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The olfactory function is impaired in patients with idiopathic inflammatory myopathies

  • FRONTIERS IN AUTOIMMUNITY
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Abstract

The aim of our study was to analyze olfactory function in patients with idiopathic inflammatory myopathies (IIM). We performed a case–control study on 60 IIM patients (48 females and 12 males) and 60 healthy controls (HC) recruited by the best friend method, matched for age, sex and lifestyle. Olfactory function was analyzed by “Sniffin’ sticks test” and expressed through a score (TDI), indicating normosmia (TDI > 30), hyposmia (TDI 15–30) and anosmia (TDI < 15). Mood was investigated by Beck depression inventory (BDI) test. Statistic was performed using SPSS package. Mean ± SD TDI was significantly reduced in patients versus HC (26.8 ± 5.2 vs. 31.4 ± 3.5, p < 0.001). Anosmia was detected in two patients (3.3 %) and no HC, hyposmia in 41 patients and 14 HC (68.3 vs. 23.3 %, p < 0.0001) and normosmia in 17 patients and 48 HC (28.3 vs. 76.6 %, p < 0.0001). In the multivariate analysis carried out in the pool population of patients and HC, low TDI score was associated with age ≥50 years (p < 0.0001), disease status (p < 0.0001) and high BDI (p = 0.007). When adjusting for BDI, disease status was still associated with low TDI (p = 0.037). In IIM, TDI was lower in subjects aged ≥50 years (p = 0.008) and in patients who were taking corticosteroids (p < 0.0001). In the multivariate analysis carried out in IIM patients, low TDI was associated with age ≥50 years (p = 0.001) and prednisone intake (p < 0.0001). The olfactory function is impaired in IIM patients. An underlying immune-mediated mechanism is conceivable, yet a possible interference due to age, steroid intake and depression should be considered.

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References

  1. Perricone C, Shoenfeld N, Agmon-Levin N, de Carolis C, Perricone R, Shoenfeld Y. Smell and autoimmunity: a comprehensive review. Clin Rev Allergy Immunol. 2013;45:87–96.

    Article  CAS  PubMed  Google Scholar 

  2. Benkler M, Agmon-Levin N, Shoenfeld Y. Parkinson’s disease, autoimmunity, and olfaction. Int J Neurosci. 2009;119:2133–43.

    Article  PubMed  Google Scholar 

  3. Makowska I, Kloszewska I, Grabowska A, Szatkowska I, Rymarczyk K. Olfactory deficits in normal aging and Alzheimer’s disease in the polish elderly population. Arch Clin Neuropsychol. 2011;26:270–9.

    Article  PubMed  Google Scholar 

  4. Erb K, Bohner G, Harms L, Goektas O, Fleiner F, Dommes E, Schmidt FA, Dahlslett B, Lüdemann L. Olfactory function in patients with multiple sclerosis: a diffusion tensor imaging study. J Neurol Sci. 2012;316:56–60.

    Article  PubMed  Google Scholar 

  5. Shoenfeld N, Agmon-Levin N, Flitman-Katzevman I, Paran D, Katz BS, Kivity S, Langevitz P, Zandman-Goddard G, Shoenfeld Y. The sense of smell in systemic lupus erythematosus. Arthritis Rheum. 2009;60:1484–7.

    Article  PubMed  Google Scholar 

  6. Kamel UF, Maddison P, Whitaker R. Impact of primary Sjogren’s syndrome on smell and taste: effect on quality of life. Rheumatology (Oxford). 2009;48:1512–4.

    Article  Google Scholar 

  7. Katzav A, Solodeev I, Brodsky O, Chapman J, Pick CG, Blank M, et al. Induction of autoimmune depression in mice by anti-ribosomal P antibodies via the limbic system. Arthritis Rheum. 2007;56:938–48.

    Article  CAS  PubMed  Google Scholar 

  8. Shoenfeld Y. To smell autoimmunity: anti-P-ribosomal autoantibodies, depression, and the olfactory system. J Autoimmun. 2007;28:165–9.

    Article  CAS  PubMed  Google Scholar 

  9. Katzav A, Ben-Ziv T, Chapman J, Blank M, Reichlin M, Shoenfeld Y. Anti-P ribosomal antibodies induce defect in smell capability in a model of CNS –SLE (depression). J Autoimmun. 2008;31:393–8.

    Article  CAS  PubMed  Google Scholar 

  10. Katzav A, Ben-Ziv T, Blank M, Pick CG, Shoenfeld Y, Chapman J. Antibody-specific behavioral effects: intracerebroventricular injection of antiphospholipid antibodies induces hyperactive behaviour while anti-ribosomal-P antibodies induces depression and smell deficits in mice. J Neuroimmunol. 2014;272:10–5.

    Article  CAS  PubMed  Google Scholar 

  11. Matus S, Burgos PV, Bravo-Zehnder M, Kraft R, Porras OH, Farías P, et al. Antiribosomal-P autoantibodies from psychiatric lupus target a novel neuronal surface protein causing calcium influx and apoptosis. J Exp Med. 2007;204:3221–34.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  12. Fasunla JA, Hundt W, Lutz J, Förger F, Thürmel K, Steinbach S. Evaluation of smell and taste in patients with Wegener’s granulomatosis. Eur Arch Otorhinolaryngol. 2012;269:179–86.

    Article  PubMed  Google Scholar 

  13. Proft F, Steinbach S, Dechant C, Witt M, Reindl C, Schulz S, Vielhauer V, Hilge R, Laubender R, Manger K, Nüsslein H, Wendler J, Schuch F, Schulze-Koops H, Grunke M. Gustatory and olfactory function in patients with granulomatosis with polyangiitis (Wegener’s). Scand J Rheumatol. 2014;10:1–7.

    Google Scholar 

  14. Ghirardello A, Zampieri S, Tarricone E, Iaccarino L, Gorza L, Doria A. Cutting edge issues in polymyositis. Clin Rev Allergy Immunol. 2011;41:179–89.

    Article  CAS  PubMed  Google Scholar 

  15. Ghirardello A, Bassi N, Palma L, Borella E, Domeneghetti M, Punzi L, Doria A. Autoantibodies in polymyositis and dermatomyositis. Curr Rheumatol Rep. 2013;15:335.

    Article  PubMed  Google Scholar 

  16. Tarricone E, Ghirardello A, Rampudda M, Bassi N, Punzi L, Doria A. Anti-SAE antibodies in autoimmune myositis: identification by unlabelled protein immunoprecipitation in an Italian patient cohort. J Immunol Methods. 2012;384:128–34.

    Article  CAS  PubMed  Google Scholar 

  17. Zampieri S, Biral D, Adami N, Ghirardello A, Rampudda ME, Tonello M, Doria A. Expression of myositis specific autoantigens during post-natal myogenesis. Neurol Res. 2008;30:145–8.

    Article  CAS  PubMed  Google Scholar 

  18. Ghirardello A, Zampieri S, Iaccarino L, Tarricone E, Bendo R, Gambari PF, Doria A. Anti-Mi-2 antibodies. Autoimmunity. 2005;38:79–83.

    Article  CAS  PubMed  Google Scholar 

  19. Franceschini F, Cavazzana I, Generali D, Quinzanini M, Viardi L, Ghirardello A, Doria A, Cattaneo R. Anti-Ku antibodies in connective tissue diseases: clinical and serological evaluation of 14 patients. J Rheumatol. 2002;29:1393–7.

    PubMed  Google Scholar 

  20. Iaccarino L, Gatto M, Bettio S, Caso F, Rampudda M, Zen M, Ghirardello A, Punzi L, Doria A. Overlap connective tissue disease syndromes. Autoimmun Rev. 2013;12:363–73.

    Article  CAS  PubMed  Google Scholar 

  21. Lega JC, Fabien N, Reynaud Q, Durieu I, Durupt S, Dutertre M, Cordier JF, Cottin V. The clinical phenotype associated with myositis specific and associated autoantibodies: a meta-analysis revisiting the so called anti-synthetase syndrome. Autoimmun Rev. 2014;13:883–91.

    Article  CAS  PubMed  Google Scholar 

  22. Mahler M, Miller FW, Fritzler MJ. Idiopathic inflammatory myositis and anti-synthetase syndrome: a comprehensive review. Autoimmun Rev. 2014;13:367–71.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  23. Zampieri S, Ghirardello A, Iaccarino L, Tarricone E, Gambari PF, Doria A. Anti-Jo-1 antibodies. Autoimmunity. 2005;38:73–8.

    Article  CAS  PubMed  Google Scholar 

  24. Bohan A, Peter JB. Polymyositis and dermatomyositis (first of two parts). N Engl J Med. 1975;292:344–7.

    Article  CAS  PubMed  Google Scholar 

  25. Bohan A, Peter JB. Polymyositis and dermatomyositis (second of two parts). N Engl J Med. 1975;292:403–7.

    Article  CAS  PubMed  Google Scholar 

  26. Hummel T, Sekinger B, Wolf SR, Pauli E, Kobal G. “Sniffin’ sticks”: olfactory performance assessed by the combined testing of odor identification, odor discrimination and olfactory threshold. Chem Senses. 1997;22:39–52.

    Article  CAS  PubMed  Google Scholar 

  27. Rider LG, Werth VP, Huber AM, Alexanderson H, Rao AP, Ruperto N, et al. Measures of adult and juvenile dermatomypositis, polymyositis and inclusion body myositis. Arthritis Care Res. 2011;63:S118–57.

    Article  Google Scholar 

  28. Ghirardello A, Rampudda M, Ekholm L, Bassi N, Tarricone E, Zampieri S, Zen M, Vattemi GA, Lundberg IE, Doria A. Diagnostic performance and validation of autoantibody testing in myositis by a commercial line blot assay. Rheumatology (Oxford). 2010;49:2370–4.

    Article  CAS  Google Scholar 

  29. Beck AT, et al. Comparison of Beck Depression Inventories -IA and -II in psychiatric outpatients. J Pers Assess. 1996;67:588–97.

    Article  CAS  PubMed  Google Scholar 

  30. van Exel E, Jacobs J, Korswagen L-A, Voskuyl AE, Stek M, Dekker J, Bultink IEM. Depression in systemic lupus erythematosus, dependent on or independent of severity of disease. Lupus. 2013;22:1462–9.

    Article  PubMed  Google Scholar 

  31. Mombaerts P. Love at first smell—the 2004 Nobel Prize in Physiology or Medicine. N Engl J Med. 2004;351:2579–80.

    Article  CAS  PubMed  Google Scholar 

  32. Doherty PC. On the nose: shared themes for the sensory and immune self. Nat Immunol. 2003;4:1043–5.

    Article  CAS  PubMed  Google Scholar 

  33. Kivity S, Ortega-Hernandez OD, Shoenfeld Y. Olfaction—a window to the mind. Isr Med Assoc J. 2009;11:238–43.

    PubMed  Google Scholar 

  34. Ortega-Hernandez OD, Kivity S, Shoenfeld Y. Olfaction, psychiatric disorders and autoimmunity: is there a common genetic association? Autoimmunity. 2009;42:80–8.

    Article  CAS  PubMed  Google Scholar 

  35. Moscavitch SD, Szyper-Kravitz M, Shoenfeld Y. Autoimmune pathology accounts for common manifestations in a wide range of neuro-psychiatric disorders: the olfactory and immune system interrelationship. Clin Immunol. 2009;130:235–43.

    Article  CAS  PubMed  Google Scholar 

  36. Strous RD, Shoenfeld Y. To smell the immune system: olfaction, autoimmunity and brain involvement. Autoimmun Rev. 2006;6:54–60.

    Article  CAS  PubMed  Google Scholar 

  37. Nguyen AD, Shenton ME, Levitt JJ. Olfactory dysfunction in schizophrenia: a review of neuroanatomy and psychophysiological measurements. Harv Rev Psychiatry. 2010;18:279–92.

    Article  PubMed  Google Scholar 

  38. Silva AM, Santos E, Moreira I, Bettencourt A, Coutinho E, Gonçalves A, Pinto C, Montalban X, Cavaco S. Olfactory dysfunction in multiple sclerosis: association with secondary progression. Mult Scler. 2012;18:616–21.

    Article  PubMed  Google Scholar 

  39. Hummel T, Kobal G, Gudziol H, Macky-Sim A. Normative data for the “Sniffin’ Sticks” including test of odor identification, odor discrimination, and olfactory threshold: an upgrade based on a group of more than 3,000 subjects. Eur Arch Otorhinolaryngol. 2007;264:237–43.

    Article  CAS  PubMed  Google Scholar 

  40. Basta M, Dalakas MC. High-dose intravenous immunoglobulin exerts its beneficial effect in patients with dermatomyositis by blocking endomysial deposition of activated complement fragments. J Clin Invest. 1994;94:1729–35.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  41. Ingram G, Hacobyan S, Robertson NP, Morgan BP. Complement in multiple sclerosis: its role in disease and potential as a biomarker. Clin Exp Immunol. 2009;155:128–39.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  42. Perricone C, Agmon-Levin N, Shoenfeld N, de Carolis C, Guarino MD, Gigliucci G, Milana I, Novelli L, Valesini G, Perricone R, Shoenfeld Y. Evidence of impaired sense of smell in hereditary angioedema. Allergy. 2011;66:149–54.

    Article  CAS  PubMed  Google Scholar 

  43. Doty RL, Shah M, Bromley SM. Drug-induced taste disorders. Drug Saf. 2008;31:199–215.

    Article  CAS  PubMed  Google Scholar 

  44. Iaccarino L, Ghirardello A, Bettio S, Zen M, Gatto M, Punzi L, Doria A. The clinical features, diagnosis and classification of dermatomyositis. J Autoimmun. 2014;48–49:122–7.

    Article  PubMed  Google Scholar 

  45. Palagnini L, Mosca M, Tani C, Gemignani A, Mauri M, Bomabardieri S. Depression and systemic lupus erythematosus: a systematic review. Lupus. 2013;2:409–16.

    Article  Google Scholar 

  46. Souza FH, Levy-Neto M, Shinjo SK. Prevalence of clinical and laboratory manifestations and comorbidities in polymyositis according to gender. Rev Bras Reumatol. 2011;51:428–83.

    Article  PubMed  Google Scholar 

  47. Croy I, Symmank A, Schellong J, Hummel C, Gerber J, Joraschky P, Hummel T. Olfaction as a marker for depression in humans. J Affect Disord. 2014;160:80–6.

    Article  PubMed  Google Scholar 

  48. Naudin M, El-Hage W, Gomes M, Gaillard P, Belzung C, Atanasova B. State and trait olfactory markers of major depression. PLoS One. 2012;7:e46938.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  49. Pinto JM, Wroblewski KE, Kern DW, Schumm LP, McClintock MK. Olfactory dysfunction predicts 5-year mortality in older adults. PLoS One. 2014;9:e107541.

    Article  PubMed Central  PubMed  Google Scholar 

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Conflict of interest

The authors declare no conflicts of interest.

Ethical standard

This study was approved by the local ethics committee.

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All patients gave informed written consent.

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Authors and Affiliations

  1. Division of Rheumatology, Department of Medicine-DIMED, University of Padova, Via Giustiniani, 2, 35128, Padua, Italy

    L. Iaccarino, M. Rampudda, M. Zen, M. Gatto, A. Ghirardello, N. Bassi, L. Punzi & A. Doria

  2. Zabludowicz Center for Autoimmune Diseases, Sheba Medical Center, Tel-Aviv University, Tel-Hashomer, Israel

    N. Shoenfeld & Y. Shoenfeld

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  1. L. Iaccarino
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  2. N. Shoenfeld
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  6. A. Ghirardello
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Correspondence to A. Doria.

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Iaccarino, L., Shoenfeld, N., Rampudda, M. et al. The olfactory function is impaired in patients with idiopathic inflammatory myopathies. Immunol Res 60, 247–252 (2014). https://doi.org/10.1007/s12026-014-8581-5

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