Abstract
Introduction
Several studies evaluated the influence of cultural components on the Sniffin’ Sticks Identification Test in different countries. The aim of this study was to analyze the olfactory function in a large sample of healthy subjects living in Sardinia, an island known for its historic genetic isolation, in relation to different age ranges to provide new data in healthy Sardinian subjects.
Methods
Olfactory perception of 161 participants (108 females and 53 males; age range 19–78 years) was assessed through three different parameters: odor detection threshold, discrimination, and identification by means of the Sniffin’Sticks Extended test (SST).
Results
Our results show that young adults were generally normosmic, while in subjects over 55, a statistically significant age-related decrease of all the parameters was observed. Regarding odor identification task, a few, such as leather, apples, lemons, cloves, and pineapples, were frequently incorrectly identified by participants probably due to the similarities between the odors and distractors.
Conclusion and Implications
Our data provide a comprehensive evaluation of the three olfactory components in the Sardinian population and confirm a decrease in the odor detection threshold, discrimination and identification as well as in the global TDI score in subjects over 55 years of age. These results may be useful in providing normative values for routine clinical use of the SSET in Sardinian subjects.
Similar content being viewed by others
References
Anderson AK, Christoff K, Stappen I, Panitz D, Ghahremani DG, Glover G, Gabrieli JD, Sobel N (2003) Dissociated neural representations of intensity and valence in human olfaction. Nat Neurosci 6:196–202
Atanasova B, Graux J, El Hage W, Hommet C, Camus V, Belzung C (2008) Olfaction: a potential cognitive marker of psychiatric disorders. Neurosci Biobehav Rev 32:1315–1325
Barresi M, Ciurleo R, Giacoppo S, Cuzzola VF (2012) Evaluation of olfactory dysfunction in neurodegenerative diseases. J Neurol Sci 323:16–24
Berendse HW, Ponsen MM (2009) Diagnosing premotor Parkinson’s disease using a two-step approach combining olfactory testing and DAT SPECT imaging. Parkinsonism Relat Disord 15(S3):S26–S30
Cătană I, Negoias S, Maniu A, Porojan M, Cosgarea M (2012) A modified version of “Sniffin’ sticks” odor identification test: the Romanian cultural adaptation. Otorinolaringologie 85:218–223
Cavazzana A, Wesarg C, Schriever VA, Hummel T, Lundström JN, Parma V (2016) Cross-cultural adaptation of the Sniffin’ Sticks Olfactory Identification Test for US children. Chem Senses 00:1–8
Cecchini MP, Viviani D, Sandri M, Hähner A, Hummel T, Zancanaro C (2016) Olfaction in people with Down syndrome: a comprehensive assessment across four decades of age. PLoS One 11(1):e0146486
Cenedese V, Mezzavilla M, Morgan A, Marino R, Ettorre CP, Margaglione M, Gasparini P, Menini A (2015) Assessment of the olfactory function in Italian patients with type 3 von Willebrand disease caused by a homozygous 253 kb deletion involving VWF and TMEM16B/ANO2. PLoS One 10(1):e0116483
Conti S, Bonazzi S, Laiacona M, Masina M, Vanelli CM (2015) Montreal cognitive assessment (MoCA)-Italian version: regression based norms and equivalent scores. Neurol Sci 36:209–214
Croy I, Nordin S, Hummel T (2014) Olfactory disorders and quality of life—an updated review. Chem Senses 39:185–194
Denzer-Lippmann MY, Beauchamp J, Freiherr J, Thuerauf N, Kornhuber J, Buettner A (2016) Development and validation of a food-associated olfactory test (FAOT). Chem Senses 42(1):47–57
Devanand DP, Michaels-Marston KS, Liu X, Pelton G, Padilla M, Marder K, Bell K, Stern Mayeux R (2000) Olfactory deficits in patients with mild cognitive impairment predict Alzheimer’s disease at follow-up. Am J Psychiatry 157:1399–1405
Doty RL (2009) The olfactory system and its disorders. Semin Neurol 29(1):74–81
Doty RL, Kamath V (2014) The influence of age on olfaction: a review. Front Phycol 5(20):1–20
Doty RL, Shaman P, Dann M (1984) Development of the University of Pennsylvania Smell Identification Test: a standardized microencapsulated test of olfactory function. Physiol Behav 32:489–502
Doty RL, Deems DA, Stellar S (1988) Olfactory dysfunction in parkinsonism: general deficit unrelated to neurologic signs, disease stage, or disease duration. Neurology 38:1237–1244
Doty RL, Marcus A, Lee WW (1996) Development of the 12-item cross-cultural smell identification test (CC-SIT). Laryngoscope 106:353–356
Eibenstein A, Fioretti AB, Lena C, Rosati N, Ottaviano I, Fusetti M (2005) Olfactory screening test: experience in 102 Italian subjects. Acta Otorhinolaryngol Ital 25:18–22
Fagundo AB, Jiménez-Murcia S, Giner-Bartolomé C, Islam MA, de la Torre R, Pastor A, Casanueva FF, Crujeiras AB, Granero R, Baños R, Botella C, Fernández-Real JM, Frühbeck G, Gómez-Ambrosi J, Menchón JM, Tinahones FJ, Fernández-Aranda F (2015) Modulation of higher-order olfaction components on executive functions in humans. PLoS One 10(6):e0130319
Fjaeldstad A, Kjaergaard T, Van Hartevelt TJ, Moeller A, Kringelbach ML, Ovesen T (2015) Olfactory screening: validation of Sniffin’ Sticks in Denmark. Clin Otolaryngol 40:545–550
Francalacci P, Morelli L, Angius A, Berutti R, Reiner F, Atzeni R, Pilu R, Busonero F, Maschio A, Zara I, Sanna D, Useli A, Urru MF, Marceli M, Cusano F, Oppo M, Zoledziewska M, Pitzalis M, Deidda F, Porcu E, Poddie F, Kang HM, Lyons R et al (2013) Low-pass DNA sequencing of 1200 Sardinians reconstructs European Y-chromosome phylogeny. Science 341(6145):565–569
Francalacci P, Sanna D, Useli A, Berutti R, Barbato M, Whalen MB, Angius A, Sidore C, Alonso S, Tofanelli S, Cucca F (2015) Detection of phylogenetically informative polymorphisms in the entire euchromatic portion of human Y chromosome from a Sardinian sample. BMC Res Notes 8:174–187
Godoy MDCL, Voegels RL, Pinna FR, Imamura R, Farfel JM (2015) Olfaction in neurologic and neurodegenerative diseases: a literature review. Int Arch Otorhinolaryngol 19:176–179
Gottfried JA (2010) Central mechanisms of odour object perception. Nat Rev Neurosci 11(9):628–641
Gottfried JA, Zald DH (2005) On the scent of human olfactory orbitofrontal cortex: metaanalysis and comparison to non-human primates. Brain Res Rev 50:287–304
Guarneros M, Hudson R, López-Palacios M, Drucker-Colín R (2015) Reference values of olfactory function for Mexico City inhabitants. Arch Med Res 46:84–90
Gudziol V, Hummel T (2009) The influence of distractors on odor identification. Arch Otolaryngol Head Neck Surg 135:143–145
Haener A, Mayer AM, Landis BN, Pournaras I, Lill K, Gudziol V, Hummel T (2009) High test–retest reliability of the extended version of the “Sniffin’ Sticks” test. Chem Senses 34:705–711
Haener A, Hummel T, Reichmann H (2014) A clinical approach towards smell loss in Parkinson's disease. J Parkinsons Dis 4:189–195
Hoskison EE (2013) Olfaction, pheromones and life. J Laryngol Otol 127:1156–1159
Hummel T, Sekinger B, Wolf SR, Pauli E, Kobal G (1997) ‘Sniffin’ Sticks’: olfactory performance assessed by the combined testing of odour identification, odour discrimination and olfactory threshold. Chem Senses 22:39–52
Hummel T, Kobal G, Gudziol H, Mackay-Sim A (2007) Normative data for the “Sniffin’ Sticks” including tests of odour identification, odour discrimination, and olfactory thresholds: an upgrade based on a group of more than 3,000 subjects. Eur Arch Otorhinolaryngol 264:237–243
Hummel T, Whitcroft KL, Andrews P, Altundag A, Cinghi C, Costanzo RM, Damm M, Frasnelli J, Gudziol H, Gupta N, Haener A, Holbrook E, Konstantinidis I, Landis BN, Leopold DA, Macchi A, Miwa T, Moesges R, Mullol J, Mueller CA et al (2017) Position paper on olfactory dysfunction. Rhinology 54(26). https://doi.org/10.4193/Rhin16.248
Iaccarino L, Shoenfeld N, Rampudda M, Zen M, Gatto M, Ghirardello A, Bassi N, Punzi L, Shoenfeld Y, Doria A (2014) The olfactory function is impaired in patients with idiopathic inflammatory myopathies. Immunol Res 60:247–252
Kalmey JK, Thewissen JG, Dluzen DE (1998) Age-related size reduction of foramina in the cribriform plate. Anat Rec 251(3):326–329
Kareken DA, Mosnik DM, Doty RL, Dzemidzic M, Hutchins GD (2003) Functional anatomy of human odor sensation, discrimination, and identification in health and aging. Neuropsychology 17:482–495
Kobal G, Hummel C (1988) Cerebral chemosensory evoked potentials elicited by chemical stimulation of the human olfactory and respiratory nasal mucosa. Electroencephalogr Clin Neurophysiol 71:241–250
Kobal G, Klimek L, Wolfensberger M, Gudziol H, Temmel A, Owen CM, Seeber H, Pauli E, Hummel T (2000) Multicenter investigation of 1,036 subjects using a standardized method for the assessment of olfactory function combining tests of odor identification, odor discrimination, and olfactory thresholds. Eur Arch Otorhinolaryngol 257:205–211
Konstantinidis I, Printza A, Genetzaki S, Mamali K, Kekes G, Constantinidis J (2008) Cultural adaptation of an olfactory identification test: the Greek version of Sniffin’ Sticks. Rhinology 46:292–296
Kumazaki H, Muramatsu T, Fujisawa TX, Miyao M, Matsuura E, Okada K, Kasaoka H, Tomoda A, Mimura M (2016) Assessment of olfactory detection thresholds in children with autism spectrum disorders using a pulse ejection system. Mol Autism 7(6). https://doi.org/10.1186/s13229-016-0071-2
Lin S-H, Chu S-T, Yuan B-C, Shu C-H (2009) Survey of the frequency of olfactory dysfunction in Taiwan. J Chin Med Assoc 72(2):68–71
Mackay-Sim M, Grant G, Owen C, Chan D, Silburn P (2004) Australian norms for a quantitative olfactory function test. J Clin Neurosci 8:874–879
Maremmani C, Rossi G, Tambasco N, Fattori B, Pierroni A, Ramat S, Napolitano A, Vanni P, Serra P, Piersanti P, Zanetti M, Coltelli M, Orsini M, Marconi R, Purcaro C, Calabresi A, Meco G (2012) The validity and reliability of the Italian olfactory identification test (IOIT) in healthy subjects and in Parkinson’s disease patients. Parkinsonism Relat Disord 18:788–793
Mazzatenta A, Cellerino A, Origlia N, Barloscio D, Sartucci F, Di Giulio C, Dominici L (2016) Olfactory phenotypic expression unveils human aging. Oncotarget 7(15):19193–19199
Mesholam RI, Moberg PJ, Mahr RN, Doty RL (1998) Olfaction in neurodegenerative disease. A meta-analysis of olfactory functioning in Alzheimer’s and Parkinson’s diseases. Arch Neurol 55:84–90
Nasreddine ZS, Phillips NA, Bédirian V, Charbonneau S, Whitehead V, Collin I, Cummings JL, Chertkow H (2005) The Montreal cognitive assessment, MoCA: a brief screening tool for mild cognitive impairment. J Am Geriatr Soc 53(4):695–699
Neumann C, Tsioulos K, Merkonidis C, Salam M, Clark A, Philpott C (2012) Validation study of the “Sniffin’ Sticks” olfactory test in a British population: a preliminary communication. Clin Otolaryngol 37:23–27
Oleszkiewicz A, Taut M, Sorokowska A, Radwan A, Kamel R, Hummel T (2016) Development of the Arabic version of the “Sniffin’ Sticks” odor identification test. Eur Arch Otrhinolaryngol 273:1179–1184
Olivieri A, Sidore C, Achili A, Angius A, Posth C, Furtwängler A, Brandini S, Capodiferro MR, Gandini F, Zoledziewska M, Pitzalis M, Maschio A, Busonero F, Lai L, Skeates R, Gradoli MG, Becket J, Marongiu M, Mazzarello V et al (2017) Mitogenome diversity in Sardinians: a genetic window onto an Island’s past. Mol Biol Evol 34(5):1230–1239
Orhan KS, Karabulut B, Keles N, Değer K (2012) Evaluation of factors concerning the olfaction using the Sniffin’ Sticks test. Otolaryngol Head Neck Surg 146(2):240–246
Ottaviano G, Frasson G, Nardello E, Martini A (2016) Olfaction deterioration in cognitive disorders in the elderly. Aging Clin Exp Res 28:37–45
Parola S, Liberini P (1999) Assessing olfaction in the Italian population: methodology and clinical application. Ital J Neurol Sci 20:287–296
Picillo M, Pellecchia MT, Erro R, Amboni M, Vitale C, Iavarone A, Moccia M, Allocca R, Orefice G, Barone P (2014) The use of University of Pennsylvania Smell Identification Test in the diagnosis of Parkinson’s disease in Italy. Neurol Sci 35:379–383
Pinto JM, Wroblewski KE, Kern DW, Schumm LP, McClintock MK (2015) The rate of age-related olfactory decline among the general population of older U.S. adults. J Gerontol A Biol Sci Med Sci 70:1435–1441
Rombaux P, Duprez T, Hummel T (2009) Olfactory bulb volume in the clinical assessment of olfactory dysfunction. Rhinology 47(1):3–9
Rumeau C, Nguyen DT, Jankowski R (2015) How to assess olfactory performance with the Sniffin’ sticks test. Eur Ann Otorhinolaryngol Head Neck Dis 133(3):203–206
Small DM, Voss J, Mak YE, Simmons KB, Parrish T, Gitelman D (2004) Experience-dependent neural integration of taste and smell in the human brain. J Neurophysiol 92:1892–1903
Sorokowska A, Sorokowski P, Frackowiak T (2015) Determinants of human olfactory performance: a cross-cultural study. Sci Total Environ 506-507:196–200
Tekeli H, Altundağ A, Salihoğlu M, Cayönü M, Kendirli MT (2013) The applicability of the “Sniffin’ Sticks” olfactory test in Turkish population. Med Sci Monit 19:1221–1226
Wolfensberger M, Schnieper I, Welge-Lüssen A (2000) Sniffin’ Sticks: a new olfactory test battery. Acta Otolaryngol 120:303–306
Yuan BC, Lee PL, Lee YL, Lin SH, Shu CH (2010) Investigation of the Sniffin’ Sticks olfactory test in Taiwan and comparison with different continents. J Chin Med Assoc 73(9):483–486
Acknowledgements
The authors thank all the participants for their availability and Dr. David Nilson for improving the English text. This work was supported by a grant from the University of Cagliari (Progetti di Ricerca di Interesse Dipartimentale, PRID 2016).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of Interest
The authors declare the they have no conflicts of interest.
Ethical Approval
This study was approved by the local Ethics Committee and was performed according to the Declaration of Helsinki (2008).
Informed Consent
Participants received an explanatory statement and gave their written informed consent to participate in the study.
Rights and permissions
About this article
Cite this article
Masala, C., Saba, L., Cecchini, M.P. et al. Olfactory Function and Age: a Sniffin’ Sticks Extended Test Study Performed in Sardinia. Chem. Percept. 11, 19–26 (2018). https://doi.org/10.1007/s12078-017-9233-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12078-017-9233-7