New chemosensory component in the U.S. National Health and Nutrition Examination Survey (NHANES): first-year results for measured olfactory dysfunction

  • Howard J. Hoffman
  • Shristi Rawal
  • Chuan-Ming Li
  • Valerie B. Duffy
Article

Abstract

The U.S. NHANES included chemosensory assessments in the 2011–2014 protocol. We provide an overview of this protocol and 2012 olfactory exam findings. Of the 1818 NHANES participants aged ≥40 years, 1281 (70.5 %) completed the exam; non-participation mostly was due to time constraints. Health technicians administered an 8-item, forced-choice, odor identification task scored as normosmic (6–8 odors identified correctly) versus olfactory dysfunction, including hyposmic (4–5 correct) and anosmic/severe hyposmic (0–3 correct). Interviewers recorded self-reported smell alterations (during past year, since age 25, phantosmia), histories of sinonasal problems, xerostomia, dental extractions, head or facial trauma, and chemosensory-related treatment and changes in quality of life. Olfactory dysfunction was found in 12.4 % (13.3 million adults; 55 % males/45 % females) including 3.2 % anosmic/severe hyposmic (3.4 million; 74 % males/26 % females). Selected age-specific prevalences were 4.2 % (40–49 years), 12.7 % (60–69 years), and 39.4 % (80+ years). Among adults ≥70 years, misidentification rates for warning odors were 20.3 % for smoke and 31.3 % for natural gas. The highest sensitivity (correctly identifying dysfunction) and specificity (correctly identifying normosmia) of self-reported olfactory alteration was among anosmics/severe hyposmics (54.4 % and 78.1 %, respectively). In age- and sex-adjusted logistic regression analysis, risk factors of olfactory dysfunction were racial/ethnic minority, income-to-poverty ratio ≤ 1.1, education <high school, and heavy drinking. Moderate-to-vigorous physical activity reduced risk of impairment. Olfactory dysfunction is prevalent, particularly among older adults. Inexpensive, brief odor identification tests coupled with questions (smell problems past year, since age 25, phantosmia) could screen for marked dysfunction. Healthcare providers should be prepared to offer education on non-olfactory avoidance of hazardous events.

Keywords

Olfaction disorders Epidemiology Taste Risk factors Public health surveillance Health status 

References

  1. 1.
    National Health and Nutrition Examination Survey: Plan and Operations, 1999–2010. Centers for Disease Control and Prevention (CDC), National Center for Health Statistics (NCHS). Available from: http://www.cdc.gov/nchs/data/series/sr_01/sr01_056.pdf. Accessed May 20, 2016.
  2. 2.
    National Institutes on Deafness and Other Communication Disorders. NIDCD Workshop on Epidemiology of Communication Disorders. 2005. Available from: http://www.nidcd.nih.gov/funding/programs/pages/episummary.aspx. Accessed May 20, 2016.
  3. 3.
    Healthy People 2020 Topics & Objectives: Hearing and Other Sensory or Communication Disorders. U.S. Department of Health and Human Services, Office of Disease Prevention and Health Promotion. Available from: http://www.healthypeople.gov/2020/topicsobjectives2020/objectiveslist.aspx?topicId=20. Accessed May 20, 2016.
  4. 4.
    National Health and Nutrition Examination Survey (NHANES) Taste and Smell Examination Component Manual. CDC, NCHS. Available from: http://www.cdc.gov/nchs/data/nhanes/nhanes_13_14/Taste_Smell.pdf. Accessed May 20, 2016.
  5. 5.
    NIH Toolbox For the Assessment of Neurological and Behavioral Function. NIH Blueprint for Neuroscience Research. Available from: http://www.nihtoolbox.org/WhatAndWhy/Sensation. Accessed May 20, 2016.
  6. 6.
    Coldwell SE, Mennella JA, Duffy VB, Pelchat ML, Griffith JW, Smutzer G, et al. Gustation assessment using the NIH Toolbox. Neurology. 2013;80(11 Suppl 3):S20–4.Google Scholar
  7. 7.
    Dalton P, Doty RL, Murphy C, Frank R, Hoffman HJ, Maute C, et al. Olfactory assessment using the NIH Toolbox. Neurology. 2013;80(11 Suppl 3):S32–6.Google Scholar
  8. 8.
    NHANES. 2011–2012 Data Documentation, Codebook, and Frequencies: Taste and Smell Disorders [internet]. CDC, NCHS. Available from: http://www.cdc.gov/nchs/nhanes/nhanes2011-2012/CSQ_G.htm. Accessed May 20, 2016.
  9. 9.
    Rawal S, Hoffman HJ, Bainbridge KE, Huedo-Medina TB, Duffy VB. Prevalence and risk factors of self-reported smell and taste alterations: results from the 2011-2012 US National Health and Nutrition Examination Survey (NHANES). Chem Senses. 2016;41(1):69–76.CrossRefPubMedGoogle Scholar
  10. 10.
    Rawal S, Hoffman HJ, Chapo AK, Duffy VB. Sensitivity and specificity of self-reported olfactory dysfunction in a home-based study of independent-living. Healthy Older Women Chemosens Percept. 2014;7(304):108–16.CrossRefPubMedGoogle Scholar
  11. 11.
    Murphy C, Schubert C, Cruickshanks K, Klein B, Klein R, Nondahl D. Prevalence of olfactory impairment in older adults. J Am Med Assoc. 2002;288(18):2307–12.CrossRefGoogle Scholar
  12. 12.
    Schubert CR, Cruickshanks KJ, Fischer ME, Huang GH, Klein BE, Klein R, et al. Olfactory impairment in an adult population: the Beaver Dam Offspring Study. Chem Senses. 2012;37(4):325–34.Google Scholar
  13. 13.
    Hoffman H, Ishii E, MacTurk R. 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. 1998;855:716–22.Google Scholar
  14. 14.
    Rawal S, Hoffman HJ, Honda M, Huedo-Medina TB, Duffy VB. The taste and smell protocol in the 2011-2014 U.S. National Health and Nutrition Examination Survey (NHANES): test-retest reliability and validity testing. Chemosens Percept. 2015;8(3):138–48.Google Scholar
  15. 15.
    Wehling E, Nordin S, Espeseth T, Reinvang I, Lundervold AJ. Unawareness of olfactory dysfunction and its association with cognitive functioning in middle aged and old adults. Arch Clin Neuropsychol. 2011;26(3):260–9.CrossRefPubMedGoogle Scholar
  16. 16.
    Bramerson A, Johansson L, Ek L, Nordin S, Bende M. Prevalence of olfactory dysfunction: the Skovde population-based study. Laryngoscope. 2004;114(4):733–7.CrossRefPubMedGoogle Scholar
  17. 17.
    Shu CH, Hummel T, Lee PL, Chiu CH, Lin SH, Yuan BC. The proportion of self-rated olfactory dysfunction does not change across the life span. Am J Rhinol Allergy. 2009;23(4):413–6.CrossRefPubMedGoogle Scholar
  18. 18.
    Lee WH, Wee JH, Kim DK, Rhee CS, Lee CH, Ahn S, et al. Prevalence of subjective olfactory dysfunction and its risk factors: Korean National Health and Nutrition Examination Survey. PLoS One. 2013;8(5):e62725.CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Michikawa T, Nishiwaki Y, Takebayashi T. Are you conscious of any age-related taste impairment? Prevalence of and factors associated with taste impairment in Japan. J Am Geriatr Soc. 2011;59(5):951–3.CrossRefPubMedGoogle Scholar
  20. 20.
    Welge-Lussen A, Dorig P, Wolfensberger M, Krone F, Hummel T. A study about the frequency of taste disorders. J Neurol. 2011;258(3):386–92.CrossRefPubMedGoogle Scholar
  21. 21.
    Bartoshuk LM, Duffy VB, Green BG, Hoffman HJ, Ko CW, Lucchina LA, et al. Valid across-group comparisons with labeled scales: the gLMS versus magnitude matching. Physiol Behav. 2004;82(1):109–14.CrossRefPubMedGoogle Scholar
  22. 22.
    Galindo-Cuspinera V, Waeber T, Antille N, Hartmann C, Stead N, Martin N. Reliability of threshold and suprathreshold methods for taste phenotyping: characterization with PROP and sodium chloride. Chemosens Percept. 2009;2(4):214–28.Google Scholar
  23. 23.
    Pepino MY, Bradley D, Eagon JC, Sullivan S, Abumrad NA, Klein S. Changes in taste perception and eating behavior after bariatric surgery-induced weight loss in women. Obesity (Silver Spring). 2014;22(5):E13–20.CrossRefGoogle Scholar
  24. 24.
    Pelletier CA, Steele CM. Influence of the perceived taste intensity of chemesthetic stimuli on swallowing parameters given age and genetic taste differences in healthy adult women. J Speech Lang Hear Res. 2014;57(1):46–56.CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    McAnally HM, Poulton R, Hancox RJ, Prescott J, Welch D. Psychosocial correlates of 6-n-propylthiouracil (PROP) ratings in a birth cohort. Appetite. 2007;49(3):700–3.CrossRefPubMedGoogle Scholar
  26. 26.
    Cruickshanks KJ, Schubert CR, Snyder DJ, Bartoshuk LM, Huang GH, Klein BE, et al. Measuring taste impairment in epidemiologic studies: the Beaver Dam Offspring Study. Ann N Y Acad Sci. 2009;1170:543–52.Google Scholar
  27. 27.
    Dias AG, Rousseau D, Duizer L, Cockburn M, Chiu W, Nielsen D, et al. Genetic variation in putative salt taste receptors and salt taste perception in humans. Chem Senses. 2013;38(2):137–45.CrossRefPubMedGoogle Scholar
  28. 28.
    Rawal S, Hayes JE, Wallace MR, Bartoshuk LM, Duffy VB. Do polymorphisms in the TAS1R1 gene associate with broader differences in human taste intensity? Chem Senses. 2013;38(8):719–28.CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Fischer ME, Cruickshanks KJ, Pankow JS, Pankratz N, Schubert CR, Huang GH, et al. The associations between 6-n-propylthiouracil (PROP) intensity and taste intensities differ by TAS2R38 haplotype. J Nutrigenet Nutrigenomics. 2014;7(3):143–52.CrossRefPubMedGoogle Scholar
  30. 30.
    Dinehart ME, Hayes JE, Bartoshuk LM, Lanier SL, Duffy VB. Bitter taste markers explain variability in vegetable sweetness, bitterness, and intake. Physiol Behav. 2006;87(2):304–13.CrossRefPubMedGoogle Scholar
  31. 31.
    Hayes JE, Sullivan BS, Duffy VB. Explaining variability in sodium intake through oral sensory phenotype, salt sensation and liking. Physiol Behav. 2010;100(4):369–80.CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Fischer ME, Cruickshanks KJ, Schubert CR, Pinto A, Huang GH, Klein BE, et al. The association of taste with change in adiposity-related health measures. J Acad Nutr Diet. 2014;114(8):1195–202.CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Simchen U, Koebnick C, Hoyer S, Issanchou S, Zunft HJ. Odour and taste sensitivity is associated with body weight and extent of misreporting of body weight. Eur J Clin Nutr. 2006;60(6):698–705.CrossRefPubMedGoogle Scholar
  34. 34.
    Kveton J, Bartoshuk L. The effect of unilateral chorda tympani damage on taste. Laryngoscope. 1994;104(1):25–9.CrossRefPubMedGoogle Scholar
  35. 35.
    Yanagisawa K, Bartoshuk LM, Catalanotto FA, Karrer TA, Kveton JF. Anesthesia of the chorda tympani nerve and taste phantoms. Physiol Behav. 1997;63(3):329–35.CrossRefGoogle Scholar
  36. 36.
    Sipiora ML, Murtaugh MA, Gregoire MB, Duffy VB. Bitter taste perception and severe vomiting in pregnancy. Physiol Behav. 2000;69(3):259–67.CrossRefPubMedGoogle Scholar
  37. 37.
    Bartoshuk LM, Catalanotto F, Hoffman H, Logan H, Snyder DJ. Taste damage (otitis media, tonsillectomy and head and neck cancer), oral sensations and BMI. Physiol Behav. 2012;107(4):516–26.CrossRefPubMedGoogle Scholar
  38. 38.
    Duffy VB, Peterson J, Bartoshuk LM. Associations between taste genetics, oral sensations and alcohol intake. Physiol Behav. 2004;82(2–3):435–45.CrossRefPubMedGoogle Scholar
  39. 39.
    Reed DR, Zhu G, Breslin PA, Duke FF, Henders AK, Campbell MJ, et al. The perception of quinine taste intensity is associated with common genetic variants in a bitter receptor cluster on chromosome 12. Hum Mol Genet. 2010;19(21):4278–85.CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Cowart B, Yokomukai Y, Beauchamp G. Bitter taste in aging: compound-specific decline in sensitivity. Physiol Behav. 1994;56(6):1237–41.CrossRefPubMedGoogle Scholar
  41. 41.
    Campbell MC, Ranciaro A, Froment A, Hirbo J, Omar S, Bodo JM, et al. Evolution of functionally diverse alleles associated with PTC bitter taste sensitivity in Africa. Mol Biol Evol. 2012;29(4):1141–53.CrossRefPubMedGoogle Scholar
  42. 42.
    Bartoshuk LM, Duffy VB, Miller Jr IJ. PTC/PROP tasting: anatomy, psychophysics, and sex effects. Physiol Behav. 1994;56(6):1165–71.Google Scholar
  43. 43.
    Tepper BJ. Nutritional implications of genetic taste variation: the role of PROP sensitivity and other taste phenotypes. Annu Rev Nutr. 2008;28:367–88.CrossRefPubMedGoogle Scholar
  44. 44.
    Akmal A, Kung J. Propylthiouracil, and methimazole, and carbimazole-related hepatotoxicity. Expert Opin Drug Saf. 2014;13(10):1397–406.CrossRefPubMedGoogle Scholar
  45. 45.
    Coldwell S, Duffy V, Bartoshuk L, Griffith J, Hoffman H. The NIH Toolbox brief gustation assessment protocol (abstract). 2013;Abstracts from the 35th Annual Meeting of AChemS—Chem Senses:A114.Google Scholar
  46. 46.
    Doty R, Frye R. Influence of nasal obstruction on smell function. Otolaryngol Clin N Am. 1989;22:397–441.Google Scholar
  47. 47.
    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(1):39–52.CrossRefPubMedGoogle Scholar
  48. 48.
    Cain WS, Rabin MD. Comparability of two tests of olfactory functioning. Chem Senses. 1989;14(4):479–85.CrossRefGoogle Scholar
  49. 49.
    Doty R, Shaman P, Dann M. Development of the University of Pennsylvania smell identification test: a standardized microencapsulated test of olfactory function. Physiol Behav. 1984;34:489–502.CrossRefGoogle Scholar
  50. 50.
    Schumm LP, McClintock M, Williams S, Leitsch S, Lundstrom J, Hummel T, et al. Assessment of sensory function in the National Social Life, Health, and Aging Project. J Gerontol B Psychol Sci Soc Sci. 2009;64(Suppl 1):i76–85.Google Scholar
  51. 51.
    NHANES 2011–2012 Overview. 2015. CDC, NCHS Available at: http://www.cdc.gov/nchs/nhanes/nhanes2011-2012/overview_g.htm. Accessed May 20, 2016.
  52. 52.
    CDC. 2011-2012 National Health and Nutrition Examination Survey (NHANES): Survey Operations Manuals. Available from URL: http://www.cdc.gov/nchs/nhanes/nhanes2011-2012/manuals11_12.htm. Accessed May 20, 2016.
  53. 53.
    U.S. Census. Poverty-Definitions. Available at: https://www.census.gov/hhes/www/poverty/methods/definitions.html. Accessed May 20, 2016.
  54. 54.
    Sabanayagam C, Shankar A. Income is a stronger predictor of mortality than education in a national sample of US adults. J Health Popul Nutr. 2012;20:82–6.Google Scholar
  55. 55.
    Doty RL, Shaman P, Applebaum SL, Giberson R, Siksorski L, Rosenberg L. Smell identification ability: changes with age. Science. 1984;226(4681):1441–2.CrossRefPubMedGoogle Scholar
  56. 56.
    Ship J, Weiffenbach J. Age, gender, medical treatment and medication effects on smell identification. J Gerontol. 1993;48:M26–32.CrossRefPubMedGoogle Scholar
  57. 57.
    Wysocki CJ, Gilbert AN. The National Geographic Smell Survey: effects of age are heterogeneous. Ann N Y Acad Sci. 1989;561:12–28.Google Scholar
  58. 58.
    Schubert CR, Cruickshanks KJ, Fischer ME, Huang GH, Klein R, Tsai MY, et al. Carotid intima media thickness, atherosclerosis, and 5-year decline in odor identification: the Beaver Dam Offspring Study. J Gerontol A Biol Sci Med Sci. 2015;70(7):879–84.Google Scholar
  59. 59.
    Vennemann M, Hummel T, Berger K. The association between smoking and smell and taste impairment in the general population. J Neurol. 2008;255(8):1121–6.CrossRefPubMedGoogle Scholar
  60. 60.
    Mullol J, Alobid I, Marino-Sanchez F, Quinto L, de Haro J, Bernal-Sprekelsen M et al. Furthering the understanding of olfaction, prevalence of loss of smell and risk factors: a population-based survey (OLFACAT study). BMJ Open. 2012;2(6).Google Scholar
  61. 61.
    Wilson RS, Arnold SE, Tang Y, Bennett DA. Odor identification and decline in different cognitive domains in old age. Neuroepidemiology. 2006;26(2):61–7.CrossRefPubMedGoogle Scholar
  62. 62.
    Roberts RO, Christianson TJ, Kremers WK, Mielke MM, Machulda MM, Vassilaki M, et al. Association between olfactory dysfunction and amnestic mild cognitive impairment and Alzheimer disease dementia. JAMA Neurol. 2016;73(1):93–101.CrossRefPubMedGoogle Scholar
  63. 63.
    Pinto JM, Wroblewski KE, Kern DW, Schumm LP, McClintock MK. The rate of age-related olfactory decline among the general population of older U.S. adults. J Gerontol A Biol Sci Med Sci. 2015;70(11):1435–41.CrossRefPubMedGoogle Scholar
  64. 64.
    Pence TS, Reiter ER, DiNardo LJ, Costanzo RM. Risk factors for hazardous events in olfactory-impaired patients. JAMA Otolaryngol Head Neck Surg. 2014;140(10):951–5.CrossRefPubMedGoogle Scholar
  65. 65.
    Suchowersky O, Reich S, Perlmutter J, Zesiewicz T, Gronseth G, Weiner WJ, et al. Practice parameter: diagnosis and prognosis of new onset Parkinson disease (an evidence-based review): Report of the Quality Standards Subcommittee of the American Academy of Neurology. Neurology. 2006;66(7):968–75.Google Scholar
  66. 66.
    Aetna. Smell and Taste Disorders: Diagnosis. 2015 Available at: http://www.aetna.com/cpb/medical/data/300_399/0390.html. Accessed May 20, 2016.
  67. 67.
    ICD10Data.com. Symptoms and signs involving cognition, perception, emotional state and behavior. In: ICD-10-CM Diagnosis Codes. 2016. Available at: http://www.icd10data.com/ICD10CM/Codes/R00-R99/R40-R46/R43-. Accessed May 20, 2016.
  68. 68.
    Malaty J, Malaty IA. Smell and taste disorders in primary care. Am Fam Physician. 2013;88(12):852–9.PubMedGoogle Scholar
  69. 69.
    Eekhof JA, De Bock GH, Schaapveld K, Springer MP. Screening for hearing and visual loss among elderly with questionnaires and tests: which method is the most convincing for action? Scand J Prim Health Care. 2000;18(4):203–7.CrossRefPubMedGoogle Scholar
  70. 70.
    Nguyen AD, Shenton ME, Levitt JJ. Olfactory dysfunction in schizophrenia: a review of neuroanatomy and psychophysiological measurements. Harv Rev Psychiatry. 2010;18(5):279–92.CrossRefPubMedGoogle Scholar
  71. 71.
    Knaapila A, Tuorila H, Kyvik KO, Wright MJ, Keskitalo K, Hansen J, et al. Self-ratings of olfactory function reflect odor annoyance rather than olfactory acuity. Laryngoscope. 2008;118(12):2212–7.CrossRefPubMedGoogle Scholar
  72. 72.
    Kuk JL, Ardern CI. The influence of ethnicity and gender on the association between measured obesity and cardiorespiratory fitness with self-rated overweight, physical activity and health. Perspect Public Health. 2014;134(1):38–43.CrossRefPubMedGoogle Scholar
  73. 73.
    Schubert CR, Cruickshanks KJ, Nondahl DM, Klein BE, Klein R, Fischer ME. Association of exercise with lower long-term risk of olfactory impairment in older adults. JAMA Otolaryngol Head Neck Surg. 2013;139(10):1061–6.CrossRefPubMedGoogle Scholar
  74. 74.
    Menon C, Westervelt HJ, Jahn DR, Dressel JA, O'Bryant SE. Normative performance on the brief smell identification test (BSIT) in a multi-ethnic bilingual cohort: a project FRONTIER study. Clin Neuropsychol. 2013;27(6):946–61.CrossRefPubMedPubMedCentralGoogle Scholar
  75. 75.
    Boesveldt S, Lindau ST, McClintock MK, Hummel T, Lundstrom JN. Gustatory and olfactory dysfunction in older adults: a national probability study. Rhinology. 2011;49(3):324–30.PubMedPubMedCentralGoogle Scholar
  76. 76.
    Doty RL, Petersen I, Mensah N, Christensen K. Genetic and environmental influences on odor identification ability in the very old. Psychol Aging. 2011;26(4):864–71.CrossRefPubMedPubMedCentralGoogle Scholar
  77. 77.
    Martinez-Martin P, Falup Pecurariu C, Odin P, van Hilten JJ, Antonini A, Rojo-Abuin JM, et al. Gender-related differences in the burden of non-motor symptoms in Parkinson's disease. J Neurol. 2012;259(8):1639–47.CrossRefPubMedGoogle Scholar
  78. 78.
    Krantz EM, Schubert CR, Dalton DS, Zhong W, Huang GH, Klein BE, et al. Test-retest reliability of the San Diego odor identification test and comparison with the brief smell identification test. Chem Senses. 2009;34(5):435–40.CrossRefPubMedPubMedCentralGoogle Scholar
  79. 79.
    Doty RL, Applebaum S, Zusho H, Settle RG. Sex differences in odor identification ability: a cross-cultural analysis. Neuropsychologia. 1985;23(5):667–72.CrossRefPubMedGoogle Scholar
  80. 80.
    Pinto JM, Schumm LP, Wroblewski KE, Kern DW, McClintock MK. Racial disparities in olfactory loss among older adults in the United States. J Gerontol A Biol Sci Med Sci. 2014;69(3):323–9.CrossRefPubMedGoogle Scholar
  81. 81.
    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(2):167–73.CrossRefPubMedGoogle Scholar
  82. 82.
    Shiga H, Yamamoto J, Kitamura M, Nakagawa H, Matsubasa T, Seo A, et al. Combinations of two odorants of smell identification test for screening of olfactory impairment. Auris Nasus Larynx. 2014;41(6):523–7.CrossRefPubMedGoogle Scholar
  83. 83.
    Ogihara H, Kobayashi M, Nishida K, Kitano M, Takeuchi K. Applicability of the cross-culturally modified University of Pennsylvania Smell Identification Test in a Japanese population. Am J Rhinol Allergy. 2011;25(6):404–10. doi:10.2500/ajra.2011.25.3658.CrossRefPubMedGoogle Scholar
  84. 84.
    Patel HH, Straight CE, Lehman EB, Tanner M, Carr MM. Indications for tonsillectomy: a 10 year retrospective review. Int J Pediatr Otorhinolaryngol. 2014;78(12):2151–5.CrossRefPubMedGoogle Scholar
  85. 85.
    Grob GN. The rise and decline of tonsillectomy in twentieth-century America. J Hist Med Allied Sci. 2007;62(4):383–421.CrossRefPubMedGoogle Scholar
  86. 86.
    Holbrook EH, Leopold DA. An updated review of clinical olfaction. Curr Opin Otolaryngol Head Neck Surg. 2006;14(1):23–8.CrossRefPubMedGoogle Scholar
  87. 87.
    Revai K, Dobbs LA, Nair S, Patel JA, Grady JJ, Chonmaitree T. Incidence of acute otitis media and sinusitis complicating upper respiratory tract infection: the effect of age. Pediatrics. 2007;119(6):e1408–12.CrossRefPubMedGoogle Scholar
  88. 88.
    Linder JA, Singer DE. Health-related quality of life of adults with upper respiratory tract infections. J Gen Intern Med. 2003;18(10):802–7.CrossRefPubMedPubMedCentralGoogle Scholar
  89. 89.
    Takano K, Yamamoto M, Kondo A, Takahashi H, Himi T. A clinical study of olfactory dysfunction in patients with Mikulicz's disease. Auris Nasus Larynx. 2011;38(3):347–51.CrossRefPubMedGoogle Scholar
  90. 90.
    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(12):1512–4.CrossRefGoogle Scholar
  91. 91.
    Coelho DH, Costanzo RM. Posttraumatic olfactory dysfunction. Auris Nasus Larynx. 2016 Apr;43(2):137–43.Google Scholar
  92. 92.
    Stuck BA, Hummel T. Olfaction in allergic rhinitis: a systematic review. J Allergy Clin Immunol. 2015;136(6):1460–70.CrossRefPubMedGoogle Scholar
  93. 93.
    Schubert CR, Cruickshanks KJ, Klein BE, Klein R, Nondahl DM. Olfactory impairment in older adults: five-year incidence and risk factors. Laryngoscope. 2011;121(4):873–8.CrossRefPubMedPubMedCentralGoogle Scholar
  94. 94.
    Maurage P, Callot C, Chang B, Philippot P, Rombaux P, de Timary P. Olfactory impairment is correlated with confabulation in alcoholism: towards a multimodal testing of orbitofrontal cortex. PLoS One. 2011;6(8):e23190.CrossRefPubMedPubMedCentralGoogle Scholar
  95. 95.
    Pasala S, Barr T, Messaoudi I. Impact of alcohol abuse on the adaptive immune system. Alcohol Res. 2015;37(2):185–97.PubMedPubMedCentralGoogle Scholar
  96. 96.
    Selya AS, Oancea SC, Thapa S. Time to first cigarette, a proxy of nicotine dependence, increases the risk of pulmonary impairment, independently of current and lifetime smoking behavior. Nicotine Tob Res. 2016;18(6):1431–9.CrossRefPubMedGoogle Scholar
  97. 97.
    Glennon S-G, Litt M, Duffy VB. Olfactory but not taste dysfunction among chronic smokers: baseline results from an e-cigarette intervention. Association for Chemoreception Sciences Annual Meeting; Bonita Springs, FL: Chemical Senses; 2016. p. in press (abstract).Google Scholar
  98. 98.
    Glennon S-G, Rawal S, Hoffman H, Duffy V. Chronic cigarette exposure associates with self-reported smell alterations: findings from the U.S. National Health and nutrition examination survey (NHANES) 2011-2012. Association for Chemoreception Sciences Annual Meeting. Bonita Springs, FL: Chemical Senses. 2015;40(7):624–5.Google Scholar
  99. 99.
    Fishman EI, Steeves JA, Zipunnikov V, Koster A, Berrigan D, Harris TA et al. Association between objectively measured physical activity and mortality in NHANES. Med Sci Sports Exerc. 2016.Google Scholar
  100. 100.
    Cain WS, Gent JF, Goodspeed RB, Leonard G. Evaluation of olfactory dysfunction in the Connecticut chemosensory clinical research center. Laryngoscope. 1988;98:83–8.CrossRefPubMedGoogle Scholar
  101. 101.
    Doty RL, Kamath V. The influences of age on olfaction: a review. Front Psychol. 2014;5:20.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  • Howard J. Hoffman
    • 1
  • Shristi Rawal
    • 2
    • 3
  • Chuan-Ming Li
    • 1
  • Valerie B. Duffy
    • 3
  1. 1.Epidemiology and Statistics ProgramDivision of Scientific Programs, National Institute on Deafness and other Communication Disorders (NIDCD) at the National Institutes of Health (NIH)BethesdaUSA
  2. 2.Epidemiology Branch, Division of Intramural Population Health ResearchEunice Kennedy Shriver National Institute of Child Health and Human Development (NICHD), NIHRockvilleUSA
  3. 3.Department of Allied Health SciencesUniversity of ConnecticutStorrsUSA

Personalised recommendations