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 » Introduction
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ORIGINAL ARTICLE
Year : 2013  |  Volume : 61  |  Issue : 4  |  Page : 365-370

Use of Indian smell identification test for evaluating olfaction in idiopathic Parkinson's disease patients in India


Department of Neurology, All India Institute of Medical Sciences, New Delhi, India

Date of Submission01-Apr-2013
Date of Decision24-Apr-2013
Date of Acceptance24-Jul-2013
Date of Web Publication4-Sep-2013

Correspondence Address:
Madhuri Behari
Room No. 702, Department of Neurology, Neurosciences Centre, AIIMS, New Delhi
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/0028-3886.117598

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 » Abstract 

Background: Olfactory dysfunction in Parkinson's Disease (PD) has been recognized for a long time and a number of studies have been performed in various parts of the world, using culturally appropriate smell identification tests. Objective: In this study, for the first time, olfactory function has been assessed in the Indian Idiopathic Parkinson's Disease (IPD) patients using an indigenously developed smell test. Materials and Methods: Olfaction was assessed in 53 IPD patients and 50 healthy controls using SniffIn-sticks ® test and Indian Smell Identification test (INSIT). In both these tests, the subjects were asked to identify the smell from a set of choices and were scored out of 10 and 12 for INSIT and SniffIn-sticks ® test, respectively. Results: Both SniffIn-sticks ® test and INSIT showed significant impairment in olfaction in IPD patients (P < 0.001). There was no significant correlation of the scores of both tests with Hoehn and Yahr (H and Y) stage, duration of illness and Levodopa Equivalent Daily Dose (LEDD). The tests had a high correlation, r = 0.75 (P < 0.001) and the area under the Receiver Operating Characteristic (ROC) curves did not differ significantly. Using a cut off value of 4 (values ≤ 4 indicating disease), INSIT showed a sensitivity of 79.2% and specificity of 78%. Conclusion: INSIT, being cheap, convenient and more acceptable in the Indian population, can be considered as a better alternative for SniffIn-sticks ® test in the evaluation of olfaction in Indian PD subjects.


Keywords: Indian smell test, olfaction, Parkinson′s disease, SniffIn test


How to cite this article:
George J, Jose T, Behari M. Use of Indian smell identification test for evaluating olfaction in idiopathic Parkinson's disease patients in India. Neurol India 2013;61:365-70

How to cite this URL:
George J, Jose T, Behari M. Use of Indian smell identification test for evaluating olfaction in idiopathic Parkinson's disease patients in India. Neurol India [serial online] 2013 [cited 2018 Dec 12];61:365-70. Available from: http://www.neurologyindia.com/text.asp?2013/61/4/365/117598



 » Introduction Top


Although Parkinson's Disease (PD) is predominantly a motor disorder, nonmotor symptoms are major determinant of quality of life in patients with PD. Some of these are premotor in appearance and may predate motor symptoms by several years. These include: Olfactory function, constipation, rapid eye movement (REM) sleep behavior disorder (RBD), depression, and others. [1],[2] Since Ansari and Johnson reported in 1975 impaired olfaction in PD patients, a number of other studies have been conducted from all around the world in the past two decades demonstrating olfactory dysfunction in PD. [3],[4],[5],[6],[7] Haehner et al. reported prevalence of olfactory impairment in 74.5% of PD patients when adjusted with age-related controls. [8] The impairment occurs many years before the onset of motor symptoms and may serve as a screening tool for people at risk. [9] These studies have used different smell kits based on cultural and regional differences. [10],[11],[12],[13],[14],[15] Various tests address different components of olfaction like threshold, discrimination, and identification. Of the various olfactory testing kits available, the University of Pennsylvania Smell Identification Test (UPSIT) [16],[17] and SniffIn-sticks [18] are the most popular and widely used for screening olfaction in idiopathic PD patients. [19],[20] In India no study has been conducted yet to test the olfaction in PD patients. Since the odorants in the SniffIn-stick as well as other similar tests were developed in other parts of the world, these odorants are mostly unfamiliar to Indian subjects. Keeping this in mind, we assessed the olfactory impairment in patients with IPD using a 12-odorant SniffIn-sticks ® and a 10-odourant Indian Smell Identification Test (INSIT) and the agreement between the two tests was studied.


 » Materials and Methods Top


Patients with IPD diagnosed on the basis of UKPDS Brain Bank Clinical Diagnostic Criteria [21] attending the Movement Disorders Clinic of a tertiary care teaching hospital in India were included in the study. All patients were diagnosed clinically by a neurologist specialized in Movement Disorders.

All consecutive nondemented IPD patients irrespective of age, gender, and duration or stage of disease were included in the study after Institute Review Board/Ethics Committee (IRB/EC) approval and informed consent. IPD patients with history or evidence of head injury, intracranial tumor, dementia (DSM-IVR), nasal polyps, deviated nasal septum, viral infection (within 1 week), chronic sinusitis, smoking, upper respiratory tract infections (within 1 week), exposure to drugs, which may alter olfaction, were excluded from the study. Clinical and demographic details were recorded on a pretested format. Fifty-three PD patients, mean age of 58.5 ± 13.1 years (range: 30-85), males 71.7%, with mean duration of disease 7.1 ± 4.9 years, of Hoehn and Yahr (H and Y) stages I-V after local, general, and neurological examination, were tested in the on-state of medication. A control group of 50 unrelated healthy individuals (male 62%; female 38%) were selected from individuals who accompanied the patients, with similar exclusion criteria.

Tests were carried out in a quiet, well ventilated room. Clinical and demographic details were recorded on a pretested format. Levodopa equivalent daily dose (LEDD) was calculated as described by Claire et al. [22] and staging was done using the Modified Hoehn and Yahr scale. [23],[24] Individuals were instructed about the test method.

SniffIn-sticks ® Smell Test (SS): The 12 odorants in the SniffIn-sticks ® test are Orange, Leather, Cinnamon, Peppermint, Banana, Lemon, Liquorice, Coffee, Cloves, Pineapple, Rose, and Fish. The sticks were placed 1 cm from one nostril and the patient was asked to inhale with the other nostril closed and the test repeated in the other nostril. The subjects were asked to identify the correct smell, from a set of four choices for each item, from an answer card. First response was taken and scored 1 for correct and 0 for wrong answer.

Indian Smell Identification Test: Essence of 10 commonly used items were used as odorants. The odorants were chosen to represent the familiarity in day to day life. The essence of cardamom, kewra, khus, lemon, mango, orange, pineapple, rose, thinner, vanilla in 20 ml air tight bottles commercially available were used. Cotton buds dipped in the essence were used as test material, which were placed 1 cm in front of the nostril with the other closed and repeated in the other. The subject was asked to sniff and identify the smell from the answer card containing four choices for each odorant. First response was taken and scored 1 for correct and 0 for wrong response.

For SniffIn-sticks ® test the maximum score was 12 and for INSIT it was 10. The total score was the sum of both the scores (out of 22). Pearson's correlation test was used to determine the agreement between the tests, while Students t-test was used to compare the mean scores in the patient and control groups. Receiver Operating Characteristic (ROC) curve was used to calculate the sensitivity and specificity. The effect of stage, LEDD and duration of illness on the test scores were evaluated with linear regression analysis.


 » Results Top


Fifty-three IPD patients and 50 controls were included in the study. IPD and control groups were not significantly different with respect to age and gender. The mean age for the IPD and control group was 58.5 ± 13.1 years and 55.8 ± 7.4 years, respectively. Most of the participants were males, 71.7% and 62%in the patient and control group, respectively. The patients had the illness for a mean duration of 7.1 years, ranging from 6 months to 20 years. The mean LEDD of the patients, calculated for medications at the time of study, was 626.43 mg. According to modified H and Y staging, 9 patients were in stage 1, 8 in stage 1.5, 4 in stage 2, and 13 and 12, respectively, in stage 2.5 and 3. Five patients were in stage 4 and two in stage 5. The characteristics of the study subjects are summarized in [Table 1].
Table 1: Characteristics of study subjects

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The difference in score between PD and controls was significant using both SniffIn-sticks ® and Indian smells (both P < 0.001). Correlation between stage, duration of illness, LEDD with smell were tested using linear regression and the results are given in [Table 2]. None of these parameters showed any significant correlation with either SniffIn score or INSIT score. ROC curve was plotted for INSIT and SniffIn-sticks ® test to determine the ability of these tests to differentiate between the control and patient groups. Both the tests had comparable area under the ROC curves -0.836 and 0.865 for SniffIn-sticks ® test and INSIT, respectively. These results are summarized in [Table 2].
Table 2: Comparison between Sniffin‑stick® and Indian smell identification test

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The SniffIn-sticks ® test scores versus INSIT scores for each subject in both control and IPD group is plotted in [Figure 1]. Using Pearson's correlation the scores of both the tests for the control and IPD groups combined showed a correlation coefficient r = 0.75, P < 0.001.
Figure 1: Scatter plot for INSIT and SniffIn-sticks® scores. The scores obtained by each individual (cross representing control subjects and diamond representing patients) using both the tests are plotted. Pearson correlation r=0.75 (P<0.001)

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The percentage correct responses for each of these 10 items in both the control as well as the IPD group are given in [Figure 2]. Thinner had the highest percentage of correct response, 92% in control group and 68% in IPD group. The lowest response rate was with mango and orange among control and IPD groups, respectively. The odorant with the best discriminative ability was vanilla in our study. Also for each of these odorants ROC curves were plotted separately and their area under the curve along with P value are reported in [Table 3]. Except cardamom and mango all the odorants showed a significant ability to differentiate between the IPD and control groups.
Table 3: Odorant specific characteristics

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Figure 2: Percentage of correct responses for each item in Indian smell identification test

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 » Discussion Top


Olfaction is a primitive sense and its importance is underestimated in clinical practice. In the current study, the smell identification ability of the Indian IPD patients has been assessed using a new olfactory test, INSIT and the test has been compared with commercially available and validated 12 odorant SniffIn-sticks ® test. The mean smell identification score using INSIT was 2.92 in patients and 5.4 in the control group. The mean smell identification score using SniffIn-sticks ® test was 4.15 in patients and 7.58 in the control group. Similarly, the mean combined (SS + INSIT) score for control and IPD group was 13.2 and 7.07, respectively. Significant differences in scores were seen among IPD and control group with INSIT, SniffIn-sticks ® and combined scores (for all, P < 0.001). This clearly shows that olfaction is impaired in PD as previously reported. [3],[4],[5],[6],[7] Both the SniffIn-sticks test as well as INSIT was able to detect olfactory impairment in IPD patients.

The effect of H and Y stage, duration of disease, LEDD on smell identification scores did not show any significant correlation with either SniffIn-sticks ® test or INSIT scores on regression analysis. These results are in agreement with previous studies. [25],[26] These findings indicate that the olfactory dysfunction occurs much early in the course of the disease and remains largely unchanged as the disease progresses. Braak et al. had shown that olfactory neuronal loss (anterior olfactory nucleus) occurs much early in the course of the disease even before the involvement of various motor areas. [27],[28] Since the H and Y staging is largely based on motor symptoms the olfaction need not alter as the staging severity increases as evident from the current study. The early loss of olfactory neurons also explains the early appearance of the olfactory impairment.

The scores obtained using INSIT showed a significant correlation with scores obtained using SniffIn-sticks ® tests (r = 0.75, P < 0.001). The significant correlation between SniffIn-sticks ® test and INSIT proves that INSIT can be used as a validated tool for testing olfactory dysfunction. Area under ROC curves for the SniffIn-sticks ® test (0.835) and INSIT (0.859) were not significantly different (P = 0.166) indicating perfect agreement. This indicates that both the tests are comparable in terms of correctly identifying the diseased and healthy subjects.

Using INSIT, in the control group the percentage of correct identification ranged from 92% (thinner) to 34% (mango) while in the IPD group it ranged from 67.9% (thinner) to 7.5% (orange). Better positive response with thinner may be due to the high intensity of the smell of thinner or it being particularly different from the rest, might appear as an odd one among the choices. The discriminative ability of each odorant in the INSIT was calculated using ROC and this showed that 8 out of 10 odorants had significantly high discriminative ability. Among the odorants, vanilla showed highest discriminative ability with area of 0.688 under the ROC curve and mango showed least discrimination with area 0.576. Cardamom and mango were the two smells in the INSIT, which did not show significant discrimination between IPD and control group.

The maximum specificity and sensitivity for INSIT was obtained when a cut off value of 4 was used, that is, values ≤4 indicating disease. Using a cut off value of 4, we obtained a sensitivity of 79.2% and specificity of 78% in our study. Deep et al. showed that a basic smell test is as effective as Dopamine Transporter Scan in the diagnosis of PD. [29] They reported that the sensitivity of UPSIT (86%) was not significantly different from that of the DaTSCAN (92%). So a good olfactory test could become a cornerstone in the early diagnosis of PD. Maremmani et al. using a 33-item olfactory multiple-choice test (Italian Olfactory Identification Test; IOIT) in Italian healthy subjects and PD patients described sensitivity of 93% and specificity of 99% while Millar et al. observed sensitivity of 70% (60-81%) and a specificity of 85% (65-100%) in Argentinean population using a hyposmia rating scale. [10],[30] An improvement in the sensitivity and specificity of INSIT with appropriate modifications can be made possible with further studies.

Since the odorants used for INSIT in the study were purchased from the market and their intensities over time or batch to batch are likely to change/decay, reproducibility needs to be studied. No decline in the scores was noted during the time course (8 weeks) of the study for both Sniffin-sticks ® as well as Indian smells, though it was a short period. Hence, further studies may be required to determine the test-retest reliability of INSIT. Hence any center using this test in India as a clinical diagnostic tool in PD, may need to determine test-retest reliability of the test kit if the test is done more than 8-12 weeks after opening the seal of the odorant.

Since olfactory dysfunction is reported in other neurological diseases, it becomes difficult to have high specificity for IPD using olfactory test alone. [31],[32] It should be noted that ability of INSIT to differentiate between IPD and other  Parkinsonism More Details syndromes was not evaluated in this study. The sensitivity and specificity mentioned were calculated from the study population, which did not include patients with other Parkinsonism plus diseases and other neuro-degenerative disorders. McKinnon et al. demonstrated sensitivity of 77% and specificity of 85% for UPSIT to differentiate IPD from other Parkinsonism plus syndromes. [33] Wenning et al. reported severely impaired olfaction in IPD patients while patients with atypical Parkinsonism such as Multiple System Atrophy (MSA), Progressive Supranuclear Palsy (PSP), or Corticobasal Degeneration (CBD) have preserved or only mildly impaired olfaction. [34] Hence, it is important to have further studies to test olfaction in other neurological diseases along with IPD using INSIT.

In the present study, only odor identification was assessed. Other components of olfaction like odor threshold and odor discrimination were not studied. Since different components contribute differently to olfaction loss, including other components of olfaction in the smell test will provide a more sensitive and specific way of assessing olfaction in PD patients and improve its discriminative value. [35] In our study it was noted that many patients with IPD were able to detect odorant from SniffIn-sticks ® test but were not able to identify them. This might represent early involvement of olfactory function as part of the disease process or because of unfamiliarity with the odorant. It was observed that a good number of the Indian patients were vegetarians and expressed displeasure when "fish odorant" of Sniffin-sticks ® test was presented to them. This necessitates the need to use cultural specific tests like the ones in INSIT to test olfaction in Indian IPD patients.

In short, our study showed that India Smell Identification Test can predict olfactory function in PD patient with equal sensitivity as SniffIn-sticks ® tests, with strong agreement between the two and, at the same time being cost effective, convenient and acceptable. In view of the cultural variability and low cost it would be better to use INSIT for evaluating olfaction in Indian IPD patients. As mentioned already, further studies are required to determine the clinical utility of INSIT test and its ability to differentiate IPD from other neurodegenerative disorders, decay of the odorant over time, and modify it if necessary.

 
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    Figures

  [Figure 1], [Figure 2]
 
 
    Tables

  [Table 1], [Table 2], [Table 3]

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