Olfactory screening of Parkinson’s Disease patients and healthy subjects in China and Germany: A study of cross-cultural adaptation of the Sniffin’ Sticks 12-identification test

Autoři: Elmar H. Pinkhardt aff001;  Huijing Liu aff002;  Di Ma aff003;  Jing Chen aff003;  Adrian Pachollek aff001;  Martin S. Kunz aff001;  Jan Kassubek aff001;  Albert C. Ludolph aff001;  Yining Huang aff003;  Haibo Chen aff002;  G. Bernhard Landwehrmeyer aff001;  Zhaoxia Wang aff003;  Wen Su aff002
Působiště autorů: Ulm University, Department of Neurology, Ulm, Germany aff001;  Neurology Department, Beijing Hospital, National Center of Gerontology, China, Dong Dan, Beijing, China aff002;  Department of Neurology, Peking University First Hospital, Beijing, China aff003
Vyšlo v časopise: PLoS ONE 14(11)
Kategorie: Research Article
doi: 10.1371/journal.pone.0224331



Olfactory testing is a useful tool in the differential diagnosis of Parkinson’s Disease (PD). Although fast and easy to use, the high intercultural variability of odor detection limits the world-wide use of the most common test sets.


The aim of this study was to test one of the most commonly used olfactory tests (Sniffin’ Sticks 12-identification test) in an adapted version for a Chinese population of healthy subjects and PD patients.


For this purpose, cohorts of 39 Chinese and 41 German PD patients as well as 70 Chinese and 100 German healthy subjects have been examined both with the original and the adapted version of the Sniffin’ Sticks test, the latter being designed according to the regional culture.


The adapted Chinese version of the Sniffin’ Sticks 12 identification test proved to discriminate Chinese PD patients from controls with a high specificity but relatively low sensitivity. Yet not all odor exchanges would have been necessary as the original odors including liquorice and coffee showed an equally high identification rate in the Chinese and German cohorts.


The results showed that the newly adapted test could be used as a screening test for PD related olfactory dysfunction in a Chinese population. However further investigation will be necessary to optimize the selection of odors for the Chinese version of the test.

Klíčová slova:

Culture – German people – Germany – Chinese people – Odorants – Olfactory bulb – Parkinson disease – Patients


1. Berg D, Postuma RB. From Prodromal to Overt Parkinson’s Disease: Towards a New Definition in the Year 2040. Brundin P, Langston JW, Bloem BR, editors. J Parkinsons Dis. 2018;8: S19–S23. Available: https://www.medra.org/servlet/aliasResolver?alias=iospress&doi=10.3233/JPD-181457 30584153

2. Doty RL, Deems DA, Stellar S. Olfactory dysfunction in parkinsonism: a general deficit unrelated to neurologic signs, disease stage, or disease duration. Neurology. 1988;38: 1237–1244. Available: http://eutils.ncbi.nlm.nih.gov/entrez/eutils/elink.fcgi?dbfrom=pubmed&id=3399075&retmode=ref&cmd=prlinks 3399075

3. Ross GW, Petrovitch H, Abbott RD, Tanner CM, Popper J, Masaki K, et al. Association of olfactory dysfunction with risk for future Parkinson’s disease. Ann Neurol. 2008;63: 167–173. Available: http://doi.wiley.com/10.1002/ana.21291 18067173

4. Mahlknecht P, Iranzo A, Hogl B, Frauscher B, Muller C, Santamaria J, et al. Olfactory dysfunction predicts early transition to a Lewy body disease in idiopathic RBD. Neurology. 2015;84: 654–658. Available: http://www.neurology.org/cgi/doi/10.1212/WNL.0000000000001265 25609758

5. Doty RL. Olfactory dysfunction in neurodegenerative diseases: is there a common pathological substrate? Lancet Neurol. 2017;16: 478–488. Available: http://dx.doi.org/10.1016/S1474-4422(17)30123-0 28504111

6. Krismer F, Pinter B, Mueller C, Mahlknecht P, Nocker M, Reiter E, et al. Sniffing the diagnosis: Olfactory testing in neurodegenerative parkinsonism. Parkinsonism Relat Disord. 2017;35: 36–41. Available: http://dx.doi.org/10.1016/j.parkreldis.2016.11.010 27890451

7. Silveira-Moriyama L, Hughes G, Church A, Ayling H, Williams DR, Petrie A, et al. Hyposmia in progressive supranuclear palsy. Mov Disord. 2010;25: 570–577. Available: http://doi.wiley.com/10.1002/mds.22688 20209627

8. Silveira-Moriyama L, Holton JL, Kingsbury A, Ayling H, Petrie A, Sterlacci W, et al. Regional differences in the severity of Lewy body pathology across the olfactory cortex. Neurosci Lett. 2009;453: 77–80. Available: https://linkinghub.elsevier.com/retrieve/pii/S0304394009001761 19356597

9. Doty RL, Stern MB, Pfeiffer C, Gollomp SM, Hurtig HI. Bilateral olfactory dysfunction in early stage treated and untreated idiopathic Parkinson’s disease. J Neurol Neurosurg Psychiatry. 1992;55: 138–142. Available: http://eutils.ncbi.nlm.nih.gov/entrez/eutils/elink.fcgi?dbfrom=pubmed&id=1538221&retmode=ref&cmd=prlinks 1538221

10. Chou KL, Bohnen NI. Performance on an Alzheimer-selective odor identification test in patients with Parkinson’s disease and its relationship with cerebral dopamine transporter activity. Parkinsonism Relat Disord. 2009;15: 640–643. Available: https://linkinghub.elsevier.com/retrieve/pii/S1353802009000662 19329351

11. Majid A, Speed L, Croijmans I, Arshamian A. What Makes a Better Smeller? Perception. 2017;46: 406–430. Available: http://journals.sagepub.com/doi/10.1177/0301006616688224 28103755

12. Hoover KC. Global Survey of Variation in a Human Olfactory Receptor Gene Reveals Signatures of Non-Neutral Evolution. Chem Senses. 2015;40: 481–488. Available: https://academic.oup.com/chemse/article-lookup/doi/10.1093/chemse/bjv030 26072518

13. Hoover KC. Smell with inspiration: The evolutionary significance of olfaction. Am J Phys Anthropol. 2010;143: 63–74. Available: http://doi.wiley.com/10.1002/ajpa.21441 21086527

14. Fjaeldstad A, Kjaergaard T, Van Hartevelt TJ, Moeller A, Kringelbach ML, Ovesen T. Olfactory screening: validation of Sniffin’ Sticks in Denmark. Clin Otolaryngol. 2015;40: 545–550. Available: http://doi.wiley.com/10.1111/coa.12405 25721152

15. Kendirli MT. The applicability of the “Sniffin’ Sticks” olfactory test in a Turkish population. Med Sci Monit. 2013;19: 1221–1226. Available: http://www.medscimonit.com/abstract/index/idArt/889838 24382345

16. Neumann C, Tsioulos K, Merkonidis C, Salam M, Clark A, Philpott C. Validation study of the “Sniffin” Sticks" olfactory test in a British population: a preliminary communication”. Clin Otolaryngol. 2012;37: 23–27. Available: http://doi.wiley.com/10.1111/j.1749-4486.2012.02431.x 22433135

17. Hummel T, Kobal G, Gudziol H, Mackay-Sim A. Normative data for the “Sniffin’ Sticks” including tests of odor identification, odor discrimination, and olfactory thresholds: an upgrade based on a group of more than 3,000 subjects. Eur Arch Oto-Rhino-Laryngology. 2006;264: 237–243. Available: http://link.springer.com/10.1007/s00405-006-0173-0

18. Ribeiro JC, Simões J, Silva F, Silva ED, Hummel C, Hummel T, et al. Cultural Adaptation of the Portuguese Version of the “Sniffin’ Sticks” Smell Test: Reliability, Validity, and Normative Data. Matsunami H, editor. PLoS One. 2016;11: e0148937–12. Available: https://dx.plos.org/10.1371/journal.pone.0148937 26863023

19. Chen W, Chen S, Kang W-Y, Li B, Xu Z-M, Xiao Q, et al. Application of odor identification test in Parkinson’s disease in China: A matched case-control study. J Neurol Sci. 2012;316: 47–50. Available: http://dx.doi.org/10.1016/j.jns.2012.01.033 22364958

20. Chen W, Tan Y-Y, Hu Y-Y, Zhan W-W, Wu L, Lou Y, et al. Combination of olfactory test and substantia nigra transcranial sonopraphy in the differential diagnosis of Parkinson’s disease: a pilot study from China. Alzheimers Res Ther. 2012;1: 1. Available: Alzheimer’s Research & Therapy

21. Shu C-H, Yuan B-C. Assessment of odor identification function in Asia using a modified “Sniffin’ Stick” odor identification test. Eur Arch Oto-Rhino-Laryngology. 2007;265: 787–790. Available: http://link.springer.com/10.1007/s00405-007-0551-2

22. Feng G, Zhuang Y, Yao F, Ye Y, Wan Q, Zhou W. Development of the Chinese Smell Identification Test. Chem Senses. 2019;44: 189–195. doi: 10.1093/chemse/bjz006 30715263

23. Postuma RB, Berg D, Adler CH, Bloem BR, Chan P, Deuschl G, et al. The new definition and diagnostic criteria of Parkinson’s disease. Lancet Neurol. 2016;15: 546–548. Available: http://dx.doi.org/10.1016/S1474-4422(16)00116-2 27302120

24. 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. Available: http://eutils.ncbi.nlm.nih.gov/entrez/eutils/elink.fcgi?dbfrom=pubmed&id=9056084&retmode=ref&cmd=prlinks 9056084

25. Antsov E, Silveira-Moriyama L, Kilk S, Kadastik-Eerme L, Toomsoo T, Lees A, et al. Adapting the Sniffin’ Sticks olfactory test to diagnose Parkinson’s disease in Estonia. Parkinsonism Relat Disord. 2014;20: 1–4. Available: http://linkinghub.elsevier.com/retrieve/pii/S1353802014001539

26. Krismer F, Pinter B, Mueller C, Mahlknecht P, Nocker M, Reiter E, et al. Sniffing the diagnosis: Olfactory testing in neurodegenerative parkinsonism. Park Relat Disord. 2017;35: 36–41. doi: 10.1016/j.parkreldis.2016.11.010 27890451

27. Nielsen T, Jensen MB, Stenager E, Andersen AD. The use of olfactory testing when diagnosing Parkinson’s disease—a systematic review. Dan Med J. 2018;65. Available: http://eutils.ncbi.nlm.nih.gov/entrez/eutils/elink.fcgi?dbfrom=pubmed&id=29726318&retmode=ref&cmd=prlinks

28. Huang Si-Fei C K W J-J L F-T Z J L W G S-S W Y-X W Y L S-S S Y-M D Z-T Y H W J. Odor Identification Test in Idiopathic REM- Behavior Disorder and Parkinson’s Disease in China. Ferri R, editor. PLoS One. 2016;11: 1–13. Available: http://dx.plos.org/10.1371/journal.pone.0160199

29. Benavent MS. Diagnostic value of combined assessment of olfaction and substantia nigra hyperechogenicity for Parkinson’s disease. Neurologia. 2015;30: 496–501. doi: 10.1016/j.nrl.2014.03.010 24839905

30. Rumiati RI, Foroni F. We are what we eat: How food is represented in our mind/brain. Psychon Bull Rev. 2016;23: 1–12. Available: http://dx.doi.org/10.3758/s13423-015-0908-2

Článek vyšel v časopise


2019 Číslo 11