Humans without a sense of smell breathe differently.
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
22 Oct 2024
22 Oct 2024
Historique:
received:
10
07
2023
accepted:
18
09
2024
medline:
23
10
2024
pubmed:
23
10
2024
entrez:
22
10
2024
Statut:
epublish
Résumé
Olfaction may play a restricted role in human behavior, yet paradoxically, its absence in anosmia is associated with diverse deleterious outcomes, culminating in reduced life expectancy. The mammalian nose serves two purposes: olfaction and breathing. Because respiratory patterns are impacted by odors, we hypothesized that nasal respiratory airflow may be altered in anosmia. We apply a wearable device that precisely logs nasal airflow for 24-hour-long sessions in participants with isolated congenital anosmia and controls. We observe significantly altered patterns of respiratory nasal airflow in anosmia in wake and in sleep. These differences allow classification of anosmia at 83% accuracy using the respiratory trace alone. Patterns of respiratory airflow have pronounced impact on health, emotion and cognition. We therefore suggest that a portion of the deleterious outcomes associated with anosmia may be attributed to altered patterns of respiratory nasal airflow rather than a direct result of lost odor perception per se.
Identifiants
pubmed: 39438441
doi: 10.1038/s41467-024-52650-6
pii: 10.1038/s41467-024-52650-6
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
8809Subventions
Organisme : Israel Science Foundation (ISF)
ID : 2751/23
Organisme : Minerva Foundation (Minerva Stiftung)
ID : 714146
Informations de copyright
© 2024. The Author(s).
Références
Haggbloom, S. J. et al. The 100 most eminent psychologists of the 20th century. Rev. Gen. Psychol. 6, 139–152 (2002).
doi: 10.1037/1089-2680.6.2.139
Harrington, A. & Rosario, V. in Science of Olfaction (eds Serby, M. J. & Chobor, K. L.) 3–27 (Springer, New York, 1992).
Kalogerakis, M. G. The role of olfaction in sexual development. Psychosom. Med. 25, 420–432 (1963).
pubmed: 14050424
doi: 10.1097/00006842-196309000-00002
McCann Worldgroup. The Truth About Youth. https://idoc.pub/queue/mccannworldgroup-truth-about-youth-vylyzxw81d4m (2011).
Hoffman, H. J., Ishii, E. K. & Macturk, R. H. Age‐related changes in the prevalence of smell/taste problems among the United States adult population: results of the 1994 Disability Supplement to the National Health Interview Survey (NHIS). Ann. N. Y. Acad. Sci. 855, 716–722 (1998).
Nordin, S., Brämerson, A. & Bende, M. Prevalence of self-reported poor odor detection sensitivity: the Skövde population-based study. Acta Oto-laryngol. 124, 1171–1173 (2004).
doi: 10.1080/00016480410017468
Landis, B. N., Konnerth, C. G. & Hummel, T. A study on the frequency of olfactory dysfunction. Laryngoscope 114, 1764–1769 (2004).
pubmed: 15454769
doi: 10.1097/00005537-200410000-00017
Murphy, C. et al. Prevalence of olfactory impairment in older adults. JAMA 288, 2307–2312 (2002).
pubmed: 12425708
doi: 10.1001/jama.288.18.2307
Doty, R. L. Olfactory dysfunction in neurodegenerative diseases: is there a common pathological substrate? Lancet Neurol. 16, 478–488 (2017).
pubmed: 28504111
doi: 10.1016/S1474-4422(17)30123-0
Han, A. Y., Mukdad, L., Long, J. L. & Lopez, I. A. Anosmia in COVID-19: mechanisms and significance. Chem. Senses 45, 423–428 (2020).
doi: 10.1093/chemse/bjaa040
Croy, I., Nordin, S. & Hummel, T. Olfactory disorders and quality of life—an updated review. Chem. Senses 39, 185–194 (2014).
pubmed: 24429163
doi: 10.1093/chemse/bjt072
Nordin, S. & Brämerson, A. Complaints of olfactory disorders: epidemiology, assessment and clinical implications. Curr. Opin. Allergy Clin. Immunol. 8, 10–15 (2008).
pubmed: 18188011
doi: 10.1097/ACI.0b013e3282f3f473
Croy, I., Negoias, S., Novakova, L., Landis, B. N. & Hummel, T. Learning about the functions of the olfactory system from people without a sense of smell. PLoS ONE 7, e33365 (2012).
pubmed: 22457756
pmcid: 3310072
doi: 10.1371/journal.pone.0033365
Karstensen, H. & Tommerup, N. Isolated and syndromic forms of congenital anosmia. Clin. Genet. 81, 210–215 (2012).
pubmed: 21895637
doi: 10.1111/j.1399-0004.2011.01776.x
Kamarck, M. L. et al. Identifying candidate genes underlying isolated congenital anosmia. Clin. Genet. 105, 376–385 (2024).
pubmed: 38148624
doi: 10.1111/cge.14470
Ghadami, M. et al. Isolated congenital anosmia with morphologically normal olfactory bulb in two Iranian families: a new clinical entity? Am. J. Med. Genet. Part A 127, 307–309 (2004).
doi: 10.1002/ajmg.a.30025
Manan, H. A., Yahya, N., Han, P. & Hummel, T. A systematic review of olfactory-related brain structural changes in patients with congenital or acquired anosmia. Brain Struct. Funct. 1–26 (2022).
Keller, A. & Malaspina, D. Hidden consequences of olfactory dysfunction: a patient report series. BMC Ear Nose Throat Disord. 13, 1–20 (2013).
doi: 10.1186/1472-6815-13-8
Patel, Z. M. et al. International consensus statement on allergy and rhinology: Olfaction. Int. Forum Allergy Rhinol. 12, 327–680 (2022) (Wiley Online Library).
Whitcroft, K. et al. Position paper on olfactory dysfunction: 2023. Rhinology 61, 1–108 (2023).
Kohli, P., Soler, Z. M., Nguyen, S. A., Muus, J. S. & Schlosser, R. J. The association between olfaction and depression: a systematic review. Chem. Senses 41, 479–486 (2016).
pubmed: 27170667
pmcid: 4918728
doi: 10.1093/chemse/bjw061
Toller, S. V. Assessing the impact of anosmia: review of a questionnaire’s findings. Chem. Senses 24, 705–712 (1999).
pubmed: 10587505
doi: 10.1093/chemse/24.6.705
Yom-Tov, E., Lekkas, D. & Jacobson, N. C. Association of COVID19-induced anosmia and ageusia with depression and suicidal ideation. J. Affect. Disord. Rep. 5, 100156 (2021).
pubmed: 34075369
pmcid: 8154197
doi: 10.1016/j.jadr.2021.100156
Aschenbrenner, K. et al. The influence of olfactory loss on dietary behaviors. Laryngoscope 118, 135–144 (2008).
pubmed: 17975508
doi: 10.1097/MLG.0b013e318155a4b9
Blomkvist, A. & Hofer, M. Olfactory impairment and close social relationships. A narrative review. Chem. Senses 46, bjab037 (2021).
pubmed: 34351415
pmcid: 8385889
doi: 10.1093/chemse/bjab037
Santos, D. V., Reiter, E. R., DiNardo, L. J. & Costanzo, R. M. Hazardous events associated with impaired olfactory function. Arch. Otolaryngol.–Head Neck Surg. 130, 317–319 (2004).
pubmed: 15023839
doi: 10.1001/archotol.130.3.317
Pinto, J. M., Wroblewski, K. E., Kern, D. W., Schumm, L. P. & McClintock, M. K. Olfactory dysfunction predicts 5-year mortality in older adults. PLoS ONE 9, e107541 (2014).
pubmed: 25271633
pmcid: 4182669
doi: 10.1371/journal.pone.0107541
McGann, J. P. Poor human olfaction is a 19th-century myth. Science 356, eaam7263 (2017).
pubmed: 28495701
pmcid: 5512720
doi: 10.1126/science.aam7263
Stevenson, R. J. An initial evaluation of the functions of human olfaction. Chem. Senses 35, 3–20 (2010).
pubmed: 19942579
doi: 10.1093/chemse/bjp083
Chen, D. & Haviland-Jones, J. Human olfactory communication of emotion. Percept. Mot. Skills 91, 771–781 (2000).
pubmed: 11153847
doi: 10.2466/pms.2000.91.3.771
Yeshurun, Y. & Sobel, N. An odor is not worth a thousand words: from multidimensional odors to unidimensional odor objects. Annu. Rev. Psychol. 61, 219–241 (2010).
pubmed: 19958179
doi: 10.1146/annurev.psych.60.110707.163639
Dikeçligil, G. N. & Gottfried, J. A. What does the human olfactory system do, and how does it do it? Annu. Rev. Psychol. 75, 155–181 (2024).
pubmed: 37788573
doi: 10.1146/annurev-psych-042023-101155
Mainland, J. & Sobel, N. The sniff is part of the olfactory percept. Chem. Senses 31, 181–196 (2006).
pubmed: 16339268
doi: 10.1093/chemse/bjj012
Arzi, A. et al. Humans can learn new information during sleep. Nat. Neurosci. 15, 1460–1465 (2012).
pubmed: 22922782
doi: 10.1038/nn.3193
Arzi, A., Rozenkrantz, L., Holtzman, Y., Secundo, L. & Sobel, N. Sniffing patterns uncover implicit memory for undetected odors. Curr. Biol. 24, R263–R264 (2014).
pubmed: 24698370
doi: 10.1016/j.cub.2014.02.004
Arzi, A. et al. Olfactory sniffing signals consciousness in unresponsive patients with brain injuries. Nature 581, 428–433 (2020).
pubmed: 32461641
doi: 10.1038/s41586-020-2245-5
Walker, J. C. et al. Human responses to propionic acid. II. Quantification of breathing responses and their relationship to perception. Chem. Senses 26, 351–358 (2001).
pubmed: 11369670
doi: 10.1093/chemse/26.4.351
Danuser, B., Moser, D., Vitale-Sethre, T., Hirsig, R. & Krueger, H. Performance in a complex task and breathing under odor exposure. Hum. Factors 45, 549–562 (2003).
pubmed: 15055453
doi: 10.1518/hfes.45.4.549.27093
Kahana-Zweig, R. et al. Measuring and characterizing the human nasal cycle. PLoS ONE 11, e0162918 (2016).
pubmed: 27711189
pmcid: 5053491
doi: 10.1371/journal.pone.0162918
Noto, T., Zhou, G., Schuele, S., Templer, J. & Zelano, C. Automated analysis of breathing waveforms using BreathMetrics: a respiratory signal processing toolbox. Chem. Senses 43, 583–597 (2018).
pubmed: 29985980
pmcid: 6150778
doi: 10.1093/chemse/bjy045
Del Negro, C. A., Funk, G. D. & Feldman, J. L. Breathing matters. Nat. Rev. Neurosci. 19, 351–367 (2018).
pubmed: 29740175
pmcid: 6636643
doi: 10.1038/s41583-018-0003-6
Herrero, J. L., Khuvis, S., Yeagle, E., Cerf, M. & Mehta, A. D. Breathing above the brain stem: volitional control and attentional modulation in humans. J. Neurophysiol. 119, 145–159 (2018).
Kluger, D. S., Balestrieri, E., Busch, N. A. & Gross, J. Respiration aligns perception with neural excitability. elife 10, e70907 (2021).
pubmed: 34904567
pmcid: 8763394
doi: 10.7554/eLife.70907
Sobel, N. et al. Sniffing and smelling: separate subsystems in the human olfactory cortex. Nature 392, 282–286 (1998).
pubmed: 9521322
doi: 10.1038/32654
Park, M., Chung, J., Kim, J. K., Jeong, Y. & Moon, W.-J. Altered functional brain networks in patients with traumatic anosmia: resting-state functional MRI based on graph theoretical analysis. Korean J. Radiol. 20, 1536–1545 (2019).
pubmed: 31606958
pmcid: 6791817
doi: 10.3348/kjr.2019.0104
Esposito, F. et al. Olfactory loss and brain connectivity after COVID‐19. Hum. Brain Mapp. 43, 1548–1560 (2022).
pubmed: 35083823
pmcid: 8886650
doi: 10.1002/hbm.25741
Peter, M. G. et al. Normal olfactory functional connectivity despite lifelong absence of olfactory experiences. Cereb. Cortex 31, 159–168 (2021).
pubmed: 32810869
doi: 10.1093/cercor/bhaa217
Ashhad, S., Kam, K., Del Negro, C. A. & Feldman, J. L. Breathing rhythm and pattern and their influence on emotion. Annu. Rev. Neurosci. 45, 223–247 (2022).
pubmed: 35259917
pmcid: 9840384
doi: 10.1146/annurev-neuro-090121-014424
Arshamian, A., Iravani, B., Majid, A. & Lundström, J. N. Respiration modulates olfactory memory consolidation in humans. J. Neurosci. 38, 3360–3317 (2018).
doi: 10.1523/JNEUROSCI.3360-17.2018
Zelano, C. et al. Nasal respiration entrains human limbic oscillations and modulates cognitive function. J. Neurosci. 36, 12448–12467 (2016).
pubmed: 27927961
pmcid: 5148230
doi: 10.1523/JNEUROSCI.2586-16.2016
Bensafi, M. et al. Olfactomotor activity during imagery mimics that during perception. Nat. Neurosci. 6, 1142 (2003).
pubmed: 14566343
doi: 10.1038/nn1145
Park, H.-D. et al. Breathing is coupled with voluntary initiation of mental imagery. NeuroImage 264, 119685 (2022).
pubmed: 36252914
doi: 10.1016/j.neuroimage.2022.119685
Perl, O. et al. Human non-olfactory cognition phase-locked with inhalation. Nat. Hum. Behav. 3, 501 (2019).
pubmed: 31089297
doi: 10.1038/s41562-019-0556-z
Berry, R. B. The AASM Manual for the Scoring of Sleep and Associated Events: Rules, Terminology and Technical Specifications. Version 2.1 (American Academy of Sleep Medicine, Darien, IL, 2014).
Mady, L. J. et al. Exploring olfactory dysfunction as a marker of frailty and postoperative outcomes in head and neck cancer. JAMA Otolaryngol.–Head Neck Surg. 149, 828–836 (2023).
pubmed: 37498617
pmcid: 10375382
doi: 10.1001/jamaoto.2023.1935
Faul, F., Erdfelder, E., Lang, A.-G. & Buchner, A. G.* Power 3: a flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behav. Res. Methods 39, 175–191 (2007).
pubmed: 17695343
doi: 10.3758/BF03193146
Cohen, J. Statistical Power Analysis for the Behavioral Sciences (Routledge, 2013).
Doty, R. L., Shaman, P., Kimmelman, C. P. & Dann, M. S. University of Pennsylvania Smell Identification Test: a rapid quantitative olfactory function test for the clinic. Laryngoscope 94, 176–178 (1984).
pubmed: 6694486
doi: 10.1288/00005537-198402000-00004
Team, J. JASP (Version 0.10. 1)[Computer Software] (JASP, 2019).
Kass, R. E. & Raftery, A. E. Bayes factors. J. Am. Stat. Assoc. 90, 773–795 (1995).
doi: 10.1080/01621459.1995.10476572