Estimation of hearing impairment occurrence in patients with Lyme borreliosis – preliminary study
 
More details
Hide details
1
Department of Infectious Diseases and Hepatology, School of Medicine with the Division of Dentistry in Zabrze, Medical University of Silesia, Katowice, Poland
 
2
Department of Otorhinolaryngology and Oncological Laryngology, School of Medicine with the Division of Dentistry in Zabrze, Medical University of Silesia, Katowice, Poland
 
3
ENT-Clinic – Gaertner-Klinik, Munich, Germany
 
 
Corresponding author
Barbara Oczko-Grzesik   

Department of Infectious Diseases and Hepatology, School of Medicine with the Division of Dentistry in Zabrze, Medical University of Silesia, Katowice, Poland, al. Legionów 49, 41-902 Bytom, Poland
 
 
Ann. Acad. Med. Siles. 2018;72:164-171
 
KEYWORDS
TOPICS
ABSTRACT
Introduction:
Lyme borreliosis (LB) is the most common tick-borne human disease. The objective of the study was to carry out preliminary evaluation of the incidence of hearing impairments in LB patients.

Material and methods:
Audiometric tests were carried out on 66 patients with diagnosed LB (aged between 18 and 45 years). All the women and men were divided into two major groups: 1 – early, disseminated LB and 2 – late LB; among them subgroups of Lyme neuroborreliosis (LNB) were distinguished. The hearing organ was diagnosed on the basis of tonal audiometry, extended high-frequency tonal audiometry (up to 18 kHz), impedance audiometry and speech audiometry tests.

Results:
Abnormal results of the audiometric tests were recorded in 66.7% of patients. The statistical analysis indicates a significant role of borrelial infection (p = 0.017). Most of those were in patients suffering from late stages of the disease, both in patients with LB and LNB.

Conclusions:
The study revealed the occurrence of hearing impairment of different degrees in more than one half of the patients with LB, especially in the late stages of the disease. The results indicate the necessity for further comprehensive studies, considering hearing and balance disorders in the course of LB, comprising larger groups of patients.

 
REFERENCES (70)
1.
Stanek G., Fingerle V., Hunfeld K.P., Jaulhac B., Kaiser R., Krause A., Kristoferitsch W., O'Connell S., Ornstein K., Strle F., Gray J. Lyme borreliosis: clinical case definitions for diagnosis and management in Europe. Clin. Microbiol. Infect. 2011; 17(1): 69–79, doi: 10.1111/j.1469-0691.2010.03175.x.
 
2.
Lyme disease [Internet]. Atlanta: U.S. Centers for Disease Control and Prevention; 2016 [cited 2017 May 02]. Available from:.http://www.cdc.gov/lyme/stats/....
 
3.
Czupryna P., Moniuszko-Malinowska A., Pancewicz S., Garkowski A., Gościk J., Siemieniako A., Zajkowska J. Lyme disease in Poland – a serious problem? Adv. Med. Sci. 2016; 61(1): 96–100, doi: 10.1016/j.advms.2015.10.007.
 
4.
Choroby zakaźne 01.01.–31.12.2015 [Infectious diseases 01.01.–31.12.2015] [Internet]. Warsaw, Poland: National Institute of Public Health – National Institute of Higiene; 2016 [cited 2017 May 02]. Polish. Available from: http://wwwold.pzh.gov.pl/oldpa....
 
5.
Choroby zakaźne 01.01.-31.12.2016 [Infectious diseases 01.01.–31.12.2016] [Internet]. Warsaw, Poland: National Institute of Public Health – National Institute of Higiene; 2017 [cited 2017 May 02]. Polish. Available from: http://wwwold.pzh.gov.pl/oldpa....
 
6.
Paradowska-Stankiewicz I., Chrześcijańska I. Lyme disease in Poland in 2013. Przegl. Epidemiol. 2015; 69: 763–764.
 
7.
Shapiro E.D. Clinical practice. Lyme disease. N. Engl. J. Med. 2014; 370(18): 1724–1731, doi: 10.1056/NEJMcp1314325.
 
8.
Mygland A., Ljøstad U., Fingerle V., Rupprecht T., Schmutzhard E., Steiner I. EFNS guidelines on the diagnosis and management of European Lyme neuroborreliosis. Eur. J. Neurol. 2010; 17(1): 8–16, e1–4, doi: 10.1111/j.1468-1331.2009.02862.x
 
9.
Sanchez J.L. Clinical manifestations and treatment of Lyme disease. Clin. Lab. Med. 2015; 35(4): 765–778, doi: 10.1016/j.cll.2015.08.004.
 
10.
Stanek G., Wormser G.P., Gray J., Strle F. Lyme borreliosis. Lancet 2012; 379(9814): 461–473, doi: 10.1016/S0140-6736(11)60103-7.
 
11.
Abuzied W.M., Ruckenstein M.J. Spirochetes in otology: are we testing for the right pathogens? Otolaryngol. Head Neck Surg. 2008; 138(1): 107–109, doi: 10.1016/j.otohns.2007.10.012.
 
12.
Lorenzi M.C., Bittar R.S., Pedalini M.E., Zerati F., Yoshinari N.H., Bento R.F. Sudden deafness and Lyme disease. Laryngoscope 2003; 113(2): 312–315, doi: 10.1097/00005537-200302000-00021.
 
13.
Marinopoulos S.S., Coylewright M., Auwaerter P.G., Flynn J.A. Clinical problem-solving. More than meets the ear. N. Engl. J. Med. 2010; 362(13): 1228–1233, doi: 10.1056/NEJMcps0808968.
 
14.
Peeters N., van der Kolk B.Y., Thijsen S.F., Colnot D.R. Lyme disease associated with sudden sensorineural hearing loss: case report and literature review. Otol. Neurotol. 2013; 34(5): 832–837, doi: 10.1097/MAO.0b013e31827c9f93.
 
15.
Walther L.E., Hentschel H., Oehme A., Gudziol H., Beleites E. Lyme disease – a reason for sudden sensorineural hearing loss and vestibular neuronitis? [Article in German]. Laryngorhinootologie 2003; 82(4): 249–257, doi: 10.1055/s-2003-38938.
 
16.
Espiney Amaro C., Montalvão P., Huins C., Saraiva J. Lyme disease: sudden hearing loss as the sole presentation. J. Laryngol. Otol. 2015; 129(2): 183–186, doi: 10.1017/S0022215114003417.
 
17.
Bertholon P., Cazorla C., Carricajo A., Oletski A., Laurent B. Bilateral sensorineural hearing loss and cerebellar ataxia in the case of late stage Lyme disease. Braz. J. Otorhinolaryngol. 2012; 78(6): 124.
 
18.
Iero I., Elia M., Cosentino F.I., Lanuzza B., Spada R.S., Toscano G., Tripodi M., Belfiore A., Ferri R. Isolated monolateral neurosensory hearing loss as a rare sign of neuroborreliosis. Neurol. Sci. 2004; 25(1): 30–33, doi: 10.1007/s10072-004-0224-8.
 
19.
Mehler K., Emmel M., Petereit H.F., Sprüth A., Dröge A., Brockmeier K. Sensorineural loss of hearing in lower registers as the main symptom of Lyme disease. [Article in German]. HNO 2007; 55(12): 961–963, doi: 10.1007/s00106-006-1490-8.
 
20.
R* Core Team. R: A language and environment for statistical compu-ting. Vienna, Austria: R Foundation for Statistical Computing; 2016 [cited 2016 May 21]. Available from: http://www.R-project.org.
 
21.
Halperin J.J. Chronic Lyme disease: misconceptions and challenges for patient management. Infect. Drug Resist. 2015; 8: 119–128, doi: 10.2147/IDR.S66739.
 
22.
Pancewicz S.A., Garlicki A.M., Moniuszko-Malinowska A., Zajkowska J., Kondrusik M., Grygorczuk S., Czupryna P., Dunaj J. Diagnosis and treatment of tick-borne diseases recommendations of the Polish Society of Epidemiology and Infectious Diseases. Przegl. Epidemiol. 2015; 69(2): 309–316.
 
23.
Melia M.T., Lantos P.M., Auwaerter P.G. Lyme disease: authentic imitator or wishful imitation? JAMA Neurol. 2014; 71(10): 1209–1210.
 
24.
Halperin J.J., Baker P., Wormser G.P. Common misconceptions about Lyme disease. Am. J. Med. 2013; 126(3): 264, e1–7, doi: 10.1016/j.amjmed.2012.10.008.
 
25.
Nelson C., Elmendorf S., Mead P. Neoplasms misdiagnosed as “chronic lyme disease”. JAMA Intern. Med. 2015; 175(1): 132–133, doi: 10.1001/jamainternmed.2014.5426.
 
26.
Reid M.C., Schoen R.T., Evans J., Rosenberg J.C., Horwitz R.I. The consequences of overdiagnosis and overtreatment of Lyme disease: an observational study. Ann. Intern. Med. 1998; 128(5): 354–362.
 
27.
Behera A.K., Hildebrand E., Scagliotii J., Steere A.C., Hu L.T. Induction of host matrix metalloproteinases by Borrelia burgdorferi differs in human and murine Lyme arthritis. Infect. Immun. 2005; 73(1): 126–134, doi: 10.1128/IAI.73.1.126-134.2005.
 
28.
Ristow L.C., Miller H.E., Padmore L.J., Chettri R., Salzman N., Caimano M.J., Rosa P.A., Coburn J. The β3-integrin ligand of Borrelia burgdorferi is critical for infection of mice but not ticks. Mol. Microbiol. 2012; 85(6): 1105–1118, doi: 10.1111/j.1365-2958.2012.08160.x.
 
29.
Hove P.R., Haldorson G.J., Magunda F., Bankhead T. Presence of Arp specifically contributes to joint tissue edema associated with early-onset Lyme arthritis. Infect. Immun. 2014; 82(1): 43–51, doi: 10.1128/IAI.01061-13.
 
30.
Pachner A.R., Steiner I. Lyme neuroborreliosis: infection, immunity and inflammation. Lancet Neurol. 2007; 6(6): 544–552.
 
31.
Petzke M., Schwartz I. Borrelia burgdorferi Pathogenesis and the Immune Response. Clin. Lab. Med. 2015; 35(4): 745–764, doi: 10.1016/j.cll.2015.07.004.
 
32.
Ramesh G., MacLean A.G., Philipp M.T. Cytokines and chemokines at the crossroads of neuroinflammation, neurodegeneration and neuropathic pain. Mediators Inflamm. 2013; 2013: 480739, doi: 10.1155/2013/480739.
 
33.
Rupprecht T.A., Koedel U., Fingerle V., Pfister H.W. The pathogenesis of Lyme neuroborreliosis: from infection to inflammation. Mol. Med. 2008; 14(3–4): 205–212.
 
34.
Steere A.C., Klitz W., Drouin E.E., Falk B.A., Kwok W.W., Nepom G.T., Baxter-Lowe L.A. Antibiotic-refractory Lyme arthritis is associated with HLA-DR molecules that bind a Borrelia burgdorferi peptide. J. Exp. Med. 2006; 203(4): 961–971.
 
35.
Kovalchuka L., Cvetkova S., Trofimova J., Eglite J., Gintere S., Lucenko I., Oczko-Grzesik B., Viksna L., Krumina A. Immunogenetic markers defini-tion in Latvian patients with Lyme borreliosis and Lyme neuroborreliosis. Int. J. Environ. Res. Public Health 2016; 13(12): E1194, doi: 10.3390/ijerph13121194.
 
36.
Antonara S., Ristow L., Coburn J. Adhesion mechanisms of Borrelia burgdorferi. Adv. Exp. Med. Biol. 2011; 715: 35–49, doi: 10.1007/978-94-007-0940-9_3.
 
37.
Behera A.K., Hildebrand E., Szafranski J., Hung H.H., Grodzinsky A.J., Lafyatis R., Koch A.E., Kalish R., Perides G., Steere A.C., Hu L.T. Role of aggrecanase 1 in Lyme arthritis. Arthritis Rheum. 2006; 54(10): 3319–3329, doi: 10.1002/art.22128.
 
38.
Behera A.K., Hildebrand E., Uematsu S., Akira S., Coburn J., Hu L.T. Identification of a TLR-independent pathway for Borrelia burgdorferi-induced expression of matrix metalloproteinases and inflammatory mediators through binding to integrin alpha 3 beta 1. J. Immunol. 2006; 177(1): 657–664.
 
39.
Imai D., Holden K., Velazquez E.M., Feng S., Hodzic E., Barthold S.W. Influence of arthritis-related protein (BBF01) on infectivity of Borrelia burgdorferi B31. BMC Microbiol. 2013; 13: 100, doi: 10.1186/1471-2180-13-100.
 
40.
Pancewicz S.A., Rutkowski R., Rutkowski K., Zajkowska J.M., Kondrusik M. Immunopathology of Lyme arthritis. [Article in Polish]. Pol. Merkur. Lekarski 2007; 23(134): 141–144.
 
41.
Pancewicz S., Popko J., Rutkowski R., Knaś M., Grygorczuk S., Guszczyn T., Bruczko M., Szajda S., Zajkowska J., Kondrusik M., Sierakowski S., Zwierz K. Activity of lysosomal exoglycosidases in serum and synvial fluid in patients with chronic Lyme and rheumatoid arthritis. Scand. J. Infect. Dis. 2009; 41(8): 584–589, doi: 10.1080/00365540903036220.
 
42.
Zajkowska J., Drozdowski W. Neuroborreliosis – diagnostics difficulties. Neurologia po Dyplomie. 2013; 8(1): 6–15.
 
43.
Trollmo C., Meyer A.L., Steere A.C., Hafler D.A., Huber B.T. Molecular mimicry in Lyme arthritis demonstrated at the single cell level: LFA-1 alpha L is a partial agonist for outer surface protein A-reactive T cells. J. Immunol. 2001; 166(8): 5286–5291.
 
44.
Strle K., Jones K.L., Drouin E.E., Li X., Steere A.C. Borrelia burgdorferi RST1 (OspC type A) genotype is associated with greater inflammation and more severe Lyme disease. Am. J. Pathol. 2011; 178(6): 2726–2739, doi: 10.1016/j.ajpath.2011.02.018.
 
45.
Zajkowska J., Stalewska J., Kondrusik M., Kuśmierczyk J., Czupryna P., Grygorczuk S., Pancewicz S. Serum concentration of selected adhesive molecules in early localised and late disseminated Lyme borreliosis. Przegl. Epidemiol. 2008; 62(1): 77–84.
 
46.
Grygorczuk S. Apoptosis of immune system cells in Lyme borreliosis [habilitation’s thesis]. Medical University of Białystok, Poland 2013.
 
47.
Strle K., Lochhead R.B., Pianta A., Crowley J.T., Arvikar S.L., Aversa J.M. Fibroblast-like synovicytes shape and perpetuate immune responses associated with antibiotic-refractory Lyme arthritis. In: Proceedings of the 14th International Conference on Lyme Borreliosis and Other Tick-Borne Disea-ses. Vienna, Austria 2015 Sept 27–30. Ed.: Avšič-Zupanec T., Barbour A.G., Bergström S. et al. ROBIDRUCK, Vienna 2015: 7–8.
 
48.
Hansen K., Crone C., Kristoferitsch W. Lyme neuroborreliosis. Handb. Clin. Neurol. 2013; 115: 559–575, doi: 10.1016/B978-0-444-52902-2.00032-1.
 
49.
Ramesh G., Borda J.T., Dufour J., Kaushal D., Ramamoorthy R., Lackner A.A., Philipp M.T. Interaction of the Lyme disease spirochete Borrelia burgdorferi with brain parenchyma elicits inflammatory mediators from glial cells as well as glial and neuronal apoptosis. Am. J. Pathol. 2008; 173(5): 1415–1427, doi: 10.2353/ajpath.2008.080483.
 
50.
Miklossy J. Chronic or late Lyme neuroborreliosis: analysis of evidence compared to chronic or late neurosyphilis. Open Neurol. J. 2012; 6: 146–157, doi: 10.2174/1874205X01206010146.
 
51.
Miklossy J. Alzheimer’s disease – a neurospirochetosis. Analysis of the evidence following Koch’s and Hill’s criteria. J. Neuroinflammation 2011; 8: 90, doi: 10.1186/1742-2094-8-90.
 
52.
Miklossy J. Historic evidence to support a casual relationship between spirochetal infections and Alzheimer’s disease. Front. Aging Neurosci. 2015; 7: 46, doi: 10.3389/fnagi.2015.00046.
 
53.
Bakker R., Aarts M.C., van der Heijden G.J., Rovers M.M. No evidence for the diagnostics value of Borrelia serology in patients with sudden hearing loss. Otolaryngol. Head Neck Surg. 2012; 146(4): 539–543, doi: 10.1177/0194599811432535.
 
54.
Bertholon P. Sensorineural hearing loss: a complex feature in Lyme disease. Otol. Neurotol. 2013; 34(8): 1543, doi: 10.1097/MAO.0b013e3182a007d4.
 
55.
Hassepass F., Schild C., Aschendorff A., Laszig R., Maier W., Beck R., Wesarg T., Arndt S. Clinical outcome after cochlear implantation in patients with unilateral hearing loss due to labyrinthitis ossificans. Otol. Neurotol. 2013; 34(7): 1278–1283, doi: 10.1097/MAO.0b013e3182937ad4.
 
56.
Saunders J.E. Routine testing for Borrelia serology in sudden sensorineural hearing loss. Otolaryngol. Head Neck Surg. 2013; 148(1): 179–180, doi: 10.1177/0194599812468276.
 
57.
Ewers E.C., Dennison D.H., Stagliano D.R. A unique case of adolescent neuroborreliosis presenting with multiple cranial neuritis and cochlear inflammation on magnetic resonance imaging. Pediatr. Neurol. 2015; 52(1): 107–109, doi: 10.1016/j.pediatrneurol.2014.10.009.
 
58.
Huda S., Wieshmann U.C. Protracted neuroborreliosis – an unusual cause of encephalomyelitis. BMJ Case Rep. 2012; bcr1120115206, doi: 10.1136/bcr.11.2011.5206.
 
59.
Maniu A., Damian L. Rapid progressive bilateral hearing loss due to granulomatous otitis media in Lyme disease. Am. J. Otolaryngol. 2013; 34(3): 245–247, doi: 10.1016/j.amjoto.2012.11.009.
 
60.
Verma V., Roman M., Shah D., Zaretskaya M., Yassin M.H. A case of chronic progressive Lyme encephalitis as a manifestation of late Lyme neuroborreliosis. Infect. Dis. Rep. 2014; 6(4): 5496, doi: 10.4081/idr.2014.5496.
 
61.
Halperin JJ. Nervous system Lyme disease. Clin. Lab. Med. 2015; 35(4): 779–795, doi: 10.1016/j.cll.2015.07.002.
 
62.
Halperin JJ. Nervous system Lyme disease, chronic Lyme disease, and none of the above. Acta Neurol. Belg. 2016; 116(1): 1–6, doi: 10.1007/s13760-015-0541-x.
 
63.
Koedel U., Fingerle V., Pfister H.W. Lyme neuroborreliosis – epidemiology, diagnosis and management. Nat. Rev. Neurol. 2015; 11(8): 446–456, doi: 10.1038/nrneurol.2015.121.
 
64.
Zajkowska J.M., Kułakowska A., Tarasiuk J., Pancewicz S.A., Drozdowski W. Peripheral neuropathies in Lyme borreliosis. [Article in Polish]. Pol. Merkur. Lekarski 2010; 29(170): 115–118.
 
65.
Grygorczuk S., Péter O., Kondrusik M., Moniuszko A., Zajkowska J., Dunaj J., Żukiewicz-Sobczak W., Pancewicz S. Assement of the frequency of different Borrelia burgdorferi sensu lato species in patients with Lyme borreliosis from north-east Poland by studying preferential serologic response and DNA isolates. Ann. Agric. Environ. Med. 2013; 20(1): 21–29.
 
66.
Rozwadowska B., Hudzik G. Borrelia burgdorferi genostrains detected in the Silesian Voivodeship in years 2010–2012. [Article in Polish]. Przegl. Epidemiol. 2012; 66(4): 587–590.
 
67.
Strzelczyk J.K., Gaździcka J., Cuber P., Asman M., Trapp G., Gołąbek K., Zalewska-Ziob M., Nowak-Chmura M., Siuda K., Wiczkowski A., Solarz K. Prevalence of Borrelia burgdorferi sensu lato in Ixodes ricinus ticks collected from southern Poland. Acta Parasitol. 2015; 60(4): 666–674, doi: 10.1515/ap-2015-0095.
 
68.
Janczewski G. Practical otolaryngology. Via Medica, Gdańsk 2005.
 
69.
Oczko-Grzesik B., Kępa L., Puszcz-Matlińska M., Pudło R., Żurek A., Badura-Głąbik T. Estimation of the cognitive and affective disorders occurence in patients with Lyme borreliosis. Ann. Agric. Environ. Med. 2017; 24(1): 33–38, doi: 10.5604/12321966.1229002.
 
70.
Shotland L.I., Mastrioanni M.A., Choo D.L., Szymko-Bennett Y.M., Dally L.G., Pikus A.T., Sledjeski K., Marques A. Audiologic manifestations of patients with post-treatment Lyme disease syndrome. Ear Hear. 2003; 24(6): 508–517, doi: 10.1097/01.AUD.0000100205.25774.5F.
 
eISSN:1734-025X
Journals System - logo
Scroll to top