those with RA11 and unilateral hearing loss in those with SLE.50,51 In people with FM, the most common complaint was hyperacusis,56 and audiometric tests showed high-frequency sensorineural hearing loss,56,57 with auditory evoked potentials showing delayed P300s, suggesting possible auditory processing difficulties (APD).58 In those with chronic Lyme disease, hypersensitivity to sound was reported in 48 percent,59 and in another study, all five subjects were found to have mild-to-moderate auditory processing deficits.37 See Table 1 for symptoms across IRDs.

Our study conducted full audiological evaluations, tympanometry testing, and APD screenings on patients with IRDs.12 Of the 25 women aged 18 to 76 (x=45.1) who were tested, 84 percent had high-frequency sensorineural hearing loss, of which 81 percent had hearing loss that notched at 6 kHz (Fig. 1). Conductive component and tympanometric abnormalities were only observed in one person who had a history of otitis media. Of the 21 who could complete the SCAN-A, a screener for APD, 76 percent did not pass, notably in those with SLE, FM, and Lyme. Contralateral and ipsilateral acoustic reflexes were present at expected levels. All subjects with FM and Lyme reported having sensitivity to sound. Our data found no correlation between medications (methotrexate, NSAIDs, Plaquenil, and prednisone), disease state, or fatigue level, and hearing loss. Although our study is preliminary, our results show that people with IRD need the care of an audiologist and a speech-language pathologist.

AUDIOLOGICAL CONSIDERATIONS

  1. Based on the findings of our literature review and research, these suggestions can help best serve those with IRD:
  2. Talk to local physicians regarding the need to refer patients with IRD for hearing and cognitive-linguistic evaluations shortly after diagnosis.
  3. Monitor hearing levels throughout the course of the disease.
  4. Add questions about IRDs when discussing a patient's medical history. For example: “Do you see a rheumatologist? What medications do you take?”
  5. Include interoctaves 3 and 6 kHz.
  6. Conduct an APD screening if hearing thresholds are better than 25 dB at 1, 2, and 4 kHz.
  7. Consider that deficits in memory, word-finding, and attention may negatively impact APD testing and the validity of test outcomes.
  8. Refer those with IRD to a speech-language pathologist.

REFERENCES

1. Nancy Garrick DD. NIAMS Health Information on Arthritis and Rheumatic Diseases [Internet]. National Institute of Arthritis and Musculoskeletal and Skin Diseases. 2017 [cited 2019 Dec 16]. Available from: https://www.niams.nih.gov/health-topics/arthritis-rheumatic-diseases.
2. Fuggle NR, Howe FA, Allen RL, Sofat N. New insights into the impact of neuro-inflammation in rheumatoid arthritis. Front Neurosci [Internet]. 2014 Nov 6;8:357. Available from: http://dx.doi.org/10.3389/fnins.2014.00357.
3. Lawrence RC, Felson DT, Helmick CG, Arnold LM, Choi H, Deyo RA, et al. Estimates of the prevalence of arthritis and other rheumatic conditions in the United States. Part II. Arthritis Rheum [Internet]. 2008 Jan;58(1):26–35. Available from: http://dx.doi.org/10.1002/art.23176.
4. Mayo Clinic. Rheumatic Disease [Internet] [Internet]. Mayo Clinic. 2015. Available from: https://www.mayoclinichealthsystem.org/locations/mankato/services-and-treatments/rheumatology/rheumatic-diseases.
5. Öztürk A, Yalçin S, Kaygusuz I, Sahin S, Gök Ü, Karlidag T, et al. High-frequency hearing loss and middle ear involvement in rheumatoid arthritis. American Journal of Otolaryngology-Head and Neck Medicine and Surgery [Internet]. 2004;25(6):411–7. Available from: http://dx.doi.org/10.1016/j.amjoto.2004.06.001.
6. Pascual-Ramos V, Contreras-Yáñez I, Rivera-Hoyos P, Enríquez L, Ramírez-Anguiano J. Cumulative disease activity predicts incidental hearing impairment in patients with rheumatoid arthritis (RA). Clin Rheumatol [Internet]. 2014;33(3):315–21. Available from: http://link.springer.com/10.1007/s10067-014-2485-6.
7. Salvinelli, F., Cancilleri, F., Casale, M., et al. Hearing thresholds in patients affected by rheumatoid arthritis. Clin Otolaryngol Allied Sci. 2004;29:75–9.
8. Rahne T, Clauß F, Plontke SK, Keyßer G. Prevalence of hearing impairment in patients with rheumatoid arthritis, granulomatosis with polyangiitis (GPA, Wegener's granulomatosis), or systemic lupus erythematosus. Clin Rheumatol [Internet]. 2017;36(7):1501–10. Available from: http://dx.doi.org/10.1007/s10067-017-3651-4.
9. Emamifar A, Bjoerndal K, Hansen IMJ. Is Hearing Impairment Associated with Rheumatoid Arthritis? A Review. Open Rheumatol J [Internet]. 2016;10(1):26–32. Available from: http://benthamopen.com/ABSTRACT/TORJ-10-26.
10. Dikici O, Muluk NB, Tosun AK, Ünlüsoy I. Subjective audiological tests and transient evoked otoacoustic emissions in patients with rheumatoid arthritis: Analysis of the factors affecting hearing levels. Eur Arch Otorhinolaryngol [Internet]. 2009;266(11):1719–26. Available from: http://dx.doi.org/10.1007/s00405-009-0975-y.
11. Takatsu M, Higaki M, Kinoshita H. Ear Involvement in Patients with Rheumatoid Arthritis. Otology & Neurology. 2005;26:755–61.
12. Dillmuth-Miller S, Batson-Magnuson L. Audiological and Cognitive Manifestations in Rheumatic Disease. Canadian Audiology Association; 2019 Oct; Halifax, Nova Scotia.
13. American College of Rheumatology. Rheumatic diseases in America: The problem, the impact and the answers. American College of Rheumatology [Internet]. 2010; Available from: https://www.bu.edu>enact>files>2012/10>ACR_Whitepaper_SinglePg.
14. Warner J. One in 12 women will have autoimmune disease [Internet. 2011 Jan 10; Available from: http://www.webmd.com/rheumatoid-arthritis/news/20110110/1-in-12-women-willhave-autoimmune-disease.
15. Porter T.F., Branch, D.W. Lupus and pregnancy: can they go together? The Lupus Group of Western Australia [Internet]. 2000 Jan; Available from: http://www.lupuswa.com.au/aboutLupus/pregnancy.html.
16. Alhusain A, Bruce IN. Cardiovascular risk and inflammatory rheumatic diseases. Clin Med [Internet]. 2013 Aug;13(4):395–7. Available from: http://dx.doi.org/10.7861/clinmedicine.13-4-395.
17. Denburg SD, Carbotte RM, Denburg JA. Cognition and mood in systemic lupus erythematosus. Evaluation and pathogenesis. Ann N Y Acad Sci [Internet]. 1997 Aug 14;823:44–59. Available from: http://dx.doi.org/10.1111/j.1749-6632.1997.tb48378.x.
18. Hamed SA, Selim ZI, Elattar AM, Elserogy YM, Ahmed EA, Mohamed HO. Assessment of biocorrelates for brain involvement in female patients with rheumatoid arthritis. Clin Rheumatol [Internet]. 2012 Jan;31(1):123–32. Available from: http://dx.doi.org/10.1007/s10067-011-1795-1.
19. Resende C, Sanga NM, Paschoalotti AL, Zerbini CA. Neurologic manifestations in systemic lupus erythematosus. Rev Paul Med [Internet]. 1988;105(5):289–93. Available from: https://europepmc.org/abstract/med/3043631.
20. Aucott JN, Soloski MJ, Rebman AW, Crowder LA, Lahey LJ, Wagner CA, et al. CCL19 as a Chemokine Risk Factor for Posttreatment Lyme Disease Syndrome: a Prospective Clinical Cohort Study. Clin Vaccine Immunol [Internet]. 2016 Sep;23(9):757–66. Available from: http://dx.doi.org/10.1128/CVI.00071-16.
21. Katz RS, Heard AR, Mills M, Leavitt F. The Prevalence and Clinical Impact of Reported Cognitive Difficulties (Fibrofog) in Patients With Rheumatic Disease With and Without Fibromyalgia [Internet]. Vol. 10, JCR: Journal of Clinical Rheumatology. 2004. p. 53–8. Available from: http://dx.doi.org/10.1097/01.rhu.0000120895.20623.9f.
22. Hein AM, O'Banion MK. Neuroinflammation and cognitive dysfunction in chronic disease and aging. J Neuroimmune Pharmacol [Internet]. 2012 Mar;7(1):3–6. Available from: http://dx.doi.org/10.1007/s11481-011-9340-1.
23. Glass JM. Fibromyalgia and cognition. J Clin Psychiatry [Internet]. 2008;69 Suppl 2:20–4. Available from: https://www.ncbi.nlm.nih.gov/pubmed/18537459.
24. Kadetoff D, Lampa J, Westman M, Andersson M, Kosek E. Evidence of central inflammation in fibromyalgia–increased cerebrospinal fluid interleukin-8 levels. J Neuroimmunol [Internet]. 2012;242(1-2):33–8. Available from: https://www.sciencedirect.com/science/article/pii/S0165572811002992.
25. Garcia JJ, Gil JC, Olea AH, Galan RG. Altered Inflammatory Mediators in Fibromyalgia [Internet]. Vol. 07, Journal of Ancient Diseases & Preventive Remedies. 2017. Available from: http://dx.doi.org/10.4172/2329-8731.1000215.
26. Menza M, Dobkin RD, Marin H, Mark MH, Gara M, Bienfait K, et al. The role of inflammatory cytokines in cognition and other non-motor symptoms of Parkinson's disease. Psychosomatics [Internet]. 2010 Nov;51(6):474–9. Available from: http://dx.doi.org/10.1176/appi.psy.51.6.474.
27. Liu C, Cui G, Zhu M, Kang X, Guo H. Neuroinflammation in Alzheimer's disease: chemokines produced by astrocytes and chemokine receptors. Int J Clin Exp Pathol [Internet]. 2014 Dec 1;7(12):8342–55. Available from: https://www.ncbi.nlm.nih.gov/pubmed/25674199.
28. Kozora E, Laudenslager M, Lemieux A, West SG. Inflammatory and hormonal measures predict neuropsychological functioning in systemic lupus erythematosus and rheumatoid arthritis patients. J Int Neuropsychol Soc [Internet]. 2001 Sep;7(6):745–54. Available from: http://dx.doi.org/10.1017/s1355617701766106.
29. Hanly JG. Neuropsychiatric lupus. Rheumatic Disease Clinics of North America [Internet]. 2005;3(3). Available from: https://link.springer.com/article/10.1007/s11926-001-0020-7.
30. Donta ST, Noto RB, Vento JA. SPECT brain imaging in chronic Lyme disease. Clin Nucl Med [Internet]. 2012 Sep;37(9):e219–22. Available from: http://dx.doi.org/10.1097/RLU.0b013e318262ad9b.
31. Lutz J, Jäger L, de Quervain D, Krauseneck T, Padberg F, Wichnalek M, et al. White and gray matter abnormalities in the brain of patients with fibromyalgia: A diffusion-tensor and volumetric imaging study. Arthritis & Rheumatism: Official Journal of the American College of Rheumatology [Internet]. 2008;58(12):3960–9. Available from: https://onlinelibrary.wiley.com/doi/abs/10.1002/art.24070.
32. Appenzeller S, Bertolo MB, Costallat LTL. Cognitive impairment in rheumatoid arthritis. Methods Find Exp Clin Pharmacol [Internet]. 2004 Jun;26(5):339–43. Available from: http://dx.doi.org/10.1358/mf.2004.26.5.831324.
33. Bartolini M, Candela M, Brugni M, Catena L, Mari F, Pomponio G, et al. Are behaviour and motor performances of rheumatoid arthritis patients influenced by subclinical cognitive impairments? A clinical and neuroimaging study. Clin Exp Rheumatol [Internet]. 2002 Jul;20(4):491–7. Available from: https://www.ncbi.nlm.nih.gov/pubmed/12175104.
34. Shin SY, Julian L, Katz P. The relationship between cognitive function and physical function in rheumatoid arthritis. J Rheumatol [Internet]. 2013 Mar;40(3):236–43. Available from: http://dx.doi.org/10.3899/jrheum.120871.
35. Adelman DC, Saltiel E, Klinenberg JR. The neuropsychiatric manifestations of systemic lupus erythematosus: an overview. Semin Arthritis Rheum [Internet]. 1986 Feb;15(3):185–99. Available from: http://dx.doi.org/10.1016/0049-0172(86)90016-8.
36. Teodoro T, Edwards MJ, Isaacs JD. A unifying theory for cognitive abnormalities in functional neurological disorders, fibromyalgia and chronic fatigue syndrome: systematic review. J Neurol Neurosurg Psychiatry [Internet]. 2018 Dec;89(12):1308–19. Available from: http://dx.doi.org/10.1136/jnnp-2017-317823.
37. Logigian EL, Kaplan RF, Steere AC. Chronic Neurologic Manifestations of Lyme Disease. N Engl J Med [Internet]. 1990 Nov;323(21):1438–44. Available from: http://www.nejm.org/doi/abs/10.1056/NEJM199011223232102.
38. Calderón J, Flores P, Babul M, Aguirre JM, Slachevsky A, Padilla O, et al. Systemic lupus erythematosus impairs memory cognitive tests not affected by depression. Lupus [Internet]. 2014 Sep;23(10):1042–53. Available from: http://dx.doi.org/10.1177/0961203314536247.
39. Coín-Mejías MA, Peralta-Ramírez MI, Santiago-Ramajo S, Morente-Soto G, Ortego-Centeno N, Rubio J-LC, et al. Alterations in episodic memory in patients with systemic lupus erythematosus. Arch Clin Neuropsychol [Internet]. 2008 Mar;23(2):157–64. Available from: http://dx.doi.org/10.1016/j.acn.2007.11.001.
40. Maneeton B, Maneeton N, Louthrenoo W. Cognitive Deficit in Patients with Sys-temic Lupus Erythematosus. Asian Pac J Allergy Immunol [Internet]. 2010;28(1):77. Available from: https://www.researchgate.net/profile/Narong_Maneeton/publication/44653378_Cognitive_Deficit_in_Patients_with_Systemic_Lupus_Erythematosus/links/09e415069b38c8113f000000.pdf.
41. Kaplan RF, Jones-Woodward L, Workman K, Steere AC, Logigian EL, Meadows ME. Neuropsychological deficits in Lyme disease patients with and without other evidence of central nervous system pathology. Appl Neuropsychol [Internet]. 1999;6(1):3–11. Available from: http://dx.doi.org/10.1207/s15324826an0601_1.
42. Halperin JJ, Krupp LB, Golightly MG, Volkman DJ. Lyme borreliosis-associated encephalopathy. Neurology [Internet]. 1990 Sep 1 [cited 2019 Dec 16];40(9):1340–1340. Available from: https://n.neurology.org/content/40/9/1340.short.
43. Dick B, Eccleston C, Crombez G. Attentional functioning in fibromyalgia, rheumatoid arthritis, and musculoskeletal pain patients. Arthritis Rheum [Internet]. 2002 Dec 15;47(6):639–44. Available from: http://dx.doi.org/10.1002/art.10800.
44. Glass JM, Park DC, Crofford LJ. Memory performance with divided attention in fibromyalgia (FM) patients. In: Arthritis and Rheumatism. WILEY-LISS DIV JOHN WILEY & SONS INC, 111 RIVER ST, HOBOKEN, NJ 07030 USA; 2004. p. S489–S489.
45. Harrison MJ, Morris KA, Horton R, Toglia J, Barsky J, Chait S, et al. Results of intervention for lupus patients with self-perceived cognitive difficulties [Internet]. Vol. 65, Neurology. 2005. p. 1325–7. Available from: http://dx.doi.org/10.1212/01.wnl.0000180938.69146.5e.
46. Schmidt H, Djukic M, Jung K, Holzgraefe M, Dechent P, von Steinbüchel N, et al. Neurocognitive functions and brain atrophy after proven neuroborreliosis: a case-control study. BMC Neurol [Internet]. 2015 Aug 19;15:139. Available from: http://dx.doi.org/10.1186/s12883-015-0386-1.
47. de Melo LF, Da-Silva SL. Neuropsychological assessment of cognitive disorders in patients with fibromyalgia, rheumatoid arthritis, and systemic lupus erythematosus. Rev Bras Reumatol [Internet]. 2012 Mar;52(2):181–8. Available from: https://www.ncbi.nlm.nih.gov/pubmed/22460408.
48. Schmeding A, Schneider M. Fatigue, health-related quality of life and other patient-reported outcomes in systemic lupus erythematosus. Best Pract Res Clin Rheumatol [Internet]. 2013 Jun;27(3):363–75. Available from: http://dx.doi.org/10.1016/j.berh.2013.07.009.
49. Uhlig T, Moe RH, Kvien TK. The burden of disease in rheumatoid arthritis. Pharmacoeconomics [Internet]. 2014 Sep;32(9):841–51. Available from: http://dx.doi.org/10.1007/s40273-014-0174-6.
50. Roverano S, Cassano G, Paira S, Chiavarini J, Graf C, Rico L, et al. Asymptomatic sensorineural hearing loss in patients with systemic lupus erythematosus. J Clin Rheumatol [Internet]. 2006;12(5):217–20. Available from: http://dx.doi.org/10.1097/01.rhu.0000242777.71604.69.
51. Maciaszczyk K, Durko T, Waszczykowska E, Erkiert-Polguj A, Pajor A. Auditory function in patients with systemic lupus erythematosus. Auris Nasus Larynx [Internet]. 2011;38(1):26–32. Available from: http://dx.doi.org/10.1016/j.anl.2010.04.008.
52. Andonopoulos AP, Naxakis S, Goumas P, Lygatsikas C. Sensorineural hearing disorders in systemic lupus erthematosus. A controlled study. ClinExpRheumatol. 1995;13:137–41.
53. Halligan CS, Bauch CD, Brey RH, Achenbach SJ, Bamlet WR, McDonald TJ, et al. Hearing loss in rheumatoid arthritis. Laryngoscope. 2006;116:2044–9.
54. Murdin L, Patel S, Walmsley J, Yeoh LH. Hearing difficulties are common in patients with rheumatoid arthritis. Clin Rheumatol [Internet]. 2008;27(5):637–40. Available from: http://dx.doi.org/10.1007/s10067-007-0802-z.
55. Roberts CM. The Impact of rheumatoid arthritis on middle ear function. 2012. Dissertation in fulfillment of Au.D. Degree at the University of Maryland, College Park, MD.
56. Wolfe F, Rasker JJ, Häuser W. Hearing loss in fibromyalgia? Somatic sensory and non-sensory symptoms in patients with fibromyalgia and other rheumatic disorders. Clin Exp Rheumatol [Internet]. 2012 Nov;30(6 Suppl 74):88–93. Available from: https://www.ncbi.nlm.nih.gov/pubmed/23137751.
57. Kapusuz Gencer Z, Balbaloglu Ö, Özkiris M, Saydam L. Does fibromyalgia have an effect on hearing loss in women? Turk J Med Sci [Internet]. 2017 Dec 19;47(6):1699–702. Available from: http://dx.doi.org/10.3906/sag-1511-25.
58. Bayazit YA, Gürsoy S, Ozer E, Karakurum G, Madenci E. Neurotologic manifestations of the fibromyalgia syndrome. J Neurol Sci [Internet]. 2002 Apr 15;196(1-2):77–80. Available from: http://dx.doi.org/10.1016/s0022-510x(02)00032-1.
59. Nields JA, Fallon BA, Jastreboff PJ. Carbamazepine in the Treatment of Lyme Disease–Induced Hyperacusis. J Neuropsychiatry Clin Neurosci [Internet]. 1999;11(1):97–9. Available from: http://neuro.psychiatryonline.org/cgi/content/abstract/11/1/97.
60. Chen Y-M, Chen H-H, Lan J-L, Chen D-Y. Improvement of cognition, a potential benefit of anti-TNF therapy in elderly patients with rheumatoid arthritis [Internet]. Vol. 77, Joint Bone Spine. 2010. p. 366–7. Available from: http://dx.doi.org/10.1016/j.jbspin.2010.01.017.
    61. Gimeno D, Marmot MG, Singh-Manoux A. Inflammatory markers and cognitive function in middle-aged adults: the Whitehall II study. Psychoneuroendocrinology [Internet]. 2008 Nov;33(10):1322–34. Available from: http://dx.doi.org/10.1016/j.psyneuen.2008.07.006.
      62. Cutolo M, Kitas GD, van Riel PLCM. Burden of disease in treated rheumatoid arthritis patients: going beyond the joint. Semin Arthritis Rheum [Internet]. 2014 Feb;43(4):479–88. Available from: http://dx.doi.org/10.1016/j.semarthrit.2013.08.004.
        63. Murthy VA, Kumar JM. Rheumatoid Factor and Hearing Loss. 2016;64(4):9–13. Available from: http://dx.doi.org/10.1007/sl2070-011-0401-9.
          64. Milisavljevic D, Stankovic I, Jovanovic J, Živkovic Marinkov E, Krstic M, Stankovic T. Hearing Loss in Rheumatoid Arhritis. Facta Universitatis, Series: Medicine and Biology [Internet]. 2017;18(2):64–64. Available from: http://casopisi.junis.ni.ac.rs/index.php/FUMedBiol/article/view/2183.
            65. Selim ZI, Hamed SA, Elattar AM. Peripheral and central auditory pathways function with rheumatoid arthritis. Int J Clin Rheumtol [Internet]. 2015;10(2):85–96. Available from: http://www.scopus.com/inward/record.url?eid=2-s2.0-84928635615&partnerID=40&md5=0214dc77b4c8008e3cb08b7e3ef0be3f.
              66. Yilmaz S, Erbek S, Erbek SS, Ozgirgin N, Yucel E. Abnormal electronystagmography in rheumatoid arthritis. Auris Nasus Larynx [Internet]. 2007;34(3):307–11. Available from: http://dx.doi.org/10.1016/j.anl.2006.11.003.
                67. Lin C, Lin S-W, Weng S-F, Lin Y-S. Risk of Sudden Sensorineural Hearing Loss in Patients with Systemic Lupus Erythematosus: A Population-Based Cohort Study [Internet]. Vol. 18, Audiology and Neurotology. 2013. p. 95–100. Available from: http://dx.doi.org/10.1159/000345512.
                  68. Sperling NM, Tehrani K, Liebling A, Ginzler E. Aural symptoms and hearing loss in patients with lupus. Otolaryngol Head Neck Surg [Internet]. 1998;118(6):762–5. Available from: http://dx.doi.org/10.1016/S0194-5998(98)70265-7.
                    69. Karatas E, Onat AM, Durucu C, Baglam T, Kanlikama M, Altunoren O, et al. Audiovestibular disturbance in patients with systemic lupus erythematosus. Otolaryngol Head Neck Surg [Internet]. 2007;136(1):82–6. Available from: http://dx.doi.org/10.1016/j.otohns.2006.06.1255.
                      70. Bowman C a., Linthicum FH, Nelson R a., Mikami K, Quismorio F. Sensorineural hearing loss associated with systemic lupus erythematosus. Otolaryngol Head Neck Surg. 1986;94(2):197–204.
                      71. Abbasi M, Yazdi Z, Kazemifar AM, Bakhsh ZZ. Hearing Loss in Patients with Systemic Lupus Erythematosus. Glob J Health Sci [Internet]. 2013;5(5):102–6. Available from: http://www.ccsenet.org/journal/index.php/gjhs/article/view/27469.
                        72. Batuecas-Caletrío A, Del Pino-Montes J, Cordero-Civantos C, Calle-Cabanillas M, Lopez-Escamez J. Hearing and vestibular disorders in patients with systemic lupus erythematosus. Lupus [Internet]. 2013;22(5):437–42. Available from: http://dx.doi.org/10.1177/0961203313477223.
                          73. Bruner AP, Sato EI, Pereira LD. Central auditory processing in patients with systemic lupus erythematosus. Acta Reumatol Port [Internet]. 2009 Oct;34(4):600–7. Available from: https://www.ncbi.nlm.nih.gov/pubmed/20852573.
                            74. Elkins LE, Pollina DA, Scheffer SR, Krupp LB. Psychological states and neuropsychological performances in chronic Lyme disease. Appl Neuropsychol [Internet]. 1999;6(1):19–26. Available from: http://dx.doi.org/10.1207/s15324826an0601_3.
                              75. Fallon BA, Nields JA, Burrascano JJ, Liegner K, DelBene D, Liebowitz MR. The neuropsychiatric manifestations of Lyme borreliosis. Psychiatr Q [Internet]. 1992 Spring;63(1):95–117. Available from: http://dx.doi.org/10.1007/bf01064684.
                                76. Benke T, Gasse T, Hittmair-Delazer M, Schmutzhard E. Lyme encephalopathy: long-term neuropsychological deficits years after acute neuroborreliosis. Acta Neurol Scand [Internet]. 1995;91(5):353–7. Available from: https://onlinelibrary.wiley.com/doi/abs/10.1111/j.1600-0404.1995.tb07020.x.
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