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Olfactory Dysfunction After Minor Head Trauma

A. Ciofalo*, G. Zambetti, M. Fusconi, P. Soldo, A. Greco, M. Romeo, C. Marinelli, G. Macri
Unit of Rhinology, Sense Organs Department, University of Rome “La Sapienza,”
Rome, Italy 00144
*  Corresponding Author: Unit of Rhinology, Sense Organs Department, University of Rome “La Sapienza,” email: andrea.ciofalo@uniroma1.it


ABSTRACT

Smell deficit is commonly due to head trauma which often causes the shearing of the olfactory nerve axons at the ethmoidal cribriform plate level.  Damage to encephalic olfactory structures, however, is also possible. The degree of olfactory function and the influence of age, sex and time since injury are evaluated in patients after trauma.  57 patients with minor head trauma (Glasgow Coma Scale score ≥13) had their medical history reviewed and were given an otorhinolaryngologic examination; a nasal endoscopy; a computerized tomography (CT) scan; a magnetic resonance imaging (MRI); and a smell test to assess odor threshold, discrimination and identification (Sniffin’ Sticks smell test). Imaging did not show any lesions of brain olfactory structures in these patients, but 82.5% of them had anosmia and 12.5% had hyposmia. Females presented a higher means of odor threshold, discrimination and identification than males; young males presented a higher degree of deficit; 60% of the patients were under 40 years of age; and the duration of the smell deficit was reported as occurring from 1 to 288 months in length.  Patients complaining of minor head trauma related to olfactory dysfunction had anosmia prevalently due to the shearing of the filia olfactoria.

Keywords: anosmia, smell test, head trauma

INTRODUCTION

Total, or partial, loss of sense of smell is a common consequence of craniofacial trauma and, in most cases, the deficit is permanent. The mechanisms involved in this pathology often arise from tearing of olfactory fiber at the level of the cribriform plate caused by an abrupt encephalic movement inside the cranial cavity; contusive, or hemorrhagic, repercussions at the olfactory bulb level and the olfactive cerebral areas, and, more rarely, or nasal obstruction caused by trauma which may be incomplete and solved surgically. Partial recovery of the olfactory function has been documented in approximately 1/3 of patients1 although the mechanisms are not known. In these cases partial repair likely occurs between the connection of the olfactory mucous and bulbs, or at the level of the central olfactory pathways. In some cases patients report recovery characterized by dysosmia, an altered qualitative perception of odors which may depend on an incomplete, or abnormal, central, or peripheral, repair process. In this study we have evaluated epidemiologic data in patients affected by olfactory deficits following minor craniofacial traumas.

METHODS

For the research presented here, 57 patients referred to the ENT Department, Rhinology Unit “La Sapienza,” University of Rome were examined. These patients (21 females (37%) and 36 males) ranged from 16 to 80 years of age and, according to the Glasgow Coma Scale (GCS) score ≥13, all had olfactory deficits following minor head traumas.

All patients underwent anamnesis; and an otorhinolaryngologic examination, which included a nasal endoscopy; and an evaluation of cranial, maxillofacial TC and magnetic resonance imaging (MRI) and of clinical neurological data with reference to the previous traumatic event. Patients were also tested for olfactory performance with the Sniffin’ Sticks method. The test was comprised of 3 subtests which evaluated the olfactory threshold, discrimination and identification. The sum of the values represented the final result defined as Threshold, Discrimination Identification (TDI)[2]. Data were elaborated with SPSS statistical software through an analysis of the frequency distributions of the olfactory performance test responses, and by evaluating the possible associations of the variables, in order to understand which of these mainly influence the occurrence of the phenomenon.

RESULTS

Post-trauma TC and MRI evaluation did not show any facial or encephalic lesions, including the olfactory cleft. During anamnesis, none of the patients reported a post-traumatic nasal obstruction, nor did we observe nasal passage obstruction due to post-traumatic damage of mucosa, or of osteocartilaginous structures of the nose, by presence of nasal polyps, or rhinosinusitis mucopurulent secretion. The Sniffin’ Sticks test revealed hyposmia in 10 cases (17.5%) with a TDI index ranging from >15 to ≤30 (5 males, 5 females), and anosmia in 47 cases (82.5%) with a TDI index ≤15 (31 males, 16 females) (Table 1). Score analysis of the 3 subtests showed a mean value of 0.9 for the Threshold (males: 0.6, females: 1.6; normal value: >7.5; Standard Deviation: 2.7) (Table 2). Discrimination mean values were 3.4 (males: 3.3; females: 3.4; normal value: >12.5; Standard Deviation: 3.9) (Table 3). Identification value was 4.8 (males: 4.5, females: 5.2; normal value: >13.5; Standard Deviation: 2.9) (Table 4). 

Table 1:  Absolute, and percentage, frequencies of patients based on gender and degree of olfactory deficit. 

 

 

Anosmia TDI: ≤15

Hyposmia TDI:16 ≤ 30

Total

Males

 

31 (86.1%)

5 (13.9%)

36 (100%)

Females

 

16 (76.2%)

5 (23.8%)

21 (100%)

Total

 

47 (82.5%)

10 (17.5%)

57 (100%)

 

Patients were divided into 3 groups based on age: ≤40, 41-60, >60. Respectively, the 3 groups were composed of 34 patients (60%: 25 males, 9 females), 18 patients (31%: 7 males, 11 females), and 5 patients (9%: 4 males, 1 female) (Figure 1). The duration of the deficit reported by the patients went from a minimum of 1 to a maximum of 288 months and, when distributing the patients in quartiles, 16 patients (28%) had been experiencing olfactory deficits for less than 6 months, 19 (33.5%) for 6 to 12 months, 10 (17.5%) for 12 to 24 months, and 12 (21%) for over 24 months (Figure 2).

Table 2:Absolute, and percentage, frequencies of patients for the olfactory threshold subtest.

 

Threshold

Females 21(100%)

Males 36(100%)

Total 57(100%)

 

Total Mean =  0.9

SD = 2.7

 

Female Mean = 1.5

Male Mean = 0.6

0

16 (76.2%)

29 (80.5%)

45 (78.9%)

0,5

0

2 (5.5%)

2 (3.5%)

0,75

0

2 (5.5%)

2 (3.5%)

2,75

0

1 (2.8%)

1 (1.8%)

3

2 (9.5%)

1 (2.8%)

3 (5.3%)

6

1 (4.7%)

0

1 (1.8%)

7

1 (4.7%)

0

1 (1.8%)

12

0

1 (2.8%)

1 (1.8%)

14

1(4.7%)

0

1 (1.8%)

 

Table 3: Absolute, and percentage, frequencies of patients for the olfactory discrimination subtest.

 

Discrimination

Females

21(100%)

Males 36(100%)

Total 57(100%)

 

 

 

 

 

  Total Mean = 3.8

SD = 3.9

 

Female Mean = 3.4

Male Mean = 3.3

 

0

11 (52.4%)

16 (44.4%)

27 (47.4%)

1

0

3 (8.3%)

3 (5.3%)

2

0

1(2.8%)

1(1.8%)

3

1 (4.7%)

0

1(1.8%)

4

1 (4.7%)

2 (5.5%)

3 (5.3%)

5

2 (9.5%)

0

2 (3.5%)

6

1 (4.7%)

5 (13.9%)

6 (10.5%)

7

2 (9.5%)

4 (11.1%)

6 (10.5%)

8

0

2 (5.5%)

2 (3.5%)

9

1 (4.7%)

1 (2.8%)

2 (3.5%)

11

1 (4.7%)

1 (2.8%)

2 (3.5%)

12

0

1 (2.8%)

1(1.8%)

15

1 (4.7%)

0

1(1.8%)

 

Table 4:  Absolute, and percentage, frequencies of patients for the olfactory discrimination subtest.

 

Identification

Females 21(100%)

Males 36(100%)

Total 57(100%)

 

 

 

 

Total Mean = 4.8

SD = 2.9

 

Female Mean = 5.2

Male Mean = 4.5

0

0

1 (2.8%)

1 (1.8%)

1

2 (9.5%)

2 (5.5%)

4 (7.0%)

2

3 (14.3%)

5 (13.9%)

8 (14.0%)

3

2 (9.5%)

5 (13.9%)

7 (12.3%)

4

2 (9.5%)

9 (25%)

11 (19.3%)

5

3 (14.3%)

5 (13.9%)

8 (14.0%)

6

3 (14.3%)

2 (5.5%)

5 (8.8%)

7

2 (9.5%)

2 (5.5%)

4 (7.0%)

8

0

2 (5.5%)

2 (3.5%)

9

2 (9.5%)

2 (5.5%)

4 (7.0%)

10

1 (4.7%)

0

1 (1.8%)

12

1 (4.7%)

0

1 (1.8%)

15

0

1 (2.8%)

1 (1.8%)

 

 

 

 

 

Figure 1: Age and gender patient distribution

 


 

 

 

 

 

 

 

 

 

 

Figure 2: Patient distribution in relation to olfactory deficit duration in months.

DISCUSSION

The olfactory organ originates at the neuroepithelium which is located in the nasal passage vault. Because of the specific membrane receptors, the bipolar sensorial cells bind external odor molecules and transmit signals through axons which, when crossing the ethmoid lamina cribrosa, form bulb synapses with glomerular mitral cells.

One of the major causes of olfactory sensitivity deficit after minor head trauma is damage to “filia olfactoria” in the passageway across the lamina cribrosa due to sudden and excessive traction. Other, or concomitant, cerebral lesions may occur in frontal traumas, especially in occipital ones3 due to consequent contusions, or hemorrhaging of olfactory bulbs, or cerebral areas designed for olfactory sensorial elaboration, such as the amygdala, the temporal lobe and the anterior pyriform cortex [4]. Haxel[5] found a correlation between olfactory dysfunction and the appearance of skull base fractures, and that intracranial hemorrhage, or hematoma, and odor-evoked potentials indicate that functional anosmia can occur even when there is some evidence of intact olfactory nerve function. De Kruijk [6] did not find a statistically significant correlation between the immediate increase of S-100B and neuron-specific enolase (NSE) proteins, known as outcome predictors in head injuries and permanent olfactory dysfunction, 2 weeks after minor head trauma.

The patients in this study presented a ≥13 GCS score. MRI and CT imaging did not show maxillofacial or encephalic structure, alterations. When undergoing the olfactory test, however, 82.5% showed anosmia, suggesting axon damage at the level of the lamina cribrosa. The subtest results indicated that the mean values were significantly lower than normal, especially as far as the threshold was concerned.  This suggested a prevalent quantitative injury of the axons. Subsequently, these lesions cause neuroepithelial cell death due to caspase-3 apoptosis enzyme activation [7].

TDI mean values were higher in females than in males and also showed fewer cases of anosmia among the female patients than in males (76.2% and 86.15, respectively). This finding can be explained by the higher olfactory sensitivity in females, due to a probable protective effect played by estrogen hormones on the neuroepithelium, as well as on the olfactory structures, even when damaged.

Doty [8] reported 268 cases with post-trauma olfactory deficit in which, with MRI imaging, only the males showed a volumetric reduction of olfactory bulbs compared to normal subjects. Deems [9] stressed the importance of the protective role of estrogens in a report where out of 99 females in menopause with olfactory deficit, and with various etiologies arising after menopause, only 4% were undergoing estrogen therapy. 

As far as age groups were concerned, the highest percentage of patients was under 40 years of age (60%) and was mostly males, whereas the lowest percentage of patients were over 60 (9%). This finding is supported by other studies and is likely due to a greater incidence of on-the-job, or car, accidents in younger age group[10]. 

When considering the duration of symptoms, only 28% of patients reported noticing the olfactory deficit less than 6 months before. The up-to 288-month time lapse before undergoing olfactory examinations may be due to the fact that some patients gave priority to other forms of rehabilitation for other injuries, caused by the same traumatic event, that were more serious and disabling. This long duration period may have also depended on the physician’s prediction of an eventual long-term spontaneous recovery.

There are no standard therapeutic protocols for the treatment of cranial post-trauma olfactory deficits.  Fujii [10], however, reported an improvement of hyposmia in some cases by applying local steroid injections immediately after trauma. In our study approximately 40% of the patients reported a persistent partial, or total, olfactory deficit for over 12 months after trauma, thus confirming a high-grade irreversibility of neurologic damage.

Craniofacial traumas, including mild ones, represent one of the major etiologic causes of olfactory deficits. The pathogenetic mechanism is mainly due to axon damage of neuroepithelial cells present in the nasal mucosa and to contusive lesions of the central olfactory structures. These lesions cause anosmia in over 80% of patients. Olfactory performance tests showed more limited deficits in females than in males. The post-traumatic olfactory sensorial reduction is often irreversible, but may, nevertheless, be evaluated and monitored with olfactory tests.

ACKNOWLEDGEMENT

CITATIONS AND REFERENCE LIST

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