This cohort study investigates the associations of prior head injury, number of prior head injuries, and head injury severity with subjective and psychophysical olfactory function in older adults.
Key Points
Question
What is the association of prior head injury, number of prior head injuries, and head injury severity with subjective and psychophysical (objective) olfactory function in older adults?
Findings
Participants with a history of prior head injury, particularly individuals with 2 or more prior head injuries and moderate, severe, or penetrating head injuries, were more likely to have objective anosmia compared with participants with no history of head injury.
Meaning
There should be consideration of objective olfactory assessment in patients with head injury; this is particularly important because poor olfaction has previously been associated with negative health outcomes.
Abstract
Importance
Traumatic brain injury has been associated with short-term olfactory dysfunction, but the association of number of prior head injuries and head injury severity with both subjective and objective long-term olfactory function is less clear.
Objective
To investigate the associations of prior head injury, number of prior head injuries, and head injury severity with subjective and psychophysical (objective) olfactory function in older adults and to examine concordance between subjective and objective olfactory function among individuals with and without head injury.
Design, Setting, and Participants
This prospective cohort study included 5951 participants who attended Atherosclerosis Risk in Communities (ARIC) Study visit 5 (2011 through 2013). Data analysis was performed between November 2021 and May 2022.
Exposures
Head injury was defined by self-report and International Classification of Diseases codes.
Main Outcomes and Measures
Self-reported subjective olfactory dysfunction was assessed by the question, “Do you suffer from smell loss or a significantly decreased sense of smell?” Objective olfactory performance was assessed using the 12-item Sniffin’ Sticks odor identification test.
Results
Overall, the 5951 participants were a mean (SD) age of 75.6 (5.2) years, 3501 (58.8%) were female, 1356 (22.8%) were of Black race, and 1666 (28.0%) had a history of head injury. Participants with prior head injury were more likely than individuals without prior head injury to report subjective olfactory dysfunction (24% vs 20%; difference, 4%; 95% CI, 1% to 6%) and have objective anosmia (15% vs 13%; difference, 2%; 95% CI, 0.1% to 4%) but had lower concordance between subjective and objective assessment (72% vs 77%; difference, −5%; 95% CI, −8% to −3%). In logistic regression models adjusted for sociodemographics and medical comorbidities including cognitive status, participants with a history of prior head injury, particularly individuals with 2 or more prior head injuries and more severe head injuries, were more likely to self-report subjective olfactory dysfunction and were more likely to be found to have objective anosmia compared with participants with no history of head injury.
Conclusions and Relevance
Findings of this cohort study provide evidence supporting the association between head injury and olfactory dysfunction, particularly among individuals who experienced multiple prior head injuries and among individuals with more severe head injury. The findings also suggest that individuals with prior head injury were more likely to both under–self-report and over–self-report deficits compared with objective olfactory testing; therefore, it may be important to consider objective olfactory testing in this patient population.
Introduction
The peripheral and central olfactory structures are located in the medial forebrain, making the olfactory system potentially vulnerable to injury following traumatic force to the head. Indeed, case reports by Jackson and Ogle in the late 1800s were among the first to propose an association between head injury and smell loss.1,2 Early clinical case series using self-report and nonstandardized olfactory testing estimated a 4% to 8% prevalence of posttraumatic olfactory loss.3,4,5,6 Because patients often underestimate or are unaware of olfactory loss or conversely may overestimate olfactory loss, these initial studies may either underestimate or overestimate posttraumatic olfactory dysfunction. The development of standardized olfactory psychophysical (objective) assessments has allowed for a more thorough understanding of posttraumatic olfactory dysfunction. When standardized testing is used, significant differences between patients with traumatic brain injury (TBI) and controls have been reliably observed, with more recent studies estimating that approximately 14% to 20% of patients with head injury have olfactory loss.7 There is also more recent evidence suggesting that the prevalence of posttraumatic olfactory dysfunction may vary with injury severity, with prevalence increasing from 0% to 13% for mild TBI to 15% to 30% for moderate or severe TBI.8,9
Many studies examining the association between head injury and olfaction evaluated psychophysical olfactory functioning only in those patients self-reporting smell loss.10 Importantly, prior studies have not comprehensively investigated associations of number of prior head injuries and head injury severity with both subjective and objective olfactory function in the chronic time period postinjury, nor have they rigorously compared concordance between subjective and objective olfactory function among individuals with and without head injury. The Atherosclerosis Risk in Communities (ARIC) Study provides a unique opportunity to examine the association of remote head injury, number of prior head injuries, and head injury severity with both subjective self-reported olfactory dysfunction and psychophysical (objective) olfactory performance in a large community-based cohort of older adults.
Methods
Study Design and Population
The ARIC Study is an ongoing prospective cohort study of 15 792 Black and White individuals aged 45 to 64 years when initially enrolled in 1987 to 1989 from the 4 US communities of suburbs of Minneapolis, Minnesota; Washington County, Maryland; Forsyth County, North Carolina; and Jackson, Mississippi.11,12 In 2011 to 2013, surviving participants were invited for a fifth in-person visit (including the ARIC Neurocognitive Study), which included olfactory assessment. Of the 6538 participants who attended ARIC visit 5, we excluded 44 participants who were of non-Black or non-White race or of Black race at the Minnesota or Maryland field centers, 501 individuals missing olfactory function data, and 42 participants missing data on covariates included in statistical models, leaving a total of 5951 participants included in the analytic population. The ARIC Study was approved by the institutional review boards of all participating institutions, and written informed consent was obtained at each study visit. This study followed the Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) reporting guidelines.
Head Injury Definition
Head injury (with or without loss of consciousness) occurring prior to ARIC visit 5 was defined using both self-reported questions and International Classification of Diseases, Ninth Revision (ICD-9) codes from hospitalizations identified by active surveillance of all ARIC study community hospitals (for all study participants between the ARIC visit 1 date and the ARIC visit 5 date) and from hospitalizations, emergency department visits, and outpatient visits identified using Centers for Medicare & Medicaid Services (CMS) data (for participants aged ≥65 years enrolled in CMS fee-for-service part B between January 1, 1991, and the ARIC visit 5 date) (eTable 1 in the Supplement). The self-reported questions asked about prior head injuries requiring physician or hospital care, the number of prior head injuries, and the year of head injury. Head injury and date of head injury were identified from ARIC hospitalization, and CMS data were defined using the Centers for Disease Control and Prevention ICD-9 code-based definition.13 The 2 main head injury definitions used in this analysis were (1) head injury status (no vs yes history of any head injury) and (2) number of prior head injuries (0, 1, or ≥2 prior head injuries). In secondary analyses, we additionally defined head injury identified by self-report alone and by ICD-9 codes alone. Among head injury cases identified using ICD-9 codes, we additionally categorized head injuries by severity using Department of Defense/Department of Veterans Affairs criteria (mild vs moderate, severe, or penetrating) (eTable 2 in the Supplement).14 If a participant had 2 or more head injury–related ICD-9 coded medical encounters, the most severe injury was used for classification. We have used these definitions previously in the ARIC cohort.15,16,17
Subjective and Psychophysical (Objective) Olfactory Assessment
All participants underwent subjective and psychophysical (objective) olfactory assessment at ARIC visit 5 (2011-2013). Self-reported subjective olfactory dysfunction (yes; no) was assessed by the question, “Do you suffer from smell loss or a significantly decreased sense of smell?” Objective olfactory performance was assessed using the multiple-choice 12-item Sniffin’ Sticks odor identification test (score range, 0-12).18 Participants were asked to identify 12 common odors embedded in felt-tip pens. Objective olfactory dysfunction was evaluated as a binary variable (anosmia [score ≤6] vs no anosmia [score >6]) and as a 3-level variable (anosmia [score ≤6] vs hyposmia [score 7-8] vs normosmia [score >8]).18
Statistical Analyses
Participant characteristics were stratified by head injury status and by number of prior head injuries using means and SDs for continuous variables and counts and proportions for categorical variables. Means and proportions were compared between head injury status groups using absolute differences and 95% CIs. Prevalence and 95% CIs for subjective olfactory dysfunction and objective anosmia were calculated and compared across head injury groups using absolute differences and 95% CIs. Sensitivity, specificity, positive predictive value, and negative predictive value and 95% CIs of self-reported subjective olfactory dysfunction compared with objective assessment of anosmia were calculated in the overall population and stratified by head injury status.
Logistic regression models were used to obtain odds ratios (ORs) and 95% CIs for associations of head injury with subjective olfactory dysfunction (vs no subjective olfactory dysfunction) and objective anosmia (vs no anosmia). Multinomial logistic regression models were used to obtain ORs and 95% CIs for associations of head injury with objective hyposmia and anosmia (vs normosmia). Formal testing for interaction by age, sex, and race was performed. In a sensitivity analysis, we excluded individuals who answered “yes” to the question, “Have you had a stuffy nose in the past 2 weeks, for example, from a cold or allergies?” (n = 2719 excluded). We also performed a sensitivity analysis excluding individuals with prior sinus surgery, nasal polyps, or chronic rhinosinusitis (as identified by the following ICD-9 diagnostic or procedure codes: 22.x, 471.x, and 473.x) (n = 1029 excluded). In an additional sensitivity analysis performed among the subpopulation of participants selected for further assessment (including questions about neurologic disease history) as part of the second stage of ARIC visit 5 (n = 2715, selection criteria detailed previously19), we excluded individuals with Parkinson disease or prior surgery/radiation therapy involving the skull base or brain (n = 92 excluded). In this sensitivity analysis, we incorporated sampling weights to account for subsample participant selection.
All covariates included in statistical models were assessed at ARIC visit 5 (2011-2013), unless otherwise specified. Race was self-reported and collected in the following categories: Black, White (ethnicity was not collected). Model 1 included age (years; continuous), sex (male; female), self-reported race (Black; White), field center (Minnesota; Maryland; North Carolina; Mississippi), education (<high school; high school/General Educational Development certificate/vocational school; college/graduate/professional school, assessed at visit 1), military veteran status (yes; no, assessed at visit 1). Model 2 included variables in model 1 plus smoking (never; former; current; not reported), alcohol consumption (never; former; current; not reported), diabetes (yes; no; defined as fasting glucose level ≥126 mg/dL, nonfasting glucose level ≥200 mg/dL [to convert to mmol/L, multiply by 0.0555], hemoglobin A1c level ≥6.5%, use of diabetes medications, or self-reported history of physician diagnosis), depression (yes; no; defined using a score of ≥9 on the 11-item Center for Epidemiologic Studies Depression questionnaire20), and cognitive status (normal; mild cognitive impairment; dementia; defined using the standardized ARIC algorithm, as previously described19). Analyses were performed between November 2021 and May 2022 using Stata SE, version 17 (StataCorp LLC).
Results
Among the 5951 included participants, 1666 had a history of prior head injury (1280 with 1 prior head injury and 386 with ≥2 prior head injuries) occurring a median (IQR) of 33.7 (15.3-58.7) years prior to olfactory function assessment. Overall, participants were a mean (SD) age of 75.6 (5.2) years, 3501 (58.8%) were female, 1356 (22.8%) were of Black race, and 4595 (77.2%) were of White race. Participants with a history of any head injury and with a greater number of head injuries were older, more likely to be men, of White race, be a military veteran, be a former or current smoker, be a current consumer of alcohol, have depression, and have mild cognitive impairment or dementia (Table 1).
Table 1. Participant Characteristics by Head Injury Status and by Number of Prior Head Injuries, ARIC Visit 5 (2011-2013).
| No. (%) | Absolute difference (95% CI) comparing yes vs no prior head injuriesa | No. (%) | Absolute difference (95% CI)a | |||||
|---|---|---|---|---|---|---|---|---|
| No history of head injury (n = 4285) | History of head injury (n = 1666) | No history of head injury (n = 4285) | 1 Prior head injury (n = 1280) | ≥2 Prior head injuries (n = 386) | Comparing 1 vs no prior head injuries | Comparing ≥2 vs no prior head injuries | ||
| Subjective olfactory dysfunction | 863 (20.1) | 399 (23.9) | 3.8 (1.4 to 6.2) | 863 (20.1) | 294 (23.0) | 105 (27.2) | 2.8 (2.3 to 5.4) | 7.1 (2.5 to 11.7) |
| Sniffin’ Sticks score, mean (SD) | 9.26 (2.39) | 9.06 (2.49) | −0.20 (−0.34 to −0.06) | 9.26 (2.39) | 9.12 (2.42) | 8.85 (2.68) | −0.14 (−0.29 to 0.01) | −0.40 (−0.66 to −0.15) |
| Objective olfactory function (Sniffin’ Sticks score) | ||||||||
| Normosmia (>8) | 3018 (70.4) | 1116 (67.0) | −3.4 (−6.1 to −0.8) | 3018 (70.4) | 872 (68.1) | 244 (63.2) | −2.3 (−5.2 to 0.6) | −7.2 (−12.2 to −2.2) |
| Hyposmia (7-8) | 700 (16.3) | 294 (17.6) | 1.3 (−0.8 to 3.5) | 700 (16.3) | 225 (17.6) | 69 (17.9) | 1.2 (−1.1 to 3.6) | 1.5 (−2.4 to 5.5) |
| Anosmia (≤6) | 567 (13.2) | 256 (15.4) | 2.1 (0.1 to 4.1) | 567 (13.2) | 183 (14.3) | 73 (18.9) | 1.1 (−1.1 to 3.2) | 5.7 (1.6 to 9.7) |
| Age, mean (SD), y | 75.4 (5.1) | 76.1 (5.3) | 0.7 (0.5 to 1.0) | 75.4 (5.1) | 76.1 (5.3) | 76.3 (5.4) | 0.7 (0.4 to 1.0) | 0.9 (0.3 to 1.5) |
| Sex | ||||||||
| Female | 2631 (61.4) | 870 (52.2) | −9.2 (−12.0 to −6.4) | 2631 (61.4) | 668 (52.2) | 202 (52.3) | −9.2 (−12.3 to −6.1) | −9.1 (−14.3 to −3.9) |
| Male | 1654 (38.6) | 796 (47.8) | 9.2 (6.4 to 12.0) | 1654 (38.6) | 612 (47.8) | 184 (47.7) | 9.2 (6.1 to 12.3) | 9.1 (3.9 to 14.3) |
| Race | ||||||||
| Black | 1061 (24.8) | 295 (17.7) | −7.1 (−9.3 to −4.8) | 1061 (24.8) | 241 (18.8) | 54 (14.0) | −5.9 (−8.4 to −3.4) | −10.8 (−14.5 to −7.1) |
| White | 3224 (75.2) | 1371 (82.3) | 7.1 (4.8 to 9.3) | 3224 (75.2) | 1039 (81.2) | 332 (86.0) | 5.9 (3.4 to 8.5) | 10.8 (7.1 to 14.5) |
| Field center | ||||||||
| Minneapolis, Minnesota | 1175 (27.4) | 523 (31.4) | 4.0 (1.4 to 6.6) | 1175 (27.4) | 414 (32.3) | 109 (28.2) | 4.9 (2.0 to 7.8) | 0.8 (−3.9 to 5.5) |
| Washington County, Maryland | 1158 (27.0) | 478 (28.7) | 1.7 (−1.0 to 4.2) | 1158 (27.0) | 346 (27.0) | 132 (34.2) | 0.0 (−2.8 to 2.8) | 7.2 (2.3 to 12.1) |
| Forsyth County, North Carolina | 966 (22.5) | 386 (23.2) | 0.6 (−1.8 to 3.0) | 966 (22.5) | 292 (22.8) | 94 (24.4) | 0.3 (−2.3 to 2.9) | 1.8 (−2.7 to 6.3) |
| Jackson, Mississippi | 986 (23.0) | 279 (16.7) | −6.2 (−8.5 to −4.1) | 986 (23.0) | 228 (17.8) | 51 (13.2) | −5.2 (−7.6 to −2.8) | −9.8 (−13.4 to −6.2) |
| Education | ||||||||
| <High school | 632 (14.7) | 229 (13.7) | −1.0 (−3.0 to 1.0) | 632 (14.7) | 187 (14.6) | 42 (10.9) | −1.4 (−2.3 to 2.1) | −3.9 (−7.2 to −0.6) |
| High school, GED, or vocational school | 1806 (42.1) | 672 (40.3) | −1.8 (−4.6 to 1.0) | 1806 (42.1) | 520 (40.6) | 152 (39.4) | −1.5 (−4.6 to 1.5) | −2.8 (−7.9 to 2.3) |
| College, graduate, or professional school | 1847 (43.1) | 765 (45.9) | 2.8 (0.0 to 5.6) | 1847 (43.1) | 573 (44.8) | 192 (49.7) | 1.7 (−1.4 to 4.8) | 6.6 (1.4 to 11.8) |
| Military veteran | 953 (22.2) | 499 (30.0) | 7.8 (5.2 to 10.2) | 953 (22.2) | 380 (29.7) | 119 (30.8) | 7.4 (4.7 to 10.2) | 8.6 (3.8 to 13.4) |
| Smoking | ||||||||
| Never | 1682 (39.3) | 550 (33.0) | −6.2 (−8.9 to −3.5) | 1682 (39.3) | 418 (32.7) | 132 (34.2) | −6.6 (−9.6 to −3.6) | −5.1 (−10.0 to −0.1) |
| Former | 1901 (44.4) | 853 (51.2) | 6.8 (4.0 to 9.7) | 1901 (44.4) | 655 (51.2) | 198 (51.3) | 6.8 (3.7 to 9.9) | 6.9 (1.7 to 12.1) |
| Current | 242 (5.6) | 92 (5.5) | −0.1 (−1.4 to 1.2) | 242 (5.6) | 66 (5.2) | 26 (6.7) | −0.5 (−1.9 to 0.9) | 1.1 (−1.5 to 3.7) |
| Not reported | 460 (10.7) | 171 (10.3) | −0.5 (−2.2 to 1.3) | 460 (10.7) | 141 (11.0) | 30 (7.8) | 0.3 (−1.7 to 2.2) | −3.0 (−5.8 to −0.1) |
| Alcohol consumption | ||||||||
| Never | 930 (21.7) | 290 (17.4) | −4.3 (−6.5 to −2.1) | 930 (21.7) | 229 (17.9) | 61 (15.8) | −3.8 (−6.2 to −1.4) | −5.9 (−9.7 to −2.1) |
| Former | 1205 (28.1) | 476 (28.6) | 0.5 (−2.1 to 3.0) | 1205 (28.1) | 372 (29.1) | 104 (26.9) | 0.9 (−1.9 to 3.8) | −1.2 (−5.8 to 3.4) |
| Current | 1965 (45.9) | 814 (48.9) | 3.0 (0.1 to 5.8) | 1965 (45.9) | 619 (48.4) | 195 (50.5) | 2.5 (−0.6 to 5.6) | 4.7 (−0.5 to 9.9) |
| Not reported | 185 (4.3) | 86 (5.2) | 0.8 (−0.4 to 2.1) | 185 (4.3) | 60 (4.7) | 26 (6.7) | 0.4 (−0.9 to 1.7) | 2.4 (−0.2 to 5.0) |
| Diabetes | 1558 (36.4) | 658 (39.5) | 3.2 (0.4 to 5.9) | 1558 (36.4) | 506 (39.5) | 152 (39.4) | 3.2 (1.3 to 6.2) | 3.0 (−2.1 to 8.1) |
| Depression | 247 (5.8) | 159 (9.5) | 3.8 (2.2 to 5.4) | 247 (5.8) | 116 (9.1) | 43 (11.1) | 3.3 (1.6 to 5.0) | 5.4 (2.2 to 8.6) |
| Cognitive status | ||||||||
| Normal cognition | 3301 (77.0) | 1169 (70.2) | −6.9 (−9.4 to −4.3) | 3301 (77.0) | 893 (69.8) | 276 (71.5) | −7.3 (−10.1 to −4.5) | −5.5 (−10.2 to −0.9) |
| Mild cognitive impairment | 844 (19.7) | 402 (24.1) | 4.4 (2.1 to 6.8) | 844 (19.7) | 318 (24.8) | 84 (21.8) | 5.1 (2.5 to 7.8) | 2.1 (−2.2 to 6.3) |
| Dementia | 140 (3.3) | 95 (5.7) | 2.4 (1.2 to 3.7) | 140 (3.3) | 69 (5.4) | 26 (6.7) | 2.1 (0.8 to 3.5) | 3.5 (0.9 to 6.0) |
Abbreviations: ARIC, Atherosclerosis Risk in Communities Study; GED, General Educational Development.
Absolute difference (95% CI) in means or percentages between groups.
Overall, 21.2% (1262 of 5951) of the population self-reported subjective olfactory dysfunction, and 13.8% (823 of 5951) of the population was found to have objective anosmia. Participants with a history of any head injury and with a greater number of prior head injuries were more likely to have both subjective and objective olfactory dysfunction (Table 1). However, individuals with prior head injury had lower overall concordance between subjective and objective assessment compared with individuals without prior head injury (1201 of 1666 [72.1%] vs 3305 of 4285 [77.1%] with subjective and objective olfactory assessment in agreement; difference, −5%; 95% CI, −8% to −3%). Among individuals reporting no subjective olfactory dysfunction, individuals with any prior head injury or with 2 or more prior head injuries were more likely to have objective anosmia on psychophysical testing (absolute difference, 2.7%; 95% CI, 0.6% to 4.8% comparing yes with no history of head injury and absolute difference, 5.7%; 95% CI, 1.3% to 11.0% comparing ≥2 prior head injuries with no prior head injuries) (Figure, B). Similarly, among individuals without objective anosmia, individuals with any prior head injury and individuals with either 1 or 2 or more prior head injuries were more likely to have self-reported subjective olfactory dysfunction (absolute difference, 4.4%; 95% CI, 1.9% to 6.9% comparing yes with no history of head injury group, absolute difference, 3.6%; 95% CI, 0.9% to 6.3% comparing 1 prior head injury with no prior head injuries, and absolute difference, 7.1%; 95% CI, 2.2% to 12.0% comparing ≥2 prior head injuries with no prior head injuries) (Figure, D). In contrast, performance across head injury groups was similar when looking among concordant self-reported olfactory dysfunction and objective anosmia (Figure, A and C). Consistent with these findings, the sensitivity and positive predictive value of self-reported subjective olfactory dysfunction compared with objective assessment of anosmia were poor but were similar between head injury groups, while the specificity and negative predictive value of self-reported olfactory dysfunction were lower in the head injury group compared with the no head injury group (Table 2).
Figure. Prevalence of Objective Anosmia Among Individuals With and Without Subjective Olfactory Dysfunction by Head Injury Status and Prevalence of Subjective Olfactory Dysfunction Among Individuals With and Without Objective Anosmia by Head Injury Status.
Prevalence of objective anosmia (defined by Sniffin’ Sticks score ≤6) among individuals with (A, n = 1262) and without (B, n = 4689) subjective olfactory dysfunction by head injury status and prevalence of subjective olfactory dysfunction among individuals with (C, n = 823) and without (D, n = 5128) objective anosmia (defined by Sniffin’ Sticks score ≤6) by head injury status. Error bars indicate 95% CIs.
Table 2. Sensitivity, Specificity, Positive Predictive Value (PPV), and Negative Predictive Value (NPV) for Self-reported Subjective Olfactory Dysfunction Compared With Objective Assessment of Anosmia (Sniffin’ Sticks Score ≤6).
| Overall population (n = 5951) | No history of head injury (n = 4285) | History of head injury (n = 1666) | |
|---|---|---|---|
| Sensitivity (95% CI) | 38.9 (35.5-42.3) | 39.7 (35.6-43.8) | 37.1 (31.2-43.3) |
| Specificity (95% CI) | 81.6 (80.5-82.7) | 82.8 (81.6-84.0) | 78.4 (76.2-80.6) |
| PPV (95% CI) | 25.4 (23.0-27.9) | 26.1 (23.2-29.1) | 23.8 (19.7-28.3) |
| NPV (95% CI) | 89.3 (88.4-90.1) | 90.0 (89.0-91.0) | 87.3 (85.3-89.1) |
A history of any head injury was significantly associated with subjective olfactory dysfunction in the fully adjusted model (model 2), whereas associations with objective anosmia were no longer significant after further adjustment for covariates included in model 2. Having 2 or more prior head injuries was significantly associated with both subjective olfactory dysfunction and with objective anosmia, but not with objective hyposmia, compared with having no prior head injuries (and compared with having 1 prior head injury for associations with objective anosmia) (Table 3). There was no evidence for interaction by age, sex, or race in these associations (all P values for interaction >.20). In a sensitivity analysis excluding individuals who self-reported nasal congestion within 2 weeks of testing, the association of any head injury and of 2 or more prior head injuries with objective anosmia remained significant, whereas associations with subjective olfactory dysfunction were not significant (eTable 3 in the Supplement). In a sensitivity analysis excluding individuals with prior sinus surgery, nasal polyps, or chronic rhinosinusitis, the association of any head injury and of 2 or more prior head injuries with subjective olfactory dysfunction and the association of 2 or more prior head injuries with objective anosmia remained significant (eTable 4 in the Supplement). In a sensitivity analysis among the subset of the population asked about neurologic disease history, excluding individuals with Parkinson disease or with a history of skull base/brain surgery or radiation therapy, a history of 2 or more prior head injuries was significantly associated with objective anosmia (eTable 5 in the Supplement).
Table 3. Associations of Prior Head Injury and Number of Prior Head Injuries With Subjective and Objective Olfactory Functioninga.
| OR (95% CI) | |||||
|---|---|---|---|---|---|
| No history of head injury (n = 4285) | History of head injury (n = 1666) | No history of head injury (n = 4285) | 1 Prior head injury (n = 1280) | ≥2 Prior head injuries (n = 386) | |
| Subjective olfactory dysfunction vs no subjective olfactory dysfunction | |||||
| Model 1 | 1 [Reference] | 1.18 (1.03-1.36) | 1 [Reference] | 1.12 (0.96-1.31) | 1.40 (1.10-1.77) |
| Model 2 | 1 [Reference] | 1.16 (1.01-1.34) | 1 [Reference] | 1.11 (0.95-1.29) | 1.35 (1.06-1.71) |
| Objective anosmia (Sniffin’ Sticks score ≤6) vs no anosmia (Sniffin’ Sticks score >6) | |||||
| Model 1 | 1 [Reference] | 1.18 (1.00-1.40) | 1 [Reference] | 1.05 (0.87-1.27) | 1.66 (1.25-2.20) |
| Model 2 | 1 [Reference] | 1.12 (0.94-1.33) | 1 [Reference] | 0.99 (0.82-1.20) | 1.61 (1.21-2.15) |
| Objective hyposmia (Sniffin’ Sticks score 7-8) vs normosmia (Sniffin’ Sticks score >8) | |||||
| Model 1 | 1 [Reference] | 1.16 (0.99-1.36) | 1 [Reference] | 1.11 (0.94-1.33) | 1.33 (0.99-1.77) |
| Model 2 | 1 [Reference] | 1.11 (0.94-1.30) | 1 [Reference] | 1.06 (0.89-1.27) | 1.27 (0.95-1.71) |
| Objective anosmia (Sniffin’ Sticks score ≤6) vs normosmia (Sniffin’ Sticks score >8) | |||||
| Model 1 | 1 [Reference] | 1.23 (1.03-1.46) | 1 [Reference] | 1.09 (0.90-1.32) | 1.78 (1.33-2.38) |
| Model 2 | 1 [Reference] | 1.15 (0.97-1.38) | 1 [Reference] | 1.01 (0.83-1.24) | 1.72 (1.27-2.32) |
Abbreviation: OR, odds ratio.
Model 1 adjusted for age, sex, race, field center, education, and military veteran status. Model 2 adjusted for age, sex, race, field center, education, military veteran status, smoking, alcohol consumption, diabetes, depression, and cognitive status.
In secondary analyses, head injury defined by ICD-9 codes was significantly associated with objective anosmia but not subjective olfactory dysfunction or objective hyposmia. Among the head injury cases defined by ICD-9 codes, 397 were of mild severity and 66 were of moderate, severe, or penetrating severity (61 moderate, 1 severe, and 4 penetrating). Individuals with moderate, severe, or penetrating severity injuries were significantly more likely to self-report subjective olfactory dysfunction and to have objective anosmia but not objective hyposmia, compared with individuals with no prior head injury and with individuals with mild injuries (Table 4). In contrast, head injury defined by self-report was not associated with subjective or objective olfactory dysfunction in fully adjusted models (eTable 6 in the Supplement).
Table 4. Associations of ICD-9 Code–Defined (From Hospitalizations, Emergency Department Visits, Outpatient Visits) Head Injury and Head Injury Severity With Subjective and Objective Olfactory Functioninga.
| OR (95% CI) | |||||
|---|---|---|---|---|---|
| No history of ICD-9 code–defined head injury (n = 5488) | History of ICD-9 code–defined head injury (n = 463) | No history of ICD-9 code–defined head injury (n = 5488) | Mild ICD-9 code–defined head injury (n = 397) | Moderate, severe, or penetrating ICD-9 code–defined head injury (n = 66) | |
| Subjective olfactory dysfunction vs no subjective olfactory dysfunction | |||||
| Model 1 | 1 [Reference] | 1.14 (0.91-1.44) | 1 [Reference] | 1.01 (0.78-1.31) | 2.05 (1.23-3.41) |
| Model 2 | 1 [Reference] | 1.13 (0.89-1.42) | 1 [Reference] | 1.00 (0.78-1.30) | 1.94 (1.16-3.24) |
| Objective anosmia (Sniffin’ Sticks score ≤6) vs no anosmia (Sniffin’ Sticks score >6) | |||||
| Model 1 | 1 [Reference] | 1.47 (1.13-1.91) | 1 [Reference] | 1.30 (0.97-1.73) | 2.68 (1.52-4.74) |
| Model 2 | 1 [Reference] | 1.37 (1.05-1.80) | 1 [Reference] | 1.22 (0.90-1.64) | 2.47 (1.37-4.43) |
| Objective hyposmia (Sniffin’ Sticks score 7-8) vs normosmia (Sniffin’ Sticks score >8) | |||||
| Model 1 | 1 [Reference] | 1.05 (0.80-1.39) | 1 [Reference] | 1.01 (0.76-1.36) | 1.35 (0.67-2.72) |
| Model 2 | 1 [Reference] | 0.99 (0.75-1.31) | 1 [Reference] | 0.96 (0.71-1.29) | 1.24 (0.61-2.52) |
| Objective anosmia (Sniffin’ Sticks score ≤6) vs normosmia (Sniffin’ Sticks score >8) | |||||
| Model 1 | 1 [Reference] | 1.49 (1.14-1.96) | 1 [Reference] | 1.30 (0.96-1.76) | 2.92 (1.60-5.33) |
| Model 2 | 1 [Reference] | 1.37 (1.04-1.82) | 1 [Reference] | 1.20 (0.88-1.64) | 2.65 (1.42-4.95) |
Abbreviations: ICD-9, International Classification of Diseases, Ninth Revision; OR, odds ratio.
Model 1 adjusted for age, sex, race, field center, education, and military veteran status. Model 2 adjusted for age, sex, race, field center, education, military veteran status, smoking, alcohol consumption, diabetes, depression, and cognitive status.
Discussion
In this cohort study, we observed an association between remote head injury and both subjective and psychophysical (objective) olfactory dysfunction. This association appears to reflect a threshold effect, as subjective and objective olfactory impairment was observed in participants with (1) multiple prior head injuries but not a single head injury and (2) moderate, severe, or penetrating head injury but not mild head injury. These findings persisted following adjustment for multiple sociodemographic and medical comorbidities. Findings also showed discordance between self-reported perception of olfactory function and objective psychophysical olfactory performance, with greater discordance among individuals with a history of head injury compared with individuals without a history of head injury.
The association between remote head injury and olfactory dysfunction in previous studies has been somewhat mixed. The population-based Epidemiology of Hearing Loss Study found that self-reported head injury was not a significant predictor of psychophysical olfactory impairment in older adults.21 In the National Health and Nutrition Examination Survey, participants with prior head injury reported greater perception of olfactory difficulties than participants without head injury; however, differences in odor identification performance were not statistically significant.22,23 In contrast, head injury was associated with an increased odds of psychophysical olfactory dysfunction in the Olfaction in Catalonia and Beaver Dam Offspring Study cohorts.24,25 Importantly, in these prior studies, head injury was not evaluated as the primary exposure of interest; head injury was just 1 of several predictor variables evaluated without adjustment for potential confounders. The differences observed across epidemiological studies may be partially explained by variability in head injury definition and in olfactory assessment. This heterogeneity in definitions may contribute to the lack of association observed between head injury and hyposmia in the current study; alternatively, it is possible that prior head injury is associated with higher risk for substantial or more complete olfactory impairment, but with similar risk for less complete olfactory impairment.
Meanwhile, an association between head injury severity and olfactory loss has been supported by prior work,26 with multiple prior studies reporting greater olfactory dysfunction among patients with moderate or severe head injury compared with patients with mild head injury or healthy controls, when injury severity was defined using the Glasgow Coma Scale, duration of loss of consciousness, or posttraumatic amnesia.26,27,28,29 Supporting and expanding on this notion, we found that 2 or more prior head injuries was associated with greater objective olfactory dysfunction compared with a single head injury, that moderate, severe, or penetrating head injury was associated with greater subjective and objective olfactory dysfunction compared with mild head injury, and that ICD code–defined but not self-report–defined head injury was associated with objective olfactory dysfunction. Still, other studies have not found an association between these injury severity characteristics and olfactory impairment.30,31,32 Coello et al33 found that the olfactory nerve was the most affected cranial nerve following mild head trauma; however, of the 16 440 cases evaluated, the incidence of olfactory cranial nerve injury was less than 0.001%, suggesting that anosmia from mild head injury is rare. Across 2 studies, Green et al26,34 found that patients with mild head injury had comparable olfactory performance to individuals with orthopedic injuries without head injury, after accounting for cognitive performance. Furthermore, and consistent with our findings, the odds of having olfactory impairment were significantly higher in those with moderate or severe injury compared with mild injury.
The proposed mechanisms for olfactory loss after head injury are multifactorial and include shearing of the olfactory nerve fibers anchored to the bony cribriform plate and mechanical injury of the sinonasal tract, olfactory bulbs, and olfactory-eloquent cortical brain regions.35 Severe depression, posttraumatic epilepsy, and medications prescribed for TBI management may also be associate with the degree of olfactory dysfunction observed.35 Although the current study focused on olfactory functioning in the chronic post–head injury time period, these proposed mechanisms suggest that it will be important to follow patients with TBI over time to investigate olfactory performance in the acute, subacute, and long-term postinjury phases in futures studies. This information will have the potential to inform our understanding of factors associated with persistent or worsening olfactory dysfunction vs recovery, which may inform future treatments for posttraumatic olfactory dysfunction.
Studies examining the frequency with which individuals perceive olfactory loss indicate significant unawareness of smell loss, with false-negative prevalence as high as 78% among older adults.21,36,37,38 In smaller studies of head injury,30,39 36% to 37% of participants with TBI were aware of their dysfunction. This is consistent with the sample in the current study, where we found evidence that individuals with head injury were less likely to have concordance between self-report and objective olfactory identification testing than individuals without head injury. In the current study’s head injury population, we report lower sensitivity and specificity for self-reported olfactory dysfunction compared with objective psychophysical than previously reported.31 These differences may be associated with the older age of the population given evidence that older individuals are less aware of their olfactory dysfunction compared with younger individuals.21,36,37,38 Prior work suggests that the method of subjective assessment may influence concordance in patients with olfactory disorders. For example, subjective assessments of olfaction using a continuous scale were found to produce better concordance rates between subjective and psychophysical assessments.40 Collectively, it appears that olfactory dysfunction may be subjectively underappreciated when objectively present and that olfactory dysfunction may be subjectively overreported when not objectively present following head injury.
Limitations
There are several limitations to this work. First, head injury was defined using self-report and ICD-9 codes. Self-report can reliably assess history of head injury, including history of remote head injuries (even in the presence of mild cognitive impairment or dementia),41 and we used established standards for defining head injury and head injury severity from ICD codes.13,41,42 However, additional clinical information, including the cause of trauma and location of impact, among others, were not available. Second, quantitative assessment of olfactory processing was limited to a single measure of odor identification obtained at the fifth ARIC Study visit, so reverse causality remains a possibility. Additionally, it is important to note that prior work has found that odor identification, detection threshold, and discrimination tests tend to load on 1 broad olfactory domain.43 Third, although the ARIC Study was not originally designed to study head injury or olfaction, it does represent one of the largest and most deeply phenotyped cohorts of cardiovascular health, thus allowing us to comprehensively investigate associations between head injury and olfaction in a community setting.
Conclusions
In this cohort study, findings provide strong inferential support for the association between remote head injury and olfactory dysfunction, particularly in individuals who experienced multiple prior head injuries or individuals with more severe head injury. Findings also suggest important clinical considerations for the diagnosis and treatment of posttraumatic olfactory loss; that individuals with remote prior head injury are at risk for posttraumatic olfactory dysfunction but are unlikely to be aware of their deficits; and conversely, that individuals with prior head injury may be more likely to overreport subjective olfactory deficits, which may not be confirmed by objective testing. Taken together, there should be consideration of objective psychophysical olfactory assessment in patients with head injury; this is particularly important because poor olfaction has previously been associated with multiple negative health outcomes.44
eTable 1. Self-Report Questions and ICD Codes Used to Define Head Injury
eTable 2. ICD Codes Used to Define Head Injury Severity Categories
eTable 3. Associations of Prior Head Injury and Number of Prior Head Injuries with Subjective and Objective Olfactory Functioning Excluding Individuals with Nasal Congestion within 2 Weeks of Testing (n=3,232)
eTable 4. Associations of Prior Head Injury and Number of Prior Head Injuries with Subjective and Objective Olfactory Functioning Excluding Individuals with Prior Sinus Surgery, Nasal Polyps, or Chronic Rhinosinusitis (n=5,724)
eTable 5. Associations of Prior Head Injury and Number of Prior Head Injuries with Subjective and Objective Olfactory Functioning in the Subsample* Selected for the Second Stage of ARIC Visit 5, Excluding Individuals with a History of Parkinson’s Disease or a History of Skull Base/Brain Surgery or Radiation (n=2,623)
eTable 6. Associations of Self-Reported Head Injury and Head Injury Severity with Subjective and Objective Olfactory Functioning
References
- 1.Jackson J. Illustrations of diseases of the nervous system. Lond Hosp Rep. 1864;1:470-471. [Google Scholar]
- 2.Ogle W. Anosmia, or cases illustrating the physiology and pathology of the sense of smell. Med Chir Trans. 1870;53:263-290. doi: 10.1177/095952877005300113 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 3.Leigh AD. Defects of smell after head injury. Lancet. 1943;241(6228):38-40. doi: 10.1016/S0140-6736(00)89072-8 [DOI] [Google Scholar]
- 4.Mifka P. The traumatically caused loss of smell. Article in German. Wien Med Wochenschr. 1964;114:793-796. [PubMed] [Google Scholar]
- 5.Zusho H. Posttraumatic anosmia. Arch Otolaryngol. 1982;108(2):90-92. doi: 10.1001/archotol.1982.00790500026006 [DOI] [PubMed] [Google Scholar]
- 6.Sumner D. Post-Traumatic Anosmia. Brain. 1964;87:107-120. doi: 10.1093/brain/87.1.107 [DOI] [PubMed] [Google Scholar]
- 7.Keller A, Malaspina D. Hidden consequences of olfactory dysfunction: a patient report series. BMC Ear Nose Throat Disord. 2013;13(1):8. doi: 10.1186/1472-6815-13-8 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 8.Costanzo RMZN. Head trauma. In: Getchell TV, Doty RLBL, Snow JB Jr, eds. Smell and Taste in Health and Disease. Raven Press; 1991:711-730. [Google Scholar]
- 9.Costanzo RMRR, Yelverton JC. Smell and taste. In: Zasler NDKD, Zafonte RD, eds. Brain Injury Medicine: Principles and Practice. Demos; 2012:794-808. doi: 10.1891/9781617050572.0048 [DOI] [Google Scholar]
- 10.Schofield PW, Moore TM, Gardner A. Traumatic brain injury and olfaction: a systematic review. Front Neurol. 2014;5:5. doi: 10.3389/fneur.2014.00005 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 11.The ARIC Investigators . The Atherosclerosis Risk in Communities (ARIC) Study: design and objectives. Am J Epidemiol. 1989;129(4):687-702. doi: 10.1093/oxfordjournals.aje.a115184 [DOI] [PubMed] [Google Scholar]
- 12.Wright JD, Folsom AR, Coresh J, et al. The ARIC (Atherosclerosis Risk In Communities) Study: JACC Focus Seminar 3/8. J Am Coll Cardiol. 2021;77(23):2939-2959. doi: 10.1016/j.jacc.2021.04.035 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 13.Langlois JA, Kegler SR, Butler JA, et al. Traumatic brain injury-related hospital discharges: results from a 14-state surveillance system, 1997. MMWR Surveill Summ. 2003;52(4):1-20. [PubMed] [Google Scholar]
- 14.Traumatic Brain Injury Center of Excellence . DOD TBI Worldwide Numbers. Accessed June 15, 2022. https://health.mil/Military-Health-Topics/Centers-of-Excellence/Traumatic-Brain-Injury-Center-of-Excellence/DOD-TBI-Worldwide-Numbers
- 15.Schneider ALC, Gottesman RF, Krauss GL, et al. Association of head injury with late-onset epilepsy: results from the Atherosclerosis Risk in Communities cohort. Neurology. 2022;98(8):e808-e817. doi: 10.1212/WNL.0000000000013214 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 16.Schneider ALC, Selvin E, Latour L, et al. Head injury and 25-year risk of dementia. Alzheimers Dement. 2021;17(9):1432-1441. doi: 10.1002/alz.12315 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 17.Schneider ALC, Selvin E, Liang M, et al. Association of head injury with brain amyloid deposition: the ARIC-PET study. J Neurotrauma. 2019;36(17):2549-2557. doi: 10.1089/neu.2018.6213 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 18.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. doi: 10.1093/chemse/22.1.39 [DOI] [PubMed] [Google Scholar]
- 19.Knopman DS, Gottesman RF, Sharrett AR, et al. Mild cognitive impairment and dementia prevalence: the Atherosclerosis Risk in Communities Neurocognitive Study (ARIC-NCS). Alzheimers Dement (Amst). 2016;2:1-11. doi: 10.1016/j.dadm.2015.12.002 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 20.Kohout FJ, Berkman LF, Evans DA, Cornoni-Huntley J. Two shorter forms of the CES-D (Center for Epidemiological Studies Depression) depression symptoms index. J Aging Health. 1993;5(2):179-193. doi: 10.1177/089826439300500202 [DOI] [PubMed] [Google Scholar]
- 21.Murphy C, Schubert CR, Cruickshanks KJ, Klein BE, Klein R, Nondahl DM. Prevalence of olfactory impairment in older adults. JAMA. 2002;288(18):2307-2312. doi: 10.1001/jama.288.18.2307 [DOI] [PubMed] [Google Scholar]
- 22.Hoffman HJ, Rawal S, Li CM, Duffy VB. New chemosensory component in the US National Health and Nutrition Examination Survey (NHANES): first-year results for measured olfactory dysfunction. Rev Endocr Metab Disord. 2016;17(2):221-240. doi: 10.1007/s11154-016-9364-1 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 23.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. doi: 10.1093/chemse/bjv057 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 24.Mullol J, Alobid I, Mariño-Sánchez F, 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):e001256. doi: 10.1136/bmjopen-2012-001256 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 25.Schubert CR, Cruickshanks KJ, Fischer ME, et al. Olfactory impairment in an adult population: the Beaver Dam Offspring Study. Chem Senses. 2012;37(4):325-334. doi: 10.1093/chemse/bjr102 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 26.Green P, Rohling ML, Iverson GL, Gervais RO. Relationships between olfactory discrimination and head injury severity. Brain Inj. 2003;17(6):479-496. doi: 10.1080/0269905031000070242 [DOI] [PubMed] [Google Scholar]
- 27.Levin HS, High WM, Eisenberg HM. Impairment of olfactory recognition after closed head injury. Brain. 1985;108(Pt 3):579-591. doi: 10.1093/brain/108.3.579 [DOI] [PubMed] [Google Scholar]
- 28.Fujiwara E, Schwartz ML, Gao F, Black SE, Levine B. Ventral frontal cortex functions and quantified MRI in traumatic brain injury. Neuropsychologia. 2008;46(2):461-474. doi: 10.1016/j.neuropsychologia.2007.08.027 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 29.Yamaki T, Oka N, Odaki M, Kobayashi S. Usability of intravenous thiamine injection test compared with odor stick identification test for Japanese patients with severe traumatic brain injury. Auris Nasus Larynx. 2020;47(2):233-237. doi: 10.1016/j.anl.2019.07.004 [DOI] [PubMed] [Google Scholar]
- 30.Neumann D, Zupan B, Babbage DR, et al. Affect recognition, empathy, and dysosmia after traumatic brain injury. Arch Phys Med Rehabil. 2012;93(8):1414-1420. doi: 10.1016/j.apmr.2012.03.009 [DOI] [PubMed] [Google Scholar]
- 31.Haxel BR, Grant L, Mackay-Sim A. Olfactory dysfunction after head injury. J Head Trauma Rehabil. 2008;23(6):407-413. doi: 10.1097/01.HTR.0000341437.59627.ec [DOI] [PubMed] [Google Scholar]
- 32.Doty RL, Yousem DM, Pham LT, Kreshak AA, Geckle R, Lee WW. Olfactory dysfunction in patients with head trauma. Arch Neurol. 1997;54(9):1131-1140. doi: 10.1001/archneur.1997.00550210061014 [DOI] [PubMed] [Google Scholar]
- 33.Coello AF, Canals AG, Gonzalez JM, Martín JJ. Cranial nerve injury after minor head trauma. J Neurosurg. 2010;113(3):547-555. doi: 10.3171/2010.6.JNS091620 [DOI] [PubMed] [Google Scholar]
- 34.Green P, Iverson GL. Effects of injury severity and cognitive exaggeration on olfactory deficits in head injury compensation claims. NeuroRehabilitation. 2001;16(4):237-243. doi: 10.3233/NRE-2001-16408 [DOI] [PubMed] [Google Scholar]
- 35.Howell J, Costanzo RM, Reiter ER. Head trauma and olfactory function. World J Otorhinolaryngol Head Neck Surg. 2018;4(1):39-45. doi: 10.1016/j.wjorl.2018.02.001 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 36.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):260-269. doi: 10.1093/arclin/acr019 [DOI] [PubMed] [Google Scholar]
- 37.Nordin S, Monsch AU, Murphy C. Unawareness of smell loss in normal aging and Alzheimer’s disease: discrepancy between self-reported and diagnosed smell sensitivity. J Gerontol B Psychol Sci Soc Sci. 1995;50(4):187-192. doi: 10.1093/geronb/50B.4.P187 [DOI] [PubMed] [Google Scholar]
- 38.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(8):1237-1244. doi: 10.1212/WNL.38.8.1237 [DOI] [PubMed] [Google Scholar]
- 39.Osborne-Crowley K, McDonald S. Hyposmia, not emotion perception, is associated with psychosocial outcome after severe traumatic brain injury. Neuropsychology. 2016;30(7):820-829. doi: 10.1037/neu0000293 [DOI] [PubMed] [Google Scholar]
- 40.Haxel BR, Bertz-Duffy S, Fruth K, Letzel S, Mann WJ, Muttray A. Comparison of subjective olfaction ratings in patients with and without olfactory disorders. J Laryngol Otol. 2012;126(7):692-697. doi: 10.1017/S002221511200076X [DOI] [PubMed] [Google Scholar]
- 41.Wilmoth K, LoBue C, Clem MA, et al. Consistency of traumatic brain injury reporting in older adults with and without cognitive impairment. Clin Neuropsychol. 2018;32(3):524-529. doi: 10.1080/13854046.2017.1378371 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 42.Annest J, Hedegaard H, Chen L, Warner M, Small E. Proposed Framework for Presenting Injury Data Using ICD-10-CM External Cause of Injury Codes. National Center for Injury Prevention and Control, National Center for Health Statistics, Centers for Disease Control and Prevention; 2014. [Google Scholar]
- 43.Doty RL, Smith R, McKeown DA, Raj J. Tests of human olfactory function: principal components analysis suggests that most measure a common source of variance. Percept Psychophys. 1994;56(6):701-707. doi: 10.3758/bf03208363 [DOI] [PubMed] [Google Scholar]
- 44.Liu B, Luo Z, Pinto JM, et al. Relationship between poor olfaction and mortality among community-dwelling older adults: a cohort study. Ann Intern Med. 2019;170(10):673-681. doi: 10.7326/M18-0775 [DOI] [PMC free article] [PubMed] [Google Scholar]
Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Supplementary Materials
eTable 1. Self-Report Questions and ICD Codes Used to Define Head Injury
eTable 2. ICD Codes Used to Define Head Injury Severity Categories
eTable 3. Associations of Prior Head Injury and Number of Prior Head Injuries with Subjective and Objective Olfactory Functioning Excluding Individuals with Nasal Congestion within 2 Weeks of Testing (n=3,232)
eTable 4. Associations of Prior Head Injury and Number of Prior Head Injuries with Subjective and Objective Olfactory Functioning Excluding Individuals with Prior Sinus Surgery, Nasal Polyps, or Chronic Rhinosinusitis (n=5,724)
eTable 5. Associations of Prior Head Injury and Number of Prior Head Injuries with Subjective and Objective Olfactory Functioning in the Subsample* Selected for the Second Stage of ARIC Visit 5, Excluding Individuals with a History of Parkinson’s Disease or a History of Skull Base/Brain Surgery or Radiation (n=2,623)
eTable 6. Associations of Self-Reported Head Injury and Head Injury Severity with Subjective and Objective Olfactory Functioning
